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Zhu C, Zhang Y, Pan Y, Zhang Z, Liu Y, Lin X, Cai J, Xiong Z, Pan Y, Nie H. Clinical correlation between intestinal flora profiles and the incidence of postmenopausal osteoporosis. Gynecol Endocrinol 2025; 41:2465587. [PMID: 39949270 DOI: 10.1080/09513590.2025.2465587] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/25/2024] [Revised: 02/03/2025] [Accepted: 02/05/2025] [Indexed: 05/09/2025] Open
Abstract
PURPOSE This study aimed to explore the characteristics of intestinal microflora polymorphism in postmenopausal women, and to determine the pathophysiological changes of gene polymorphism of intestinal flora and bone metabolism in postmenopausal osteoporosis (PMOP) patients. METHODS A total of 104 postmenopausal women with PMOP or normal bone density were included. Lifestyle, hip T-score, bone metabolism indexes (25(OH)D, PTH, β-CTX, PINP), intestinal mucous membrane barrier function (diamine oxidase, D-lactic acid, LPS), gene polymorphisms, and characteristics of gut microbiota were examined. RESULTS Women with PMOP had reduced physical activity, less dietary protein and calcium intake, lower levels of 25(OH)D, hip T-score, and BMD, but PMOP group had increased total energy and fat intake, and higher levels of PTH, β-CTX, diamine oxidase, D-lactic acid, and LPS (p < .05 for all), as compared with normal subjects. Analyses of the α- and β-diversity of fecal microbiota indicated remarkably differences in postmenopausal women with or without PMOP. In details, individuals with PMOP had increased abundances of some genera (e.g. Roseburia and Bacteroides), but decreased abundances of some genera (e.g. Streptococcus and Dorea). Furthermore, use of a random forest model based on differential abundant taxa and ROC analysis could efficiently identify women with PMOP in the present cohort (AUC = 0.93). CONCLUSION The incidence of PMOP was closely associated with fecal microbial compositions and intestinal functional changes. The present findings supported potential applications of gut microbiome analysis for early diagnosis of PMOP, and provided potential therapeutic targets.
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Affiliation(s)
- Cuifeng Zhu
- Shenzhen Hospital, Southern Medical University, Shenzhen, Guangdong Province, China
| | - Yuan Zhang
- Shenzhen Hospital, Southern Medical University, Shenzhen, Guangdong Province, China
| | - Yi Pan
- Hunan Engineering Research Center for Obesity and Metabolic Complications, ChangSha, Hunan Province, China
| | - Zhentian Zhang
- Shenzhen Hospital, Southern Medical University, Shenzhen, Guangdong Province, China
| | - Yan Liu
- Shenzhen Hospital, Southern Medical University, Shenzhen, Guangdong Province, China
| | - Xiuping Lin
- Shenzhen Hospital, Southern Medical University, Shenzhen, Guangdong Province, China
| | - Jinchuan Cai
- Shenzhen Hospital, Southern Medical University, Shenzhen, Guangdong Province, China
| | - Zhuang Xiong
- Yearth Biotechnology Co. Ltd, Changsha, Hunan Province, China
| | - Yong Pan
- Department of Pathophysiology, School of Basic Medical Sciences, Shenzhen University Medical School, Shenzhen, Guangdong Province, China
| | - Hezhongrong Nie
- Shenzhen Hospital, Southern Medical University, Shenzhen, Guangdong Province, China
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Hao S, Sun W, Wei P, Wu H, Lu W, He Y. Supplementation with Rare Earth-Chitosan Chelate Improves Tibia Quality, Disease Resistance Capacity, and Performance in Nursery Pigs. Int J Mol Sci 2025; 26:2409. [PMID: 40141053 PMCID: PMC11942057 DOI: 10.3390/ijms26062409] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/23/2025] [Revised: 02/16/2025] [Accepted: 02/18/2025] [Indexed: 03/28/2025] Open
Abstract
The aim of this study was to investigate the effects on the tibia, liver, and gut, and on performance, when supplementing nursery pigs with different levels of rare earth-chitosan chelate (RECC). A total of 80 piglets, weaned at 7.67 ± 0.09 kg, were randomly assigned to groups RECC0 (RECC, 0 mg/kg diet), RECC200 (RECC, 200 mg/kg diet), RECC400 (RECC, 400 mg/kg diet), and RECC600 (RECC, 600 mg/kg diet), with four replicates in each group and five pigs per replicate during a 28 d experiment. Samples of the left hind tibia, serum, and feces were collected for analysis. The results indicated that, compared to pigs from group RECC0, pigs from group RECC200 presented with the following: a longer trabecular perimeter (p < 0.05), a larger trabecular area (p < 0.01), a higher trabecular number (p < 0.05), a smaller degree of trabecular separation (p < 0.01), and a lower number of osteoclasts (p < 0.01) in the tibia; higher abundances of beneficial fecal bacteria such as g_Prevotellaceae_NK3B31_group, g_UCG_005, g_Rikenellaceae_RC9_gut_group, g_Acetitomaculum, g_Glutamicibacter, g_Frisingicoccus, and g_Alistipes; higher (p < 0.01) serum levels of IgM, IgA, IgG, and IL-10; a lower (p < 0.01) serum concentration of TNF-α; a higher (p < 0.05) average daily gain and feed conversion ratio; and a lower (p < 0.01) incidence of diarrhea. The dietary addition of RECC contributes to improvements in tibia quality, gut health, and performance in nursery pigs.
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Affiliation(s)
- Shaobin Hao
- Jiangxi Province Key Laboratory of Animal Nutrition and Feed, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, China; (S.H.); (W.S.); (P.W.); (W.L.)
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China;
| | - Wenchen Sun
- Jiangxi Province Key Laboratory of Animal Nutrition and Feed, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, China; (S.H.); (W.S.); (P.W.); (W.L.)
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China;
| | - Panting Wei
- Jiangxi Province Key Laboratory of Animal Nutrition and Feed, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, China; (S.H.); (W.S.); (P.W.); (W.L.)
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China;
| | - Huadong Wu
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China;
| | - Wei Lu
- Jiangxi Province Key Laboratory of Animal Nutrition and Feed, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, China; (S.H.); (W.S.); (P.W.); (W.L.)
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China;
| | - Yuyong He
- Jiangxi Province Key Laboratory of Animal Nutrition and Feed, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, China; (S.H.); (W.S.); (P.W.); (W.L.)
- College of Animal Science and Technology, Jiangxi Agricultural University, Nanchang 330045, China;
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Papa V, Li Pomi F, Minciullo PL, Borgia F, Gangemi S. Skin Disorders and Osteoporosis: Unraveling the Interplay Between Vitamin D, Microbiota, and Epigenetics Within the Skin-Bone Axis. Int J Mol Sci 2024; 26:179. [PMID: 39796035 PMCID: PMC11720247 DOI: 10.3390/ijms26010179] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/04/2024] [Revised: 12/24/2024] [Accepted: 12/26/2024] [Indexed: 01/13/2025] Open
Abstract
Growing scientific evidence suggests a strong interconnection between inflammatory skin diseases and osteoporosis (OP), a systemic condition characterized by decreased bone density and structural fragility. These conditions seem to share common pathophysiological mechanisms, including immune dysregulation, chronic inflammation, and vitamin D deficiency, which play a crucial role in both skin and bone health. Additionally, the roles of gut microbiota (GM) and epigenetic regulation via microRNAs (miRNAs) emerge as key elements influencing the progression of both conditions. This review aims to examine the skin-bone axis, exploring how factors such as vitamin D, GM, and miRNAs interact in a subtle pathophysiological interplay driving skin inflammation and immune-metabolic bone alterations. Recent research suggests that combined therapeutic approaches-including vitamin D supplementation, targeted microbiota interventions, and miRNA-based therapies-could be promising strategies for managing comorbid inflammatory skin diseases and OP. This perspective highlights the need for multidisciplinary approaches in the clinical management of conditions related to the skin-bone axis.
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Affiliation(s)
- Vincenzo Papa
- Department of Clinical and Experimental Medicine, School and Operative Unit of Allergy and Clinical Immunology, University of Messina, 98125 Messina, Italy; (V.P.); (S.G.)
| | - Federica Li Pomi
- Department of Precision Medicine in Medical, Surgical and Critical Care (Me.Pre.C.C.), University of Palermo, 90127 Palermo, Italy;
| | - Paola Lucia Minciullo
- Department of Clinical and Experimental Medicine, School and Operative Unit of Allergy and Clinical Immunology, University of Messina, 98125 Messina, Italy; (V.P.); (S.G.)
| | - Francesco Borgia
- Department of Clinical and Experimental Medicine, Section of Dermatology, University of Messina, 98125 Messina, Italy;
| | - Sebastiano Gangemi
- Department of Clinical and Experimental Medicine, School and Operative Unit of Allergy and Clinical Immunology, University of Messina, 98125 Messina, Italy; (V.P.); (S.G.)
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Lei H, Liu J, Deng J, Zou P, Zou Z, Li Z, Li H, Luo L, Tan Z. Behavior, hormone, and gut microbiota change by YYNS intervention in an OVX mouse model. Front Cell Infect Microbiol 2024; 14:1445741. [PMID: 39575307 PMCID: PMC11580528 DOI: 10.3389/fcimb.2024.1445741] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/08/2024] [Accepted: 10/08/2024] [Indexed: 11/24/2024] Open
Abstract
OBJECT Perimenopause depression disorder (PDD) is a very common problem in clinical practice and is characterized by depression and autonomic nervous symptoms, including hot flashes, palpitation, and night sweating. In addition, the comorbidity of menopause depression has long been an integral component of the estradiol (E2) shortage. Previous studies have suggested that the mechanisms underlying this comorbidity involved overlap of endocrine and cerebellar networks. Emerging evidence has shown that the endocrine-brain-gut-microbiota axis plays a key role in the regulation of affective disorders. Yangyin-ningshen formula (YYNS) is a traditional Chinese decoction tailored by Yijintang for menopausal depression intervention. Thus, we hypothesized that the YYNS may be involved in the menopause depression alleviation through the endocrine-brain-gut-microbiota axis. METHODS To verify this, we constructed a bilateral ovariectomy (OVX) mouse model to simulate menopausal-related depression. Subsequently, behavioral tests including the open field test (OFT) and the forced swimming test (FST) were conducted to examine the depression state post-OVX. With YYNS or E2 intervention, enzyme-linked immunosorbent assay (ELISA) was used to determine the serum sex hormones level. 16S rRNA gene sequencing and liquid chromatography-mass spectrometry (LC-MS) were used to analyze the microbiome of the colon samples collected from mice in the sham surgery group (CSH), the OVX model group (CMD), the OVX with E2 hormone intervention group (CHM), and the OVX with YYNS intervention group (CYYNS). One week after OVX, CMD, CHM, and CYYNS showed depression in OFT, FST. Three weeks post-OVX, CHM and CYYNS showed a notable relief of depression; CMD shaped the OTUs shrinkage; and OTUs were raised in the sham, CHM, and CYYNS group. The CMD group showed that the abundance of Actinobiota decreased but that of Bacteriodia increased. The relative abundance of the genus varied in each group. Moreover, functional correlation of changes in sex hormone and gut microbes between different groups showed that the PRL level was negatively correlated with Odoribacter. T level was positively correlated with Lachnospiraceae NK4A136 group and Odoribacter abundance (p < 0.05). CONCLUSION Our results not only offer novel insights into the sex hormones and depression with OVX mice but also build an important basis for E2 or YYNS therapeutic efficacy on PDD, which provide for future research on this etiology through the endocrine-brain-gut-microbiota network.
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Affiliation(s)
- Huajuan Lei
- Department of Anesthesiology, the First Hospital of Hunan University of Chinese Medicine, Changsha, China
- Department of Chinese Medicine, ChangSha Medical University, Changsha, China
| | - Jian Liu
- Department of Innovation Experiments Center, the First Hospital of Hunan University of Chinese Medicine, Changsha, China
| | - Juan Deng
- Department of Anesthesiology, Changsha Hospital Affiliated with Hunan University of Chinese Medicine, Changsha, China
| | - Pan Zou
- Department of Radiology, the First Hospital of Hunan University of Chinese Medicine, Changsha, China
| | - Zixiang Zou
- Department of Gynaecology, the First Hospital of Hunan University of Chinese Medicine, Changsha, China
| | - Ziou Li
- Department of Radiology, Changsha Hospital Affiliated with Hunan University of Chinese Medicine, Changsha, China
| | - Honghui Li
- Department of Orthopedics, the First Hospital of Hunan University of Chinese Medicine, Changsha, China
| | - Lin Luo
- Department of Medicine, Hunan University of Chinese Medicine, Changsha, China
| | - Zhoujin Tan
- Department of Medicine, Hunan University of Chinese Medicine, Changsha, China
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Ma J, Wang XR, Zhou YX, Zhou WJ, Zhang JN, Sun CY. Navigating the gut-bone axis: The pivotal role of Coprococcus3 in osteoporosis prevention through Mendelian randomization. Medicine (Baltimore) 2024; 103:e38861. [PMID: 39029026 PMCID: PMC11398822 DOI: 10.1097/md.0000000000038861] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/05/2024] [Accepted: 06/18/2024] [Indexed: 07/21/2024] Open
Abstract
Osteoporosis (OP) constitutes a notable public health concern that significantly impacts the skeletal health of the global aging population. Its prevalence is steadily escalating, yet the intricacies of its diagnosis and treatment remain challenging. Recent investigations have illuminated a profound interlink between gut microbiota (GM) and bone metabolism, thereby opening new avenues for probing the causal relationship between GM and OP. Employing Mendelian randomization (MR) as the investigative tool, this study delves into the causal rapport between 211 varieties of GM and OP. The data are culled from genome-wide association studies (GWAS) conducted by the MiBioGen consortium, in tandem with OP genetic data gleaned from the UK Biobank, BioBank Japan Project, and the FinnGen database. A comprehensive repertoire of statistical methodologies, encompassing inverse-variance weighting, weighted median, Simple mode, Weighted mode, and MR-Egger regression techniques, was adroitly harnessed for meticulous analysis. The discernment emerged that the genus Coprococcus3 is inversely associated with OP, potentially serving as a deterrent against its onset. Additionally, 21 other gut microbial species exhibited a positive correlation with OP, potentially accentuating its proclivity and progression. Subsequent to rigorous scrutiny via heterogeneity and sensitivity analyses, these findings corroborate the causal nexus between GM and OP. Facilitated by MR, this study successfully elucidates the causal underpinning binding GM and OP, thereby endowing invaluable insights for deeper exploration into the pivotal role of GM in the pathogenesis of OP.
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Affiliation(s)
- Jun Ma
- Department of Orthopedics, 2nd Hospital of Mudanjiang People, Heilongjiang Province, China
| | - Xin-Ran Wang
- Department of Critical Care Medicine, The First Affiliated Hospital of Harbin Medical University, Heilongjiang Province, China
| | - Yu-Xin Zhou
- Department of Critical Care Medicine, The First Affiliated Hospital of Harbin Medical University, Heilongjiang Province, China
| | - Wei-Jin Zhou
- Department of Orthopedics, The Second Affiliated Hospital of Harbin Medical University, Heilongjiang Province, China
| | - Jian-Nan Zhang
- Department of Critical Care Medicine, The First Affiliated Hospital of Harbin Medical University, Heilongjiang Province, China
| | - Chong-Yi Sun
- Department of Orthopedics, The Second Affiliated Hospital of Harbin Medical University, Heilongjiang Province, China
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Zhang YW, Wu Y, Liu XF, Chen X, Su JC. Targeting the gut microbiota-related metabolites for osteoporosis: The inextricable connection of gut-bone axis. Ageing Res Rev 2024; 94:102196. [PMID: 38218463 DOI: 10.1016/j.arr.2024.102196] [Citation(s) in RCA: 30] [Impact Index Per Article: 30.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/03/2023] [Revised: 12/24/2023] [Accepted: 01/09/2024] [Indexed: 01/15/2024]
Abstract
Osteoporosis is a systemic skeletal disease characterized by decreased bone mass, destruction of bone microstructure, raised bone fragility, and enhanced risk of fractures. The correlation between gut microbiota and bone metabolism has gradually become a widespread research hotspot in recent years, and successive studies have revealed that the alterations of gut microbiota and its-related metabolites are related to the occurrence and progression of osteoporosis. Moreover, several emerging studies on the relationship between gut microbiota-related metabolites and bone metabolism are also underway, and extensive research evidence has indicated an inseparable connection between them. Combined with latest literatures and based on inextricable connection of gut-bone axis, this review is aimed to summarize the relation, potential mechanisms, application strategies, clinical application prospects, and existing challenges of gut microbiota and its-related metabolites on osteoporosis, thus updating the knowledge in this research field and providing certain reference for future researches.
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Affiliation(s)
- Yuan-Wei Zhang
- Department of Orthopaedics, Xinhua Hospital Affiliated to Shanghai JiaoTong University School of Medicine, Shanghai 200092, China; Institute of Translational Medicine, Shanghai University, Shanghai 200444, China; Organoid Research Center, Shanghai University, Shanghai 200444, China; National Center for Translational Medicine (Shanghai) SHU Branch, Shanghai University, Shanghai 200444, China
| | - Yan Wu
- Institute of Translational Medicine, Shanghai University, Shanghai 200444, China; Organoid Research Center, Shanghai University, Shanghai 200444, China; National Center for Translational Medicine (Shanghai) SHU Branch, Shanghai University, Shanghai 200444, China
| | - Xiang-Fei Liu
- Department of Orthopaedics, Shanghai Zhongye Hospital, Shanghai 200941, China.
| | - Xiao Chen
- Department of Orthopaedics, Xinhua Hospital Affiliated to Shanghai JiaoTong University School of Medicine, Shanghai 200092, China.
| | - Jia-Can Su
- Department of Orthopaedics, Xinhua Hospital Affiliated to Shanghai JiaoTong University School of Medicine, Shanghai 200092, China; Institute of Translational Medicine, Shanghai University, Shanghai 200444, China; Organoid Research Center, Shanghai University, Shanghai 200444, China; National Center for Translational Medicine (Shanghai) SHU Branch, Shanghai University, Shanghai 200444, China.
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Wang Y, Li Y, Bo L, Zhou E, Chen Y, Naranmandakh S, Xie W, Ru Q, Chen L, Zhu Z, Ding C, Wu Y. Progress of linking gut microbiota and musculoskeletal health: casualty, mechanisms, and translational values. Gut Microbes 2023; 15:2263207. [PMID: 37800576 PMCID: PMC10561578 DOI: 10.1080/19490976.2023.2263207] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/21/2023] [Accepted: 09/21/2023] [Indexed: 10/07/2023] Open
Abstract
The musculoskeletal system is important for balancing metabolic activity and maintaining health. Recent studies have shown that distortions in homeostasis of the intestinal microbiota are correlated with or may even contribute to abnormalities in musculoskeletal system function. Research has also shown that the intestinal flora and its secondary metabolites can impact the musculoskeletal system by regulating various phenomena, such as inflammation and immune and metabolic activities. Most of the existing literature supports that reasonable nutritional intervention helps to improve and maintain the homeostasis of intestinal microbiota, and may have a positive impact on musculoskeletal health. The purpose of organizing, summarizing and discussing the existing literature is to explore whether the intervention methods, including nutritional supplement and moderate exercise, can affect the muscle and bone health by regulating the microecology of the intestinal flora. More in-depth efficacy verification experiments will be helpful for clinical applications.
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Affiliation(s)
- Yu Wang
- Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, China
| | - Yusheng Li
- Department of Orthopedics, Xiangya Hospital, Central South University, Changsha, China
- National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, China
| | - Lin Bo
- Department of Rheumatology, The Second Affiliated Hospital of Soochow University, Suzhou, Jiangsu, China
| | - Enyuan Zhou
- Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, China
| | - Yanyan Chen
- Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, China
| | - Shinen Naranmandakh
- School of Arts and Sciences, National University of Mongolia, Ulaanbaatar, Mongolia
| | - Wenqing Xie
- Department of Orthopedics, Xiangya Hospital, Central South University, Changsha, China
- National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, Changsha, China
| | - Qin Ru
- Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, China
| | - Lin Chen
- Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, China
| | - Zhaohua Zhu
- Clinical Research Centre, Orthopedic Centre, Zhujiang Hospital, Southern Medical University, Guangzhou, China
| | - Changhai Ding
- Clinical Research Centre, Orthopedic Centre, Zhujiang Hospital, Southern Medical University, Guangzhou, China
- Department of Rheumatology, Guangzhou First People’s Hospital, School of Medicine, South China University of Technology, Guangzhou, China
- Department of Orthopaedics, Affiliated Hospital of Youjiang Medical University for Nationalities, Baise, China
- Menzies Institute for Medical Research, University of Tasmania, Hobart, Australia
| | - Yuxiang Wu
- Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, China
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Akinsuyi OS, Roesch LFW. Meta-Analysis Reveals Compositional and Functional Microbial Changes Associated with Osteoporosis. Microbiol Spectr 2023; 11:e0032223. [PMID: 37042756 PMCID: PMC10269714 DOI: 10.1128/spectrum.00322-23] [Citation(s) in RCA: 19] [Impact Index Per Article: 9.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/23/2023] [Accepted: 03/28/2023] [Indexed: 04/13/2023] Open
Abstract
Over the past decade, the role of the gut microbiota in many disease states has gained a great deal of attention. Mounting evidence from case-control and observational studies has linked changes in the gut microbiota to the pathophysiology of osteoporosis (OP). Nonetheless, the results of these studies contain discrepancies, leaving the literature without a consensus on osteoporosis-associated microbial signatures. Here, we conducted a comprehensive meta-analysis combining and reexamining five publicly available 16S rRNA partial sequence data sets to identify gut bacteria consistently associated with osteoporosis across different cohorts. After adjusting for the batch effect associated with technical variation and heterogeneity of studies, we observed a significant shift in the microbiota composition in the osteoporosis group. An increase in the relative abundance of opportunistic pathogens Clostridium sensu stricto, Bacteroides, and Intestinibacter was observed in the OP group. Moreover, short-chain-fatty-acid (SCFA) producers, including members of the genera Collinsella, Megasphaera, Agathobaculum, Mediterraneibacter, Clostridium XIV, and Dorea, were depleted in the OP group relative to the healthy control (HC) group. Lactic acid-producing bacteria, including Limosilactobacillus, were significantly increased in the OP group. The random forest algorithm further confirmed that these bacteria differentiate the two groups. Furthermore, functional prediction revealed depletion of the SCFA biosynthesis pathway (glycolysis, tricarboxylic acid [TCA] cycle, and Wood-Ljungdahl pathway) and amino acid biosynthesis pathway (methionine, histidine, and arginine) in the OP group relative to the HC group. This study uncovered OP-associated compositional and functional microbial alterations, providing robust insight into OP pathogenesis and aiding the possible development of a therapeutic intervention to manage the disease. IMPORTANCE Osteoporosis is the most common metabolic bone disease associated with aging. Mounting evidence has linked changes in the gut microbiota to the pathophysiology of osteoporosis. However, which microbes are associated with dysbiosis and their impact on bone density and inflammation remain largely unknown due to inconsistent results in the literature. Here, we present a meta-analysis with a standard workflow, robust statistical approaches, and machine learning algorithms to identify notable microbial compositional changes influencing osteoporosis.
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Affiliation(s)
- Oluwamayowa S. Akinsuyi
- Institute of Food and Agriculture, Department of Microbiology and Cell Science, University of Florida, Gainesville, Florida, USA
| | - Luiz F. W. Roesch
- Institute of Food and Agriculture, Department of Microbiology and Cell Science, University of Florida, Gainesville, Florida, USA
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9
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Pan W, Du J, An L, Xu G, Yuan G, Sheng Y, Sun J, Wang M, Zhao N, Guo X, Li H, Han X. Sika deer velvet antler protein extract modulater bone metabolism and the structure of gut microbiota in ovariectomized mice. Food Sci Nutr 2023; 11:3309-3319. [PMID: 37324858 PMCID: PMC10261755 DOI: 10.1002/fsn3.3316] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/16/2022] [Revised: 02/21/2023] [Accepted: 02/26/2023] [Indexed: 09/20/2023] Open
Abstract
Osteoporosis is a systemic osteopathy characterized by bone metabolism disorders that become more serious with age increases in postmenopausal women. Recent studies have found that antler protein is the main bioactive component of cervus pantotrichum, and it has a positive regulatory effect on bone metabolism and can improve estrogen level. This study aimed to investigate the effect of velvet antler extract (VAE) on the prevention of osteoporosis and the modulation of gut microbiota in ovariectomized (OVX) mice. OVX mice treated with 12 weeks of VAE exhibited higher levels of serum BGP, Ca2+, CT, and HyP (p < .05). Micro-CT scans showed that VAE significantly elevated bone volume fraction (BV/TV), trabecular bone number (Tb.N), trabecular bone thickness (Tb.Th), trabecular bone connection density (Conn.D), decreased trabecular separation (Tb.Sp), and structural modality index (SMI) than untreated OVX mice. The right tibial retinaculum in the VAE group was clearer, with a clearer reticular structure, smaller gaps, a tighter distribution, and a more orderly arrangement. The gut microbiota of the cecal contents was analyzed by 16 s rDNA amplicon sequencing. The data indicated that VAE modulated the species, numbers, and diversity of the gut microbiota in OVX mice. Ovariectomy caused dysbiosis of the intestinal microbiota by increasing the ratio of Firmicutes to Bacteroidetes in mice, but the ratio decreased after treatment with VAE. These results suggest that VAE has a therapeutic effect on OVX mice via modulate bone-related biochemical markers in serum and structure of gut microbiota.
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Affiliation(s)
- Wang Pan
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Juan Du
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Liping An
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Guangyu Xu
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Guangxin Yuan
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Yu Sheng
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Jingbo Sun
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Manli Wang
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Nanxi Zhao
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Xiao Guo
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Hongyu Li
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
| | - Xiao Han
- Department of Pharmaceutical AnalysisBeihua University College of PharmacyJilinChina
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10
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Liu T, Yu H, Wang S, Li H, Du X, He X. Chondroitin sulfate alleviates osteoporosis caused by calcium deficiency by regulating lipid metabolism. Nutr Metab (Lond) 2023; 20:6. [PMID: 36747190 PMCID: PMC9901125 DOI: 10.1186/s12986-023-00726-3] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/29/2022] [Accepted: 01/21/2023] [Indexed: 02/08/2023] Open
Abstract
The use of non-drug intervention for calcium deficiency has attracted attention in recent years. Although calcium carbonate is the preferred raw material for calcium supplementation, there are few reports on the mechanism of the combined action of chondroitin sulfate and calcium to alleviate osteoporosis from the perspective of gut microbiota and metabolomics. In this study, a rat model of osteoporosis was established by feeding a low-calcium diet. The intestinal microbiota abundance, fecal and plasma metabolite expression levels of rats fed a basal diet, a low-calcium diet, a low-calcium diet plus calcium carbonate, and a low-calcium diet plus chondroitin sulfate were compared. The results showed that compared with the low calcium group, the calcium content and bone mineral density of femur were significantly increased in the calcium carbonate and chondroitin sulfate groups. 16 S rRNA sequencing and metabolomics analysis showed that chondroitin sulfate intervention could reduce short-chain fatty acid synthesis of intestinal flora, slow down inflammatory response, inhibit osteoclast differentiation, promote calcium absorption and antioxidant mechanism, and alleviate osteoporosis in low-calcium feeding rats. Correlation analysis showed that the selected intestinal flora was significantly correlated with metabolites enriched in feces and plasma. This study provides scientific evidence of the potential impact of chondroitin sulfate as a dietary supplement for patients with osteoporosis.
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Affiliation(s)
- Tianshu Liu
- grid.27255.370000 0004 1761 1174Department of Epidemiology, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan, 250012 Shandong China ,grid.27255.370000 0004 1761 1174Institute for Medical Dataology, Shandong University, National Institute of Health Data Science of China, Jinan, 250012 Shandong China
| | - Hai Yu
- grid.272242.30000 0001 2168 5385Division of Cancer RNA Research, National Cancer Center Research Institute, Tokyo, 104-0045 Japan ,grid.27255.370000 0004 1761 1174Institute for Medical Dataology, Shandong University, National Institute of Health Data Science of China, Jinan, 250012 Shandong China
| | - Shuai Wang
- grid.27255.370000 0004 1761 1174Institute of Toxicology, School of Public Health, Cheeloo College of Medicine, Shandong University, Jining, 250012 Shandong China
| | - Huimin Li
- grid.27255.370000 0004 1761 1174Department of Physical and Chemical Inspection, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan, 250012 Shandong China ,grid.506261.60000 0001 0706 7839National Human Genetic Resources Center; National Research Institute for Health and Family Planning, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, 100730 China
| | - Xinyiran Du
- grid.449428.70000 0004 1797 7280College of Stomatology, Jining Medical University, Jining, 272067 Shandong China
| | - Xiaodong He
- Department of Physical and Chemical Inspection, School of Public Health, Cheeloo College of Medicine, Shandong University, Jinan, 250012, Shandong, China. .,Institute for Medical Dataology, Shandong University, National Institute of Health Data Science of China, Jinan, 250012, Shandong, China.
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11
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Xie H, Hua Z, Guo M, Lin S, Zhou Y, Weng Z, Wu L, Chen Z, Xu Z, Li W. Gut microbiota and metabonomics used to explore the mechanism of Qing'e Pills in alleviating osteoporosis. PHARMACEUTICAL BIOLOGY 2022; 60:785-800. [PMID: 35387559 PMCID: PMC9004512 DOI: 10.1080/13880209.2022.2056208] [Citation(s) in RCA: 18] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 06/14/2021] [Revised: 01/20/2022] [Accepted: 03/16/2022] [Indexed: 06/14/2023]
Abstract
CONTEXT The traditional Chinese medicine Qing'e Pills (QEP) has been used to treat postmenopausal osteoporosis (PMO). OBJECTIVE We evaluated the regulatory effects of QEP on gut microbiota in osteoporosis. MATERIALS AND METHODS Eighteen female SD rats were divided into three groups: sham surgery (SHAM), ovariectomized (OVX) and ovariectomized treated with QEP (OVX + QEP). Six weeks after ovariectomy, QEP was administered to OVX + QEP rats for eight weeks (4.5 g/kg/day, i.g.). After 14 weeks, the bone microstructure was evaluated. Differences in gut microbiota were analysed via 16S rRNA gene sequencing. Changes in endogenous metabolites were studied using UHPLC-Q-TOF/MS technology. GC-MS was used to detect short-chain fatty acids. Furthermore, we measured serum inflammatory factors, such as IL-6, TNF-α and IFN-γ, which may be related to gut microbiota. RESULTS OVX + QEP exhibited increased bone mineral density (0.11 ± 0.03 vs. 0.21 ± 0.02, p< 0.001) compared to that of OVX. QEP altered the composition of gut microbiota. We identified 19 potential biomarkers related to osteoporosis. QEP inhibited the elevation of TNF-α (38.86 ± 3.19 vs. 29.43 ± 3.65, p< 0.05) and IL-6 (83.38 ± 16.92 vs. 45.26 ± 3.94, p< 0.05) levels, while it increased the concentrations of acetic acid (271.95 ± 52.41 vs. 447.73 ± 46.54, p< 0.001), propionic acid (28.96 ± 5.73 vs. 53.41 ± 14.26, p< 0.01) and butyric acid (24.92 ± 18.97 vs. 67.78 ± 35.68, p< 0.05). CONCLUSIONS These results indicate that QEP has potential of regulating intestinal flora and improving osteoporosis. The combination of anti-osteoporosis drugs and intestinal flora could become a new treatment for osteoporosis.
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Affiliation(s)
- Hui Xie
- School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, China
- Jiangsu Key Laboratory of Chinese Medicine Processing, Engineering Center of State Ministry of Education for Standardization of Chinese Medicine Processing, Nanjing University of Chinese Medicine, Nanjing, China
| | - Zhengying Hua
- School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, China
- Jiangsu Key Laboratory of Chinese Medicine Processing, Engineering Center of State Ministry of Education for Standardization of Chinese Medicine Processing, Nanjing University of Chinese Medicine, Nanjing, China
| | - Mengyu Guo
- School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, China
- Jiangsu Key Laboratory of Chinese Medicine Processing, Engineering Center of State Ministry of Education for Standardization of Chinese Medicine Processing, Nanjing University of Chinese Medicine, Nanjing, China
| | - Shangyang Lin
- School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, China
- Jiangsu Key Laboratory of Chinese Medicine Processing, Engineering Center of State Ministry of Education for Standardization of Chinese Medicine Processing, Nanjing University of Chinese Medicine, Nanjing, China
| | - Yaqian Zhou
- School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, China
- Jiangsu Key Laboratory of Chinese Medicine Processing, Engineering Center of State Ministry of Education for Standardization of Chinese Medicine Processing, Nanjing University of Chinese Medicine, Nanjing, China
| | - Zebin Weng
- School of Chinese Medicine, Nanjing University of Chinese Medicine, Nanjing, China
| | - Li Wu
- School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, China
| | - Zhipeng Chen
- School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, China
- Jiangsu Key Laboratory of Chinese Medicine Processing, Engineering Center of State Ministry of Education for Standardization of Chinese Medicine Processing, Nanjing University of Chinese Medicine, Nanjing, China
| | - Zisheng Xu
- Wuhu Pure Sunshine Natural Medicine Company Limited, Wuhu, China
| | - Weidong Li
- School of Pharmacy, Nanjing University of Chinese Medicine, Nanjing, China
- Jiangsu Key Laboratory of Chinese Medicine Processing, Engineering Center of State Ministry of Education for Standardization of Chinese Medicine Processing, Nanjing University of Chinese Medicine, Nanjing, China
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12
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Damani JJ, De Souza MJ, VanEvery HL, Strock NCA, Rogers CJ. The Role of Prunes in Modulating Inflammatory Pathways to Improve Bone Health in Postmenopausal Women. Adv Nutr 2022; 13:1476-1492. [PMID: 34978320 PMCID: PMC9526830 DOI: 10.1093/advances/nmab162] [Citation(s) in RCA: 27] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/20/2021] [Revised: 10/31/2021] [Accepted: 12/30/2021] [Indexed: 01/28/2023] Open
Abstract
The prevalence of osteoporosis among women aged 50 y and older is expected to reach 13.6 million by 2030. Alternative nonpharmaceutical agents for osteoporosis, including nutritional interventions, are becoming increasingly popular. Prunes (dried plums; Prunus domestica L.) have been studied as a potential whole-food dietary intervention to mitigate bone loss in preclinical models of osteoporosis and in osteopenic postmenopausal women. Sixteen preclinical studies using in vivo rodent models of osteopenia or osteoporosis have established that dietary supplementation with prunes confers osteoprotective effects both by preventing and reversing bone loss. Increasing evidence from 10 studies suggests that, in addition to antiresorptive effects, prunes exert anti-inflammatory and antioxidant effects. Ten preclinical studies have found that prunes and/or their polyphenol extracts decrease malondialdehyde and NO secretion, increase antioxidant enzyme expression, or suppress NF-κB activation and proinflammatory cytokine production. Two clinical trials have investigated the impact of dried plum consumption (50-100 g/d for 6-12 mo) on bone health in postmenopausal women and demonstrated promising effects on bone mineral density and bone biomarkers. However, less is known about the impact of prune consumption on oxidative stress and inflammatory mediators in humans and their possible role in modulating bone outcomes. In this review, the current state of knowledge on the relation between inflammation and bone health is outlined. Findings from preclinical and clinical studies that have assessed the effect of prunes on oxidative stress, inflammatory mediators, and bone outcomes are summarized, and evidence supporting a potential role of prunes in modulating inflammatory and immune pathways is highlighted. Key future directions to bridge the knowledge gap in the field are proposed.
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Affiliation(s)
- Janhavi J Damani
- Intercollege Graduate Degree Program in Integrative and Biomedical Physiology, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA
| | - Mary Jane De Souza
- Department of Kinesiology, The Pennsylvania State University, University Park, PA, USA
| | - Hannah L VanEvery
- Department of Nutritional Sciences, The Pennsylvania State University, University Park, PA, USA
| | - Nicole C A Strock
- Department of Kinesiology, The Pennsylvania State University, University Park, PA, USA
| | - Connie J Rogers
- Department of Nutritional Sciences, The Pennsylvania State University, University Park, PA, USA
- Center for Molecular Immunology and Infectious Disease, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, USA
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Zhang F, Zhao Y, Wang Y, Wang H, Nan X, Guo Y, Xiong B. Dietary supplementation with calcium propionate could beneficially alter rectal microbial composition of early lactation dairy cows. Front Vet Sci 2022; 9:940216. [PMID: 35958310 PMCID: PMC9360568 DOI: 10.3389/fvets.2022.940216] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/10/2022] [Accepted: 07/06/2022] [Indexed: 11/13/2022] Open
Abstract
Dietary supplementation with calcium propionate can effectively alleviate negative energy balance and hypocalcemia of dairy cows in early lactation. The objective of this study was to investigate the effects of calcium propionate feeding levels on the immune function, liver function, and fecal microbial composition of dairy cows in early lactation. Thirty-two multiparous Holstein cows were randomly assigned to four treatments after calving. Treatments were a basal diet plus 0, 200, 350, and 500 g calcium propionate per cow per day throughout a 5-week trial period. Cows were milked three times a day, and blood was sampled to measure immune function and liver function on d 7, 21, and 35. The rectal contents were sampled and collected on d 35 to analyze the microbial composition using 16S rRNA gene sequencing. The results indicated that increasing amounts of calcium propionate did not affected the serum concentrations of total protein, IgG, IgM, and calcium, but the concentrations of albumin and IgA changed quadratically. With the increase of calcium propionate, the activity of serum alanine transaminase and aspartate aminotransferase increased linearly, in contrast, the activity of alkaline phosphatase decreased linearly. Moreover, dietary supplementation with increasing levels of calcium propionate tended to quadratically decrease the relative abundance of Firmicutes while quadratically increased the abundance of Bacteroidetes, and consequently linearly decreased the Firmicutes/Bacteroidetes ratio in the rectal microbiota. Additionally, the supplementation of calcium propionate increased the relative abundances of Ruminococcaceae_UCG-005 and Prevotellaceae_UCG-004 linearly, and Ruminococcaceae_UCG-014 quadratically, but decreased the relative abundances of Lachnospiraceae_NK3A20_group and Family_XIII_AD3011_group quadratically. Compared with the CON group, the calcium propionate supplementation significantly decreased the relative abundance of Acetitomaculum but increased the abundances of Rikenellaceae_RC9_gut_group and Alistipes. In summary, these results suggested that the supplementation of calcium propionate to dairy cows in early lactation could beneficially alter the rectal microbiota.
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Affiliation(s)
- Fan Zhang
- State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
- State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, China
| | - Yiguang Zhao
- State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Yue Wang
- State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Hui Wang
- State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Xuemei Nan
- State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
| | - Yuming Guo
- State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing, China
- *Correspondence: Yuming Guo
| | - Benhai Xiong
- State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, China
- Benhai Xiong
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Mitchell S, Lee A, Stenquist R, Yatsonsky II D, Mooney ML, Shendge VB. Extensive adhesion formation in a total knee replacement in the setting of a gastrointestinal stromal tumor: A case report. World J Orthop 2022; 13:538-543. [PMID: 35633745 PMCID: PMC9124998 DOI: 10.5312/wjo.v13.i5.538] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/12/2021] [Revised: 02/04/2022] [Accepted: 04/24/2022] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Gastrointestinal stromal tumors (GISTs) are rare primary neoplasms of the gastrointestinal tract, accounting for 1% to 2% of all gastrointestinal neoplasms worldwide. GISTs are frequently discovered incidentally during workup for other diagnosis or intestinal obstruction, as they can present with few or no symptoms. Simultaneously, GISTs confer a high degree of malignant transformation, with a progression in about 10% to 30% of cases.
CASE SUMMARY A 63-year-old healthy female presented to our institution with complaints of right knee pain and limited passive and active motion in the setting of a previous right total knee arthroplasty (TKA). One year after TKA, the patient was incidentally diagnosed with a GIST, which was successfully removed. After removal, the patient continued to have limited range of motion of the right knee and subsequently underwent revision TKA. Intraoperatively significant fibrotic adhesions were found encapsulating the femoral and tibial components. The patient’s pain improved postoperatively, however, she continued to have decreased range of motion with difficulty ambulating.
CONCLUSION We propose that this case may demonstrate a proinflammatory milieu arising from a GIST, which had a direct influence on the outcome of recent total knee arthroplasty. This proposed mechanism between neoplastic cytokinetic activity and adhesion formation could have implications on preoperative and postoperative orthopedic management of total knee arthroplasty.
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Affiliation(s)
- Steven Mitchell
- Department ofOrthopaedic Surgery, The University of Toledo Medical Center, Toledo, OH 43614, United States
| | - Anderson Lee
- Department ofOrthopaedic Surgery, The University of Toledo Medical Center, Toledo, OH 43614, United States
| | - Ryan Stenquist
- Department ofOrthopaedic Surgery, The University of Toledo Medical Center, Toledo, OH 43614, United States
| | - David Yatsonsky II
- Department ofOrthopaedic Surgery, The University of Toledo Medical Center, Toledo, OH 43614, United States
| | - Megan L Mooney
- Department ofOrthopaedic Surgery, The University of Toledo Medical Center, Toledo, OH 43614, United States
| | - Vithal B Shendge
- Department ofOrthopaedic Surgery, The University of Toledo Medical Center, Toledo, OH 43614, United States
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15
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Jhong JH, Tsai WH, Yang LC, Chou CH, Lee TY, Yeh YT, Huang CH, Luo YH. Heat-Killed Lacticaseibacillus paracasei GMNL-653 Exerts Antiosteoporotic Effects by Restoring the Gut Microbiota Dysbiosis in Ovariectomized Mice. Front Nutr 2022; 9:804210. [PMID: 35187034 PMCID: PMC8856183 DOI: 10.3389/fnut.2022.804210] [Citation(s) in RCA: 14] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/29/2021] [Accepted: 01/13/2022] [Indexed: 12/15/2022] Open
Abstract
Osteoporosis is a metabolic inflammatory disease, an imbalance occurs between bone resorption and formation, leading to bone loss. Anti-inflammatory diet is considered having the potential to ameliorate osteoporosis. Heat-killed probiotics exhibit health benefits in relation to their immunomodulatory effects, but the detail mechanism involved in gut microbiota balance, host metabolism, immunity, and bone homeostasis remains unclear. In this study, we evaluated the antiosteoporotic effects of heat-killed Lacticaseibacillus paracasei GMNL-653 in vitro and in ovariectomized (OVX) mice. Furthermore, whole-genome sequencing and comparative genomics analysis demonstrated potentially genes involved in antiosteoporotic activity. The GMNL-653 exerts anti-inflammatory activity which restored gut microbiota dysbiosis and maintained intestinal barrier integrity in the OVX mice. The levels of IL-17 and LPS in the sera decreased following GMNL-653 treatment compared with those of the vehicle control; mRNA levels of RANKL were reduced and TGF-β and IL-10 enhanced in OVX-tibia tissue after treatment. The levels of IL-17 were significantly associated with gut microbiota dysbiosis. Gut microbial metagenomes were further analyzed by PICRUSt functional prediction, which reveal that GMNL-653 intervention influence in several host metabolic pathways. The analysis of whole-genome sequencing accompanied by comparative genomics on three L. paracasei strains revealed a set of GMNL-653 genes that are potentially involved in antiosteoporotic activity. Our findings validated antiosteoporotic activity of heat-killed GMNL-653 using in vitro and in vivo models, to whole-genome sequencing and identifying genes potentially involved in this gut microbiota–bone axis.
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Affiliation(s)
- Jhih-Hua Jhong
- Department of Computer Science and Engineering, Yuan Ze University, Taoyuan, Taiwan
| | - Wan-Hua Tsai
- Research and Development Department, GenMont Biotech Incorporation, Tainan, Taiwan
| | - Li-Chan Yang
- Department of Pharmacy, China Medical University, Taichung, Taiwan
| | - Chia-Hsuan Chou
- Research and Development Department, GenMont Biotech Incorporation, Tainan, Taiwan
| | - Tzong-Yi Lee
- School of Life and Health Sciences, The Chinese University of Hong Kong, Shenzhen, China
- Warshel Institute for Computational Biology, The Chinese University of Hong Kong, Shenzhen, China
| | - Yao-Tsung Yeh
- Aging and Diseases Prevention Research Center, Fooyin University, Kaohsiung, Taiwan
- Biomed Analysis Center, Fooyin University Hospital, Pingtung, Taiwan
| | - Cheng-Hsieh Huang
- Aging and Diseases Prevention Research Center, Fooyin University, Kaohsiung, Taiwan
- Ph.D. Program in Environmental and Occupational Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
| | - Yueh-Hsia Luo
- Department of Life Sciences, National Central University, Taoyuan, Taiwan
- *Correspondence: Yueh-Hsia Luo
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Chen L, Yan S, Yang M, Yu F, Wang J, Wang X, Xu H, Shi J, Pan L, Zeng Y, Li S, Li L, You L, Peng Y. The gut microbiome is associated with bone turnover markers in postmenopausal women. Am J Transl Res 2021; 13:12601-12613. [PMID: 34956476 PMCID: PMC8661154] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/03/2021] [Accepted: 09/05/2021] [Indexed: 06/14/2023]
Abstract
OBJECTIVE The association of the gut microbiome with bone turnover markers (BTMs) in postmenopausal women is poorly understood. METHODS Fecal samples were collected from 97 Chinese postmenopausal women, and the serum CTX and P1NP were determined. Individuals with serum CTX lower or higher than the median value were divided into LCTX and P1NP groups; and individuals with serum P1NP lower or higher than the median value were grouped into LP1NP and HP1NP groups. Microbiota profiles were determined by high-throughput 16S rRNA gene sequencing. RESULTS In postmenopausal women, only Faecalibacterium showed significant alteration in the HCTX group compared with the LCTX group (P=0.004, q=0.143). Linear discriminant analysis effect size (LEfSe) analysis revealed that Clostridiaceae (P=0.015, LDA=2.89), Faecalibacterium (P=0.017, LDA=4.60), Prevotella (P=0.040, LDA=3.61) and Clostridium (P=0.007, LDA=2.79) were abundant in the LCTX group, and Facklamia (P=0.044, LDA=3.10) was enriched in the HCTX group. Peptostreptococcaceae (P=0.048, LDA=2.83) and the SMB53 (P=0.028, LDA=2.05) genus were enriched in the LPINP group, and Veillonellaceae (P=0.025, LDA=4.43) and the S24_7 (P=0.023, LDA=3.08) family were enriched in the HPINP group. Six taxa correlated with BTMs in all subjects, including Clostridium (Clostridiaceae) that was negatively correlated with serum CTX amounts significantly (r=-0.34, P<0.001). CONCLUSION This study identified taxa-specific differences in the intestinal microflora associated with BTMs, notably CTX. These findings may help in uncovering the roles of gut microbiota on bone metabolism.
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Affiliation(s)
- Lin Chen
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Shuai Yan
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Ming Yang
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Fudong Yu
- Basic Reproduction Laboratory, Shanghai Institute of Planned Parenthood Research, Fudan UniversityShanghai 200032, China
| | - Jingjing Wang
- Shanghai Key Laboratory for Pancreatic Diseases, Institute of Translational Medicine, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Xiaoxin Wang
- Shanghai Key Laboratory for Pancreatic Diseases, Institute of Translational Medicine, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Huanbai Xu
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Jianxia Shi
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Ling Pan
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Yuexi Zeng
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Siyu Li
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Li Li
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Li You
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
| | - Yongde Peng
- Department of Endocrinology and Metabolism, Shanghai General Hospital, Shanghai Jiao Tong University School of MedicineShanghai 200080, China
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Ilesanmi-Oyelere BL, Roy NC, Kruger MC. Modulation of Bone and Joint Biomarkers, Gut Microbiota, and Inflammation Status by Synbiotic Supplementation and Weight-Bearing Exercise: Human Study Protocol for a Randomized Controlled Trial. JMIR Res Protoc 2021; 10:e30131. [PMID: 34698648 PMCID: PMC8579214 DOI: 10.2196/30131] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/02/2021] [Revised: 08/08/2021] [Accepted: 08/10/2021] [Indexed: 01/19/2023] Open
Abstract
BACKGROUND There is strong evidence suggesting that prebiotics and probiotics regulate gut microbiota, reducing inflammation and thereby potentially improving bone health status. Similarly, mechanistic evidence suggests that either low-impact or high-impact weight-bearing exercises improve body composition and consequently increase bone mineral density in individuals with osteoporosis and osteoarthritis. OBJECTIVE This study aims to investigate the effects of a synbiotic (probiotic+prebiotic) supplementation, an exercise intervention, or a combination of both on gut microbiota, inflammation, and bone biomarkers in postmenopausal women. METHODS A total of 160 postmenopausal women from New Zealand will be recruited and randomized to one of four interventions or treatments for 12 weeks: control, synbiotic supplementation, exercise intervention, or synbiotic supplementation and exercise. The primary outcome measure is the bone and joint biomarkers at baseline and week 12, whereas the gut microbiota profile and inflammatory cytokine measurements will serve as the secondary outcome measures at baseline and week 12. Baseline data and exercise history will be used to assess, allocate, and stratify participants into treatment measures. RESULTS Recruitment of participants will begin in September 2021, and the anticipated completion date is June 2022. CONCLUSIONS To the best of our knowledge, this will be the first randomized controlled trial to analyze the effects of both a synbiotic supplement and an exercise intervention in postmenopausal women. On the basis of the results obtained, a combination of synbiotic supplements and exercise might serve as a noninvasive approach to manage and/or improve body composition and bone health in postmenopausal women. TRIAL REGISTRATION Australian New Zealand Clinical Trials Registry ACTRN12620000998943p; https://www.anzctr.org.au/Trial/Registration/TrialReview.aspx?id=380336&isClinicalTrial=False.
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Affiliation(s)
| | - Nicole C Roy
- Department of Human Nutrition, University of Otago, Dunedin, New Zealand
| | - Marlena C Kruger
- College of Health, Massey University, Palmerston North, New Zealand
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18
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Nourbakhsh F, Lotfalizadeh M, Badpeyma M, Shakeri A, Soheili V. From plants to antimicrobials: Natural products against bacterial membranes. Phytother Res 2021; 36:33-52. [PMID: 34532918 DOI: 10.1002/ptr.7275] [Citation(s) in RCA: 36] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/18/2020] [Revised: 07/16/2021] [Accepted: 08/25/2021] [Indexed: 12/24/2022]
Abstract
Bacterial membrane barrier provides a cytoplasmic environment for organelles of bacteria. The membrane is composed of lipid compounds containing phosphatide protein and a minimal amount of sugars, and is responsible for intercellular transfers of chemicals. Several antimicrobials have been found that affect bacterial cytoplasmic membranes. These compounds generally disrupt the organization of the membrane or perforate it. By destroying the membrane, the drugs can permeate and replace the effective macromolecules necessary for cell life. Furthermore, they can disrupt electrical gradients of the cells through impairment of the membrane integrity. In recent years, considering the spread of microbial resistance and the side effects of antibiotics, natural antimicrobial compounds have been studied by researchers extensively. These molecules are the best alternative for controlling bacterial infections and reducing drug resistance due to the lack of severe side effects, low cost of production, and biocompatibility. Better understanding of the natural compounds' mechanisms against bacteria provides improved strategies for antimicrobial therapies. In this review, natural products with antibacterial activities focusing on membrane damaging mechanisms were described. However, further high-quality research studies are needed to confirm the clinical efficacy of these natural products.
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Affiliation(s)
- Fahimeh Nourbakhsh
- Medical Toxicology Research Centre, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Marzieh Lotfalizadeh
- Department of Obstetrics and Gynecology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Mohaddeseh Badpeyma
- Student Research Committee, Department of Clinical Nutrition, Nutrition Research Center, School of Nutrition and Food Sciences, Tabriz University of Medical Sciences, Tabriz, Iran
| | - Abolfazl Shakeri
- Department of Pharmacognosy, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Vahid Soheili
- Department of Pharmaceutical Control, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
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Shen Q, Zhang C, Qin X, Zhang H, Zhang Z, Richel A. Modulation of gut microbiota by chondroitin sulfate calcium complex during alleviation of osteoporosis in ovariectomized rats. Carbohydr Polym 2021; 266:118099. [PMID: 34044918 DOI: 10.1016/j.carbpol.2021.118099] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/11/2021] [Revised: 03/29/2021] [Accepted: 04/15/2021] [Indexed: 12/21/2022]
Abstract
Although chondroitin sulfate calcium complex (CSCa) was claimed to have the bioactivity for bone care in vitro, its anti-osteoporosis bioactivity was little reported in vivo. Here, the effects of CSCa on osteoporosis rats were investigated. Results showed that, compared with the osteoporosis rats, CSCa could improve the bone mineral density and microstructure of femur, and change the bone turnover markers level in serum. 16S rRNA sequencing and metabolomics analysis indicated CSCa intervention altered the composition of gut microbiota along with metabolite profiles in ovariectomized rat faeces. The correlation analysis showed some gut microbiota taxa were significantly correlated with osteoporosis phenotypes and the enriched metabolites. Taken together, dietary CSCa intervention has the potential to alleviate the osteoporosis and related symptoms probably involving gut microbiota or the metabolite profiles as demonstrated in rats. This study provides some scientific evidence for the potential effects of CSCa as the food supplement on the osteoporosis.
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Affiliation(s)
- Qingshan Shen
- Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China; University of Liege-Gembloux Agro-Bio Tech, Laboratory of Biomass and Green Technologies, Passage des déportés 2, B-5030 Gembloux, Belgium
| | - Chunhui Zhang
- Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China.
| | - Xiaojie Qin
- Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China
| | - Hongru Zhang
- Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Beijing 100193, China; University of Liege-Gembloux Agro-Bio Tech, Laboratory of Biomass and Green Technologies, Passage des déportés 2, B-5030 Gembloux, Belgium
| | - Zhiqiang Zhang
- Shandong Haiyu Biotechnology Co., Ltd., Jining 272113, China
| | - Aurore Richel
- University of Liege-Gembloux Agro-Bio Tech, Laboratory of Biomass and Green Technologies, Passage des déportés 2, B-5030 Gembloux, Belgium
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Pérez-Burillo S, Navajas-Porras B, López-Maldonado A, Hinojosa-Nogueira D, Pastoriza S, Rufián-Henares JÁ. Green Tea and Its Relation to Human Gut Microbiome. Molecules 2021; 26:molecules26133907. [PMID: 34206736 PMCID: PMC8271705 DOI: 10.3390/molecules26133907] [Citation(s) in RCA: 59] [Impact Index Per Article: 14.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/25/2021] [Revised: 06/22/2021] [Accepted: 06/23/2021] [Indexed: 12/14/2022] Open
Abstract
Green tea can influence the gut microbiota by either stimulating the growth of specific species or by hindering the development of detrimental ones. At the same time, gut bacteria can metabolize green tea compounds and produce smaller bioactive molecules. Accordingly, green tea benefits could be due to beneficial bacteria or to microbial bioactive metabolites. Therefore, the gut microbiota is likely to act as middle man for, at least, some of the green tea benefits on health. Many health promoting effects of green tea seems to be related to the inter-relation between green tea and gut microbiota. Green tea has proven to be able to correct the microbial dysbiosis that appears during several conditions such as obesity or cancer. On the other hand, tea compounds influence the growth of bacterial species involved in inflammatory processes such as the release of LPS or the modulation of IL production; thus, influencing the development of different chronic diseases. There are many studies trying to link either green tea or green tea phenolic compounds to health benefits via gut microbiota. In this review, we tried to summarize the most recent research in the area.
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Affiliation(s)
- Sergio Pérez-Burillo
- Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigación Biomédica, Universidad de Granada, 18071 Granada, Spain; (S.P.-B.); (B.N.-P.); (A.L.-M.); (D.H.-N.); (S.P.)
- Department of Biochemistry and Molecular Biology, Boonshoft School of Medicine, Wright State University, Dayton, OH 45435, USA
- Instituto de Investigación Biosanitaria ibs. GRANADA, Universidad de Granada, 18071 Granada, Spain
| | - Beatriz Navajas-Porras
- Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigación Biomédica, Universidad de Granada, 18071 Granada, Spain; (S.P.-B.); (B.N.-P.); (A.L.-M.); (D.H.-N.); (S.P.)
- Instituto de Investigación Biosanitaria ibs. GRANADA, Universidad de Granada, 18071 Granada, Spain
| | - Alicia López-Maldonado
- Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigación Biomédica, Universidad de Granada, 18071 Granada, Spain; (S.P.-B.); (B.N.-P.); (A.L.-M.); (D.H.-N.); (S.P.)
- Instituto de Investigación Biosanitaria ibs. GRANADA, Universidad de Granada, 18071 Granada, Spain
| | - Daniel Hinojosa-Nogueira
- Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigación Biomédica, Universidad de Granada, 18071 Granada, Spain; (S.P.-B.); (B.N.-P.); (A.L.-M.); (D.H.-N.); (S.P.)
- Instituto de Investigación Biosanitaria ibs. GRANADA, Universidad de Granada, 18071 Granada, Spain
| | - Silvia Pastoriza
- Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigación Biomédica, Universidad de Granada, 18071 Granada, Spain; (S.P.-B.); (B.N.-P.); (A.L.-M.); (D.H.-N.); (S.P.)
- Instituto de Investigación Biosanitaria ibs. GRANADA, Universidad de Granada, 18071 Granada, Spain
| | - José Ángel Rufián-Henares
- Departamento de Nutrición y Bromatología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigación Biomédica, Universidad de Granada, 18071 Granada, Spain; (S.P.-B.); (B.N.-P.); (A.L.-M.); (D.H.-N.); (S.P.)
- Instituto de Investigación Biosanitaria ibs. GRANADA, Universidad de Granada, 18071 Granada, Spain
- Correspondence: ; Tel.: +34-958-24-28-41
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Keshavarz Azizi Raftar S, Hoseini Tavassol Z, Amiri M, Ejtahed HS, Zangeneh M, Sadeghi S, Ashrafian F, Kariman A, Khatami S, Siadat SD. Assessment of fecal Akkermansia muciniphila in patients with osteoporosis and osteopenia: a pilot study. J Diabetes Metab Disord 2021; 20:279-284. [PMID: 34222066 PMCID: PMC8212221 DOI: 10.1007/s40200-021-00742-1] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/28/2020] [Accepted: 01/12/2021] [Indexed: 12/18/2022]
Abstract
OBJECTIVES Osteoporosis is characterized by slow deterioration in bone mass and disruption of its structure, leading to an increased risk of bone fractures. Gut microbiota plays an important role in the transport and absorption of nutrients needed for bone health. Akkermansia muciniphila is one of the gut microbiota members that its beneficial role in prevention of metabolic disorder was suggested. The aim of the current pilot study was the assessment of fecal A. muciniphila in patients with osteoporosis and osteopenia. METHODS A total of 36 subjects including eight with osteoporosis (three men and five women), eight with osteopenia (two men and six women), and 20 normal controls (six men and 14 women) were selected. Microbial genome was extracted from fresh stool samples. The bacterial load was determined by quantitative real-time PCR using 16S rRNA specific primers. RESULTS The participants' mean age in the osteoporosis, osteopenia and control groups were 61.71, 45 and 45.05 years, respectively. The majority of osteoporosis patients were post-menopause women, while in osteopenia group was pre-menopause. There were significant differences in terms of age, T-score, Z-score, and menopause among groups (P value < 0.05). The presence of A. muciniphila was higher in the healthy group compared to osteopenia group; however, these differences were not statistically significant. CONCLUSIONS In conclusion, however, there was no statistically significant difference between the study groups; it seems that the load of A. muciniphila may be related to bone health. Further in vivo and in vitro studies are needed to investigate the immunological and biochemical pathways.
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Affiliation(s)
- Shahrbanoo Keshavarz Azizi Raftar
- Microbiology Research Center (MRC), Pasteur Institute of Iran, Tehran, Iran
- Department of Mycobacteriology and Pulmonary Research, Pasteur Institute of Iran, Tehran, Iran
| | - Zahra Hoseini Tavassol
- Microbiology Research Center (MRC), Pasteur Institute of Iran, Tehran, Iran
- Obesity and Eating Habits Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran
| | - Meysam Amiri
- Microbiology Research Center (MRC), Pasteur Institute of Iran, Tehran, Iran
| | - Hanieh-Sadat Ejtahed
- Obesity and Eating Habits Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran
- Endocrinology and Metabolism Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran
| | - Mehrangiz Zangeneh
- Department of Infectious Disease, Faculty of Medicine, Tehran Medical science, Islamic Azad University, Tehran, Iran
| | - Sedigheh Sadeghi
- Department of Biochemistry, Pasteur Institute of Iran, Tehran, Iran
| | - Fatemeh Ashrafian
- Microbiology Research Center (MRC), Pasteur Institute of Iran, Tehran, Iran
- Department of Mycobacteriology and Pulmonary Research, Pasteur Institute of Iran, Tehran, Iran
| | | | - Shohreh Khatami
- Department of Biochemistry, Pasteur Institute of Iran, Tehran, Iran
| | - Seyed Davar Siadat
- Microbiology Research Center (MRC), Pasteur Institute of Iran, Tehran, Iran
- Department of Mycobacteriology and Pulmonary Research, Pasteur Institute of Iran, Tehran, Iran
- Endocrinology and Metabolism Research Center, Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran
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Bacillus subtilis-Based Probiotic Improves Skeletal Health and Immunity in Broiler Chickens Exposed to Heat Stress. Animals (Basel) 2021; 11:ani11061494. [PMID: 34064126 PMCID: PMC8224346 DOI: 10.3390/ani11061494] [Citation(s) in RCA: 36] [Impact Index Per Article: 9.0] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/30/2021] [Revised: 05/06/2021] [Accepted: 05/11/2021] [Indexed: 12/12/2022] Open
Abstract
Simple Summary High ambient temperature is a major environmental stressor affecting the physiological and behavioral status of animals, increasing stress susceptibility and immunosuppression, and consequently increasing intestinal permeability (leaky gut) and related neuroinflammation. Probiotics, as well as prebiotics and synbiotics, have been used to prevent or decrease stress-associated detrimental effects on physiological and behavioral homeostasis in humans and various animals. The current data indicate that a dietary probiotic supplement, Bacillus subtilis, reduces heat stress-induced abnormal behaviors and negative effects on skeletal health in broilers through a variety of cellular responses, regulating the functioning of the microbiota–gut–brain axis and/or microbiota-modulated immunity during bone remodeling under thermoneutral and heat-stressed conditions. Abstract The elevation of ambient temperature beyond the thermoneutral zone leads to heat stress, which is a growing health and welfare issue for homeothermic animals aiming to maintain relatively constant reproducibility and survivability. Particularly, global warming over the past decades has resulted in more hot days with more intense, frequent, and long-lasting heat waves, resulting in a global surge in animals suffering from heat stress. Heat stress causes pathophysiological changes in animals, increasing stress sensitivity and immunosuppression, consequently leading to increased intestinal permeability (leaky gut) and related neuroinflammation. Probiotics, as well as prebiotics and synbiotics, have been used to prevent or reduce stress-induced negative effects on physiological and behavioral homeostasis in humans and various animals. The current data indicate dietary supplementation with a Bacillus subtilis-based probiotic has similar functions in poultry. This review highlights the recent findings on the effects of the probiotic Bacillus subtilis on skeletal health of broiler chickens exposed to heat stress. It provides insights to aid in the development of practical strategies for improving health and performance in poultry.
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Cañamares-Orbis P, Bernal-Monterde V, Sierra-Gabarda O, Casas-Deza D, Garcia-Rayado G, Cortes L, Lué A. Impact of Liver and Pancreas Diseases on Nutritional Status. Nutrients 2021; 13:1650. [PMID: 34068295 PMCID: PMC8153270 DOI: 10.3390/nu13051650] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/31/2021] [Revised: 05/02/2021] [Accepted: 05/11/2021] [Indexed: 12/12/2022] Open
Abstract
Liver and pancreatic diseases have significant consequences on nutritional status, with direct effects on clinical outcomes, survival, and quality of life. Maintaining and preserving an adequate nutritional status is crucial and should be one of the goals of patients with liver or pancreatic disease. Thus, the nutritional status of such patients should be systematically assessed at follow-up. Recently, great progress has been made in this direction, and the relevant pathophysiological mechanisms have been better established. While the spectrum of these diseases is wide, and the mechanisms of the onset of malnutrition are numerous and interrelated, clinical and nutritional manifestations are common. The main consequences include an impaired dietary intake, altered macro and micronutrient metabolism, energy metabolism disturbances, an increase in energy expenditure, nutrient malabsorption, sarcopenia, and osteopathy. In this review, we summarize the factors contributing to malnutrition, and the effects on nutritional status and clinical outcomes of liver and pancreatic diseases. We explain the current knowledge on how to assess malnutrition and the efficacy of nutritional interventions in these settings.
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Affiliation(s)
- Pablo Cañamares-Orbis
- Unidad de Gastroenterología, Hepatología y Nutrición, Hospital Universitario San Jorge, 22004 Huesca, Spain;
| | - Vanesa Bernal-Monterde
- Servicio de Aparato Digestivo, Hospital Universitario Miguel Servet, 50009 Zaragoza, Spain; (V.B.-M.); (O.S.-G.); (D.C.-D.)
- Instituto de Investigación Sanitaria (IIS) Aragón, 50009 Zaragoza, Spain; (G.G.-R.); (L.C.)
| | - Olivia Sierra-Gabarda
- Servicio de Aparato Digestivo, Hospital Universitario Miguel Servet, 50009 Zaragoza, Spain; (V.B.-M.); (O.S.-G.); (D.C.-D.)
- Instituto de Investigación Sanitaria (IIS) Aragón, 50009 Zaragoza, Spain; (G.G.-R.); (L.C.)
| | - Diego Casas-Deza
- Servicio de Aparato Digestivo, Hospital Universitario Miguel Servet, 50009 Zaragoza, Spain; (V.B.-M.); (O.S.-G.); (D.C.-D.)
- Instituto de Investigación Sanitaria (IIS) Aragón, 50009 Zaragoza, Spain; (G.G.-R.); (L.C.)
| | - Guillermo Garcia-Rayado
- Instituto de Investigación Sanitaria (IIS) Aragón, 50009 Zaragoza, Spain; (G.G.-R.); (L.C.)
- Service of Digestive Diseases, Hospital Clínico Universitario Lozano Blesa, 50009 Zaragoza, Spain
| | - Luis Cortes
- Instituto de Investigación Sanitaria (IIS) Aragón, 50009 Zaragoza, Spain; (G.G.-R.); (L.C.)
- Service of Digestive Diseases, Hospital Clínico Universitario Lozano Blesa, 50009 Zaragoza, Spain
| | - Alberto Lué
- Unidad de Gastroenterología, Hepatología y Nutrición, Hospital Universitario San Jorge, 22004 Huesca, Spain;
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Cui J, Fu Y, Yi Z, Dong C, Liu H. The beneficial effects of ultraviolet light supplementation on bone density are associated with the intestinal flora in rats. Appl Microbiol Biotechnol 2021; 105:3705-3715. [PMID: 33893837 DOI: 10.1007/s00253-021-11282-2] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/17/2020] [Revised: 03/22/2021] [Accepted: 04/07/2021] [Indexed: 01/14/2023]
Abstract
The general public spends one-third of its time under artificial lighting, which lacks bands beneficial to human health, and long-term exposure will have a negative impact on bone health. Here, we report the effects of long-term, low-dose ultraviolet (UV) supplementation to white light-emitting diode (LED) light exposure on intestinal microorganisms and bone metabolism, as well as the correlations between the two. Normal and ovariectomized rats were irradiated with LED white light with or without supplementation with UV. The effects of UV supplementation on the intestinal flora and the relationship between the intestinal flora and bone were investigated by measuring the intestinal flora, bone metabolism markers, and bone histomorphology. UV supplementation affected the bone density and bone mass by changing the relative content of Firmicutes, Saccharibacteria, and Proteobacteria; however, the intestinal flora were not the only factors affecting bone. Ultraviolet supplementation changed the composition and function of the gut flora in the bone loss model. By increasing the synthesis of short-chain fatty acids and affecting immunomodulatory, intestinal flora directly or indirectly regulate the activity of osteoclasts and thus mediate UV-mediated improvements in bone metabolism. Our work shows that UV supplementation affects bone density by influencing the intestinal flora, introducing a novel strategy to develop healthier artificial light sources and prevent bone loss. KEY POINTS: • We measured the bone metabolism markers and bone histomorphometry of rats. • The diversity, composition, and function of intestinal flora were analyzed. • The relationship between gut microbiota and host bone physiology was analyzed.
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Affiliation(s)
- Jingjing Cui
- Key Laboratory for Biomechanics and Mechanobiology of the Ministry of Education, Beijing Advanced Innovation Centre for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, 100191, China.,International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing, 100191, China.,State Key Laboratory of Virtual Reality Technology and Systems, School of Computer Science and Engineering, Beihang University, No.37 Xueyuan Road, Beijing, 100083, China
| | - Yuming Fu
- Key Laboratory for Biomechanics and Mechanobiology of the Ministry of Education, Beijing Advanced Innovation Centre for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, 100191, China. .,International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing, 100191, China. .,State Key Laboratory of Virtual Reality Technology and Systems, School of Computer Science and Engineering, Beihang University, No.37 Xueyuan Road, Beijing, 100083, China.
| | - Zhihao Yi
- Key Laboratory for Biomechanics and Mechanobiology of the Ministry of Education, Beijing Advanced Innovation Centre for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, 100191, China.,International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing, 100191, China.,State Key Laboratory of Virtual Reality Technology and Systems, School of Computer Science and Engineering, Beihang University, No.37 Xueyuan Road, Beijing, 100083, China
| | - Chen Dong
- School of Sport Social Science, Shandong Sport University, Jinan, 250102, China
| | - Hong Liu
- Key Laboratory for Biomechanics and Mechanobiology of the Ministry of Education, Beijing Advanced Innovation Centre for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, 100191, China.,International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing, 100191, China.,State Key Laboratory of Virtual Reality Technology and Systems, School of Computer Science and Engineering, Beihang University, No.37 Xueyuan Road, Beijing, 100083, China
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Liu H, Xu Y, Cui Q, Liu N, Chu F, Cong B, Wu Y. Effect of Psoralen on the Intestinal Barrier and Alveolar Bone Loss in Rats With Chronic Periodontitis. Inflammation 2021; 44:1843-1855. [PMID: 33839980 DOI: 10.1007/s10753-021-01462-7] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/26/2021] [Revised: 03/29/2021] [Accepted: 04/01/2021] [Indexed: 12/25/2022]
Abstract
To study the effects of psoralen on the intestinal barrier and alveolar bone loss (ABL) in rats with chronic periodontitis. Fifty-two 8-week-old specific pathogen-free (SPF) male Sprague-Dawley (SD) rats were randomly divided into the following four groups: Control group (Control), psoralen group of healthy rats (Pso), periodontitis model group (Model), and psoralen group of periodontitis rats (Peri+Pso). The alveolar bone resorption of maxillary molars was observed via haematoxylin-eosin staining and micro-computed tomography. The expression level of receptor activator of nuclear factor-κB ligand (RANKL) and osteoprotegerin (OPG) in periodontal tissues was evaluated by immunofluorescence staining. The changes in serum tumour necrosis factor (TNF)-α, interleukin (IL)-10, IL-6, intestinal mucosal occludin, and claudin-5 were detected using enzyme-linked immunosorbent assay (ELISA). The level of intestinal mucosal NOD2 was detected using immunohistochemical methods. DNA was extracted from the intestinal contents and the 16s rRNA gene was sequenced using an Illumina MiSeq platform. The expression of NOD2 protein in the intestinal tract of periodontitis rats decreased after intragastric psoralen administration. Psoralen increased the intestinal microbiota diversity of rats. The level of serum pro-inflammatory factor TNF-α decreased and the level of anti-inflammatory factor IL-10 increased. ABL was observed to be significantly decreased in rats treated with psoralen. Psoralen decreased the RANKL/OPG ratio of periodontitis rats. Psoralen may affect the intestinal immune barrier and ecological barrier, mediate immune response, promote the secretion of anti-inflammatory factor IL-10, and reduce the secretion of the pro-inflammatory factor TNF-α, thus reducing ABL in experimental periodontitis in rats.
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Affiliation(s)
- Hua Liu
- Department of Stomatology, School of Stomatology of Qingdao University, Qingdao, 266003, Shandong Province, China
| | - Yingjie Xu
- Qingdao Stomatological Hospital Affiliated to Qingdao University, No.17 Dexian Road, Shinan District, Qingdao, 266001, Shandong Province, China
| | - Qi Cui
- Qingdao Stomatological Hospital Affiliated to Qingdao University, No.17 Dexian Road, Shinan District, Qingdao, 266001, Shandong Province, China
| | - Ning Liu
- Qingdao Stomatological Hospital Affiliated to Qingdao University, No.17 Dexian Road, Shinan District, Qingdao, 266001, Shandong Province, China
| | - Fuhang Chu
- Qingdao Stomatological Hospital Affiliated to Qingdao University, No.17 Dexian Road, Shinan District, Qingdao, 266001, Shandong Province, China
| | - Beibei Cong
- Qingdao Stomatological Hospital Affiliated to Qingdao University, No.17 Dexian Road, Shinan District, Qingdao, 266001, Shandong Province, China
| | - Yingtao Wu
- Qingdao Stomatological Hospital Affiliated to Qingdao University, No.17 Dexian Road, Shinan District, Qingdao, 266001, Shandong Province, China.
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Extra-skeletal effects of dietary calcium: Impact on the cardiovascular system, obesity, and cancer. ADVANCES IN FOOD AND NUTRITION RESEARCH 2021; 96:1-25. [PMID: 34112350 DOI: 10.1016/bs.afnr.2021.02.012] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/24/2022]
Abstract
Calcium is well known to be integral to bone and muscle health, with deleterious effects such as osteoporosis associated with inadequate calcium intake. Recent studies have also highlighted the significant effects of calcium in extra-musculoskeletal functioning, including the cardiovascular system, obesity, and cancer. Calcium impacts the cardiovascular system as an antagonist associated with a reduction in hypertension, increase vasodilation, and improvement in blood vessel function when obtained in the diet as an organic source, through food. However, the inorganic source of calcium, found in supplements, may be negatively associated with the cardiovascular system due to plaque deposits and atherogenesis when taken in excess. Some studies suggest that calcium intake may impact obesity by regulation of adipogenesis and reducing fat deposits with resulting weight loss. The pathogenesis of calcium for reducing obesity is thought to be related in part to its impact on gut microbiota profile, with the suggestion that calcium may have prebiotic properties. Animal and some human studies propose that calcium may also have a role in cancer prevention and/or treatment due to its function in the cell proliferation process and the impact on hormonal regulation, and thus warrants more investigations in the human population. Some prospective and small clinical studies suggest that calcium may be beneficial for colorectal cancer. Overall, emerging research in various areas continues to highlight the essentiality of dietary calcium for functioning at the molecular and biochemical level toward improvement in health and some chronic disease conditions.
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Lu Y, Yang J, Dong C, Fu Y, Liu H. Gut microbiome-mediated changes in bone metabolism upon infrared light exposure in rats. JOURNAL OF PHOTOCHEMISTRY AND PHOTOBIOLOGY B-BIOLOGY 2021; 217:112156. [PMID: 33647735 DOI: 10.1016/j.jphotobiol.2021.112156] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/11/2020] [Revised: 12/25/2020] [Accepted: 02/15/2021] [Indexed: 12/14/2022]
Abstract
Adequate sunlight exposure helps reduce bone loss and is important to bone health. Currently, about 90% of the world population spends a major portion of daily life under artificial lighting. Unlike sunlight, LED white light, the main source of artificial lighting, has no infrared radiation, which is known to be beneficial to human health. In artificial lighting environments, infrared supplementation may be used to simulate the effects of sunlight on bone metabolism. Here, we supplemented white LED exposure with infrared light in normal and ovariectomized rats for three consecutive months and examined bone turnover, bone mass, and bone density. We also analyzed the structure and function of gut microbiota in the rats. Infrared supplementation significantly reduced the abundance of Saccharibacteria and increased the abundance of Clostridiaceae 1 and Erysipelotrichaceae bacteria. Our results indicate that changes in the gut microbiome correlate well with bone mass and bone metabolism. Our work demonstrates that infrared supplementation can have a positive effect on rat bone metabolism by affecting gut microbiota. Our findings will be important considerations in the future design of healthy lighting environments that prevent or possibly ameliorate osteoporosis.
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Affiliation(s)
- Yueying Lu
- Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100191, China; International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing 100191, China; State Key Laboratory of Virtual Reality Technology and Systems, School of Computer Science and Engineering, Beihang University, Beijing 100083, China.
| | - Jianlou Yang
- Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100191, China; International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing 100191, China; State Key Laboratory of Virtual Reality Technology and Systems, School of Computer Science and Engineering, Beihang University, Beijing 100083, China
| | - Chen Dong
- Laboratory of Sport Nutrition and Intelligent Cooking, Shandong Sport University, Jinan 250102，China.
| | - Yuming Fu
- Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100191, China; International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing 100191, China; State Key Laboratory of Virtual Reality Technology and Systems, School of Computer Science and Engineering, Beihang University, Beijing 100083, China.
| | - Hong Liu
- Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing 100191, China; International Joint Research Center of Aerospace Biotechnology & Medical Engineering, Beihang University, Beijing 100191, China; State Key Laboratory of Virtual Reality Technology and Systems, School of Computer Science and Engineering, Beihang University, Beijing 100083, China.
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Liu J, Liu J, Liu L, Zhang G, Zhou A, Peng X. The gut microbiota alteration and the key bacteria in Astragalus polysaccharides (APS)-improved osteoporosis. Food Res Int 2020; 138:109811. [DOI: 10.1016/j.foodres.2020.109811] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/25/2020] [Revised: 10/11/2020] [Accepted: 10/13/2020] [Indexed: 12/16/2022]
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De Martinis M, Ginaldi L, Allegra A, Sirufo MM, Pioggia G, Tonacci A, Gangemi S. The Osteoporosis/Microbiota Linkage: The Role of miRNA. Int J Mol Sci 2020; 21:E8887. [PMID: 33255179 PMCID: PMC7727697 DOI: 10.3390/ijms21238887] [Citation(s) in RCA: 46] [Impact Index Per Article: 9.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/27/2020] [Revised: 11/18/2020] [Accepted: 11/23/2020] [Indexed: 02/07/2023] Open
Abstract
Hundreds of trillions of bacteria are present in the human body in a mutually beneficial symbiotic relationship with the host. A stable dynamic equilibrium exists in healthy individuals between the microbiota, host organism, and environment. Imbalances of the intestinal microbiota contribute to the determinism of various diseases. Recent research suggests that the microbiota is also involved in the regulation of the bone metabolism, and its alteration may induce osteoporosis. Due to modern molecular biotechnology, various mechanisms regulating the relationship between bone and microbiota are emerging. Understanding the role of microbiota imbalances in the development of osteoporosis is essential for the development of potential osteoporosis prevention and treatment strategies through microbiota targeting. A relevant complementary mechanism could be also constituted by the permanent relationships occurring between microbiota and microRNAs (miRNAs). miRNAs are a set of small non-coding RNAs able to regulate gene expression. In this review, we recapitulate the physiological and pathological meanings of the microbiota on osteoporosis onset by governing miRNA production. An improved comprehension of the relations between microbiota and miRNAs could furnish novel markers for the identification and monitoring of osteoporosis, and this appears to be an encouraging method for antagomir-guided tactics as therapeutic agents.
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Affiliation(s)
- Massimo De Martinis
- Department of Life, Health and Environmental Sciences, University of L’Aquila, 67100 L’Aquila, Italy; (L.G.); (M.M.S.)
- Allergy and Clinical Immunology Unit, Center for the Diagnosis and Treatment of Osteoporosis, AUSL 04 Teramo, 64100 Teramo, Italy
| | - Lia Ginaldi
- Department of Life, Health and Environmental Sciences, University of L’Aquila, 67100 L’Aquila, Italy; (L.G.); (M.M.S.)
- Allergy and Clinical Immunology Unit, Center for the Diagnosis and Treatment of Osteoporosis, AUSL 04 Teramo, 64100 Teramo, Italy
| | - Alessandro Allegra
- Division of Hematology, Department of Human Pathology in Adulthood and Childhood “Gaetano Barresi”, University of Messina, 98125 Messina, Italy;
| | - Maria Maddalena Sirufo
- Department of Life, Health and Environmental Sciences, University of L’Aquila, 67100 L’Aquila, Italy; (L.G.); (M.M.S.)
- Allergy and Clinical Immunology Unit, Center for the Diagnosis and Treatment of Osteoporosis, AUSL 04 Teramo, 64100 Teramo, Italy
| | - Giovanni Pioggia
- Institute for Biomedical Research and Innovation (IRIB), National Research Council of Italy (CNR), 98164 Messina, Italy;
| | - Alessandro Tonacci
- Clinical Physiology Institute, National Research Council of Italy (IFC-CNR), 56124 Pisa, Italy;
| | - Sebastiano Gangemi
- School and Operative Unit of Allergy and Clinical Immunology, Department of Clinical and Experimental Medicine, University of Messina, 98125 Messina, Italy;
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30
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Lee CS, Kim JY, Kim BK, Lee IO, Park NH, Kim SH. Lactobacillus-fermented milk products attenuate bone loss in an experimental rat model of ovariectomy-induced post-menopausal primary osteoporosis. J Appl Microbiol 2020; 130:2041-2062. [PMID: 32920885 DOI: 10.1111/jam.14852] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/09/2020] [Revised: 07/09/2020] [Accepted: 09/03/2020] [Indexed: 01/08/2023]
Abstract
AIM In this study, we investigated the anti-osteoporotic effect of two fermented milk products (FMPs) fermented by Lactobacillus plantarum A41 and Lactobacillus fermentum SRK414 on a rat model of ovariectomy-induced post-menopausal primary osteoporosis. METHODS AND RESULTS The two Lactobacillus FMPs increased the bone volume and bone mineral density (BMD) in ovariectomized (OVX) rats, and normalized the bone biomarkers in the serum. Additionally, they altered the gene expression levels of bone-metabolism-related markers. Furthermore, the two Lactobacillus FMPs downregulated bone-apoptosis-related genes stimulated by ovariectomy. Interestingly, the Lactobacillus FMPs decreased the levels of inflammation markers in the serum, bone, ileum and colon of the rats. Gut bacterial populations were also affected upon FMP treatment due to increase in the abundance of the genus Lactobacillus and Faecalibacterium prausnitzii. CONCLUSIONS Milk products fermented by L. plantarum A41 and L. fermentum SRK414 can exhibit anti-osteoporotic effects on post-menopausal osteoporosis via regulating the expression of bone-metabolism-related markers. SIGNIFICANCE AND IMPACT OF THE STUDY The two Lactobacillus FMPs used in the study can be an ideal method that has its potential of treating post-menopausal osteoporosis instead of drug treatments.
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Affiliation(s)
- C S Lee
- College of Life Sciences and Biotechnology, Korea University, Seoul, Republic of Korea.,Institute of Animal Molecular Biotechnology, Korea University, Seoul, Republic of Korea
| | - J-Y Kim
- College of Life Sciences and Biotechnology, Korea University, Seoul, Republic of Korea
| | - B K Kim
- Probiotic Research Laboratory, CKD Bio Research Institute, Ansan, Republic of Korea
| | - I O Lee
- Probiotic Research Laboratory, CKD Bio Research Institute, Ansan, Republic of Korea
| | - N H Park
- Probiotic Research Laboratory, CKD Bio Research Institute, Ansan, Republic of Korea
| | - S H Kim
- College of Life Sciences and Biotechnology, Korea University, Seoul, Republic of Korea.,Institute of Animal Molecular Biotechnology, Korea University, Seoul, Republic of Korea
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31
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A Multi-Omic Analysis for Low Bone Mineral Density in Postmenopausal Women Suggests a RELATIONSHIP between Diet, Metabolites, and Microbiota. Microorganisms 2020; 8:microorganisms8111630. [PMID: 33105628 PMCID: PMC7690388 DOI: 10.3390/microorganisms8111630] [Citation(s) in RCA: 31] [Impact Index Per Article: 6.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/09/2020] [Revised: 10/20/2020] [Accepted: 10/20/2020] [Indexed: 02/07/2023] Open
Abstract
The effect of microbiota composition and its health on bone tissue is a novel field for research. However, their associations with bone mineral density (BMD) have not been established in postmenopausal women. The present study investigates the relation of diet, the microbiota composition, and the serum metabolic profile in postmenopausal women with normal-BMD or with low-BMD. Ninety-two Mexican postmenopausal women were classified into normal-BMD (n = 34) and low-BMD (n = 58). The V4 hypervariable region was sequenced using the Miseq platform. Serum vitamin D was determined by chemiluminescence immunoassay. Serum concentrations of acyl-carnitines and amino acids were determined by electrospray tandem mass spectrometry. Diet was assessed by a food frequency questionnaire. The low-BMD group had fewer observed species, higher abundance of γ-Proteobacteria, lower consumption of lycopene, and lower concentrations of leucine, valine, and tyrosine compared with the normal-BMD group. These amino acids correlated positively with the abundance of Bacteroides. Lycopene consumption positively correlated with Oscillospira and negatively correlated with Pantoea genus abundance. Finally, the intestinal microbiota of women with vitamin D deficiency was related to Erysipelotrichaceae and Veillonellaceae abundance compared to the vitamin D non-deficient group. Associations mediated by the gut microbiota between diet and circulating metabolites with low-BMD were identified.
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32
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Liu S, Yuan X, Ma C, Zhao J, Xiong Z. 1H-NMR-based urinary metabolomic analysis for the preventive effects of gushudan on glucocorticoid-induced osteoporosis rats. Anal Biochem 2020; 610:113992. [PMID: 33075315 DOI: 10.1016/j.ab.2020.113992] [Citation(s) in RCA: 13] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/14/2020] [Revised: 10/08/2020] [Accepted: 10/08/2020] [Indexed: 12/13/2022]
Abstract
Gushudan (GSD), a traditional Chinese medicine with a history of more than 15 years, has been shown to have anti-osteoporosis effects, but the specific therapeutic mechanism behind it is still unclear. To further elucidate the pathogenesis of osteoporosis and the preventive mechanism of GSD on glucocorticoid-induced osteoporosis (GIOP) rats, a rapid and comprehensive 1H NMR metabolomics method was established to detect urinary metabolic profiles in the control group, model group and GSD treatment group in this study. The orthogonal partial least squares discriminant analysis (OPLS-DA) was performed to investigate changes in the metabolites, and related metabolic pathways were discovered using MetaboAnalyst platform. As a result, a total of 27 differential metabolites were identified. Of these, 17 metabolites such as formate, allantoin and l-threonate were newly discovered as GIOP potential biomarkers. Energy metabolism, intestinal flora metabolism, amino acid metabolism and oxidative stress response were significantly changed in the urinary profiles of GIOP rats, and GSD could play an anti-osteoporosis role by regulating these metabolic pathways. This study compliments the earlier LC-MS based urine metabolomics research, and helps further understand the pathogenesis of osteoporosis and the potential preventive effects of GSD on GIOP rats.
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Affiliation(s)
- Shuo Liu
- School of Pharmacy, Shenyang Pharmaceutical University, Benxi, 117004, PR China
| | - Xuemei Yuan
- School of Pharmacy, Shenyang Pharmaceutical University, Benxi, 117004, PR China
| | - Chang Ma
- School of Pharmacy, Shenyang Pharmaceutical University, Benxi, 117004, PR China
| | - Jing Zhao
- School of Pharmacy, Shenyang Pharmaceutical University, Benxi, 117004, PR China
| | - Zhili Xiong
- School of Pharmacy, Shenyang Pharmaceutical University, Benxi, 117004, PR China.
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33
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Fisher L, Fisher A, Smith PN. Helicobacter pylori Related Diseases and Osteoporotic Fractures (Narrative Review). J Clin Med 2020; 9:E3253. [PMID: 33053671 PMCID: PMC7600664 DOI: 10.3390/jcm9103253] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/21/2020] [Revised: 09/28/2020] [Accepted: 10/07/2020] [Indexed: 02/06/2023] Open
Abstract
Osteoporosis (OP) and osteoporotic fractures (OFs) are common multifactorial and heterogenic disorders of increasing incidence. Helicobacter pylori (H.p.) colonizes the stomach approximately in half of the world's population, causes gastroduodenal diseases and is prevalent in numerous extra-digestive diseases known to be associated with OP/OF. The studies regarding relationship between H.p. infection (HPI) and OP/OFs are inconsistent. The current review summarizes the relevant literature on the potential role of HPI in OP, falls and OFs and highlights the reasons for controversies in the publications. In the first section, after a brief overview of HPI biological features, we analyze the studies evaluating the association of HPI and bone status. The second part includes data on the prevalence of OP/OFs in HPI-induced gastroduodenal diseases (peptic ulcer, chronic/atrophic gastritis and cancer) and the effects of acid-suppressive drugs. In the next section, we discuss the possible contribution of HPI-associated extra-digestive diseases and medications to OP/OF, focusing on conditions affecting both bone homeostasis and predisposing to falls. In the last section, we describe clinical implications of accumulated data on HPI as a co-factor of OP/OF and present a feasible five-step algorithm for OP/OF risk assessment and management in regard to HPI, emphasizing the importance of an integrative (but differentiated) holistic approach. Increased awareness about the consequences of HPI linked to OP/OF can aid early detection and management. Further research on the HPI-OP/OF relationship is needed to close current knowledge gaps and improve clinical management of both OP/OF and HPI-related disorders.
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Affiliation(s)
- Leon Fisher
- Department of Gastroenterology, Frankston Hospital, Peninsula Health, Melbourne 3199, Australia
| | - Alexander Fisher
- Department of Geriatric Medicine, The Canberra Hospital, ACT Health, Canberra 2605, Australia;
- Department of Orthopedic Surgery, The Canberra Hospital, ACT Health, Canberra 2605, Australia;
- Australian National University Medical School, Canberra 2605, Australia
| | - Paul N Smith
- Department of Orthopedic Surgery, The Canberra Hospital, ACT Health, Canberra 2605, Australia;
- Australian National University Medical School, Canberra 2605, Australia
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34
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Elmassry MM, Chung E, Cao JJ, Hamood AN, Shen CL. Osteoprotective effect of green tea polyphenols and annatto-extracted tocotrienol in obese mice is associated with enhanced microbiome vitamin K 2 biosynthetic pathways. J Nutr Biochem 2020; 86:108492. [PMID: 32920088 DOI: 10.1016/j.jnutbio.2020.108492] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/16/2020] [Revised: 07/15/2020] [Accepted: 08/18/2020] [Indexed: 12/11/2022]
Abstract
The role of the gut microbiome in bone health has received significant attention in the past decade. We investigated the effects of green tea polyphenols (GTP) and annatto-extracted tocotrienols (AT) on bone properties and gut microbiome in obese mice. Male mice were assigned to a two (no AT vs. 400 mg/kg diet AT) × two (no GTP vs. 0.5% w/v GTP) factorial design, namely control, G, T, and G+T group respectively, for 14 weeks. The 4th lumbar vertebra (LV-4) and femur were harvested for bone microstructural analysis using μ-CT. Microbiome analysis using 16S rRNA gene sequencing of cecal feces was performed. AT increased bone volume at distal femur. GTP increased serum procollagen type 1 N-terminal propeptide concentration, bone volume at the distal femur and the LV-4, and trabecular number at distal femur; whereas GTP decreased trabecular separation at distal femur. Interactions between GTP and AT were observed in serum C-terminal telopeptide of type I collagen level (control>G=T=G+T) as well as the cortical bone area (control<G=T=G+T) and thickness (T≥G+T≥G≥control) at femur mid-diaphysis. Redundancy analysis showed a significant difference in the gut microbiome profile among different groups and the relative abundance of Akkermansia muciniphila, Clostridum saccharogumia, and Subdoligranulum variabile was increased in the GTP- and AT-supplemented groups. Functional profiling of the gut microbiome showed the combination of GTP and AT induced biosynthetic pathways for vitamin K2. Our results suggest that GTP and AT supplementation benefits bone properties in obese mice through modifying gut microbiome composition and function.
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Affiliation(s)
- Moamen M Elmassry
- Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409.
| | - Eunhee Chung
- Department of Kinesiology, Health, and Nutrition, University of Texas at San Antonio, San Antonio, TX 78249.
| | - Jay J Cao
- USDA ARS Grand Forks Human Nutrition Research Center, Grand Forks, ND 58203.
| | - Abdul N Hamood
- Department of Immunology and Molecular Microbiology, Texas Tech University Health Sciences Center, Lubbock, TX 79430; Department of Surgery, Texas Tech University Health Sciences Center, Lubbock, TX 79430.
| | - Chwan-Li Shen
- Department of Pathology, Texas Tech University Health Sciences Center, Lubbock, TX 79430; Center of Excellence for Integrative Health, Texas Tech University Health Sciences Center, Lubbock, TX 79430; Obesity Research Institute, Texas Tech University, Lubbock, TX 79409.
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35
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Gut microbiota: a perspective of precision medicine in endocrine disorders. J Diabetes Metab Disord 2020; 19:1827-1834. [PMID: 33520863 DOI: 10.1007/s40200-020-00593-2] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/30/2020] [Revised: 06/29/2020] [Accepted: 07/23/2020] [Indexed: 02/06/2023]
Abstract
Gut microbiota composition is unique in every individual, it impacts on organ functions that produce hormones. Gut microbiota composition balance is directly related to our general health status. This continual interaction between gut microbiota and endocrine organs sometimes can be considered as the etiology of diseases such as type 2 diabetes mellitus (T2DM), obesity, osteoporosis, polycystic ovary syndrome (PCOS), and thyroid diseases. Microbiota is introduced for a total collection of microbial organisms in our bodies and microbiome referred for their genome and their collective functions. Near 100 trillion microorganisms live in our body and almost all of them occupy the human gut gastrointestinal tract. Precision medicine can play a crucial role in health maintenance by affecting gut microbiota composition in every individual. It can also develop special treatments specifically for every individual. In this review, we addressed any correlation between gut microbiota and endocrine disorders including T2DM, obesity, PCOS, thyroid disorders and osteoporosis.
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36
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Chen C, Dong B, Wang Y, Zhang Q, Wang B, Feng S, Zhu Y. The role of Bacillus acidophilus in osteoporosis and its roles in proliferation and differentiation. J Clin Lab Anal 2020; 34:e23471. [PMID: 32779308 PMCID: PMC7676190 DOI: 10.1002/jcla.23471] [Citation(s) in RCA: 17] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/18/2020] [Revised: 05/31/2020] [Accepted: 06/23/2020] [Indexed: 12/16/2022] Open
Abstract
Background Osteoporosis is one of the most closely related diseases associated with the elderly. In recent years, the studies found that gut microbiota can cause osteoporosis. We evaluated the role of Bacillus acidophilus in osteoporosis and its roles in proliferation and differentiation. Methods We selected 5 healthy people and 10 osteoporosis patients and analyzed their level of 25‐hydroxyvitamin D and procollagen type I N‐terminal peptide (PINP), the characteristic of gut microbiota. The effect of lactobacillus acidophilus and Lactobacillus rhamnosus supernatant and butanoic acids on proliferation, differentiation, and maturity of osteoblasts MC3T3‐E1 and osteoclasts RAW 264.7 cells and the activity of alkaline phosphatase, concentration of osteocalcin, and the expression of RUNX2, RANK, NFATc1, cathepsin K, DC‐STAMP, OSCAR, WNT2, and CTNNB1 were measured in the above cell lines. Results The diversity of gut microbiota in osteoporosis patients is decreased and imbalanced with lower abundance of lactobacillus and butyric acid bacteria; meanwhile, 25‐hydroxyvitamin D and PINP of osteoporosis patient were significantly lower than the normal group. The proliferation, differentiation, and maturity of MC3T3‐E1 cells were stimulated; the activity of alkaline phosphatase, concentration of osteocalcin, and the expression of RUNX2, NFATc1, cathepsin K, DC‐STAMP, OSCAR, WNT2, and CTNNB1 were improved by supernatant of lactobacillus acidophilus, Lactobacillus rhamnosus and butanoic acids; however, the proliferation, differentiation, maturity, and the expression of RANK, NFATc1, cathepsin K, DC‐STAMP, OSCAR, WNT2, and CTNNB1 in RAW 264.7 cells were suppressed. Conclusions The lactobacillus acidophilus and Lactobacillus rhamnosus supernatant could stimulate the proliferation, differentiation, and maturation of osteoblasts; the production of butyric acid may be the potential mechanism.
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Affiliation(s)
- Chen Chen
- Department of Geriatric, Tianjin Medical University General Hospital, Tianjin, China
| | - Baokang Dong
- Department of Orthopedics, Tianjin First Center Hospital Tianjin, China
| | - Yuming Wang
- Department of Gastroenterology, Tianjin Medical University General Hospital, Tianjin, China
| | - Qiang Zhang
- Department of Geriatric, Tianjin Medical University General Hospital, Tianjin, China
| | - Bangmao Wang
- Department of Gastroenterology, Tianjin Medical University General Hospital, Tianjin, China
| | - Shuzhi Feng
- Department of Geriatric, Tianjin Medical University General Hospital, Tianjin, China
| | - Yu Zhu
- Department of Clinical Laboratory, Tianjin Haihe Hospital, Tianjin, China
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Vaiserman A, Romanenko M, Piven L, Moseiko V, Lushchak O, Kryzhanovska N, Guryanov V, Koliada A. Differences in the gut Firmicutes to Bacteroidetes ratio across age groups in healthy Ukrainian population. BMC Microbiol 2020; 20:221. [PMID: 32698765 PMCID: PMC7374892 DOI: 10.1186/s12866-020-01903-7] [Citation(s) in RCA: 120] [Impact Index Per Article: 24.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/01/2020] [Accepted: 07/14/2020] [Indexed: 02/07/2023] Open
Abstract
BACKGROUND Gut microbiota plays an important role in physiological and pathological processes of the host organism, including aging. Microbiota composition was shown to vary significantly throughout the life course. Age-related changes in the composition of microbiota were reported in several human studies. In present study, age-related dynamics of phylogenetic profile of gut microbiota was investigated in 1550 healthy participants from Ukrainian population. RESULTS Significant changes in the microbiota composition determined by qRT-PCR at the level of major microbial phyla across age groups have been observed. The relative abundance of Actinobacteria and Firmicutes phyla increased, while that of Bacteroidetes decreased from childhood to elderly age. Accordingly, the Firmicutes/Bacteroidetes (F/B) ratio was shown to significantly increase until elder age. In both sexes, odds to have F/B > 1 tended to increase with age, reaching maximum values in elder age groups [OR = 2.7 (95% CI, 1.2-6.0) and OR = 3.7 (95% CI, 1.4-9.6) for female and male 60-69-year age groups, respectively, compared to same-sex reference (0-9-year) age groups]. CONCLUSIONS In conclusion, data from our study indicate that composition of the human intestinal microbiota at the level of major microbial phyla significantly differs across age groups. In both sexes, the F/B ratio tends to increase with age from 0-9-year to 60-69-year age groups. Further studies are needed for a better understanding of mechanisms underlying age-related dynamics of human microbiota composition.
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Affiliation(s)
| | - Mariana Romanenko
- Institute of Gerontology, Vyshgorodskaya st. 67, Kyiv, 04114, Ukraine
| | - Liubov Piven
- Institute of Gerontology, Vyshgorodskaya st. 67, Kyiv, 04114, Ukraine
| | | | - Oleh Lushchak
- Vasyl Stefanyk Precarpathian National University, Ivano-Frankivsk, Ukraine
| | | | | | - Alexander Koliada
- Institute of Gerontology, Vyshgorodskaya st. 67, Kyiv, 04114, Ukraine
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Correa MJ, Giannuzzi L, Weisstaub AR, Zuleta A, Ferrero C. Chemically modified resistant starch in breadmaking: Impact on bone, mineral metabolism and gut health of growing
Wistar
rats. Int J Food Sci Technol 2019. [DOI: 10.1111/ijfs.14352] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/14/2022]
Affiliation(s)
- María Jimena Correa
- Centro de Investigación y Desarrollo en Criotecnología de Alimentos (CIDCA), Facultad de Ciencias Exactas‐UNLP, CIC, CONICET La Plata Argentina
| | - Leda Giannuzzi
- Centro de Investigación y Desarrollo en Criotecnología de Alimentos (CIDCA), Facultad de Ciencias Exactas‐UNLP, CIC, CONICET La Plata Argentina
| | - Adriana R. Weisstaub
- Departamento de Nutrición y Bromatología Facultad de Farmacia y Bioquímica Universidad de Buenos Aires Junín 956 Buenos Aires Argentina
| | - Angela Zuleta
- Departamento de Nutrición y Bromatología Facultad de Farmacia y Bioquímica Universidad de Buenos Aires Junín 956 Buenos Aires Argentina
| | - Cristina Ferrero
- Centro de Investigación y Desarrollo en Criotecnología de Alimentos (CIDCA), Facultad de Ciencias Exactas‐UNLP, CIC, CONICET La Plata Argentina
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Jeong HM, Kim DJ. Bone Diseases in Patients with Chronic Liver Disease. Int J Mol Sci 2019; 20:4270. [PMID: 31480433 PMCID: PMC6747370 DOI: 10.3390/ijms20174270] [Citation(s) in RCA: 64] [Impact Index Per Article: 10.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/08/2019] [Revised: 08/25/2019] [Accepted: 08/28/2019] [Indexed: 02/07/2023] Open
Abstract
Osteoporosis is a frequently observed complication in patients with chronic liver disease, particularly liver cirrhosis and cholestatic liver diseases. In addition, osteoporosis is critical in patients receiving a liver transplant. Nevertheless, few studies have evaluated bone diseases in patients with more frequently observed chronic liver disease, such as chronic viral hepatitis, nonalcoholic fatty liver disease and alcoholic liver disease. Osteoporosis is a disease caused by an imbalance in the activities of osteoblasts and osteoclasts. Over the last few decades, many advances have improved our knowledge of the pathogenesis of osteoporosis. Importantly, activated immune cells affect the progression of osteoporosis, and chronic inflammation may exert an additional effect on the existing pathophysiology of osteoporosis. The microbiota of the intestinal tract may also affect the progression of bone loss in patients with chronic liver disease. Recently, studies regarding the effects of chronic inflammation on dysbiosis in bone diseases have been conducted. However, mechanisms underlying osteoporosis in patients with chronic liver disease are complex and precise mechanisms remain unknown. The following special considerations in patients with chronic liver disease are reviewed: bone diseases in patients who underwent a liver transplant, the association between chronic hepatitis B virus infection treatment and bone diseases, the association between sarcopenia and bone diseases in patients with chronic liver disease, and the association between chronic liver disease and avascular necrosis of the hip. Few guidelines are currently available for the management of low bone mineral density or bone diseases in patients with chronic liver disease. Due to increased life expectancy and therapeutic advances in chronic liver disease, the importance of managing osteoporosis and other bone diseases in patients with chronic liver disease is expected to increase. Consequently, specific guidelines need to be established in the near future.
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Affiliation(s)
- Hae Min Jeong
- Department of Internal Medicine, Hallym University Chuncheon Sacred Heart Hospital, Chuncheon, Gangwon-do 24253, Korea
- Institute for Liver and Digestive Diseases, Hallym University, Chuncheon, Gangwon-do 24253, Korea
| | - Dong Joon Kim
- Institute for Liver and Digestive Diseases, Hallym University, Chuncheon, Gangwon-do 24253, Korea.
- Department of Internal Medicine, Hallym University College of Medicine, Seoul 05355, Korea.
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40
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Hao ML, Wang GY, Zuo XQ, Qu CJ, Yao BC, Wang DL. Gut microbiota: an overlooked factor that plays a significant role in osteoporosis. J Int Med Res 2019; 47:4095-4103. [PMID: 31436117 PMCID: PMC6753565 DOI: 10.1177/0300060519860027] [Citation(s) in RCA: 24] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/31/2022] Open
Abstract
Gut microbes are known as the body’s second gene pool. Symbiotic intestinal
bacteria play a major role in maintaining balance in humans. Bad eating habits,
antibiotic abuse, diseases, and a poor living environment have a negative effect
on intestinal flora. Abnormal intestinal microbes are prone to cause a variety
of diseases, affecting life expectancy and long-term quality of life, especially
in older people. Several recent studies have found a close association between
intestinal microorganisms and osteoporosis. The potential mechanism of
intestinal flora affecting bone formation or destruction by mediating nitric
oxide, the immune and endocrine systems, and other factors is briefly described
in this review. All of these factors may be responsible for the intestinal flora
that causes osteoporosis. Studying the relationship between intestinal flora and
bone health not only provides new ideas for studying the role of intestinal
microorganism in osteoporosis, but also provides a new therapeutic direction for
clinically refractory osteoporosis. Study of the relationship between intestinal
microbiota and osteoporosis is important for maintaining bone health and
minimizing osteoporosis.
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Affiliation(s)
- Meng-Lei Hao
- Department of Geriatric Medicine, Affiliated Hospital of Qinghai University, Xining, Qinghai Province, P.R. China
| | - Guang-Yao Wang
- Juxian Hospital of Traditional Chinese Medicine, Juxian, Shandong Provence, P.R. China
| | - Xiao-Qin Zuo
- Department of Geriatric Medicine, Affiliated Hospital of Qinghai University, Xining, Qinghai Province, P.R. China
| | - Chan-Juan Qu
- Department of Radiology, Peking Union Medical Hospital, Beijing, P.R. China
| | - Bo-Chen Yao
- Department of Cardiac Surgery, Tianjin Chest Hospital, Tianjin, P. R. China
| | - Dong-Lai Wang
- Department of Orthopedics, The Fourth Hospital of Hebei Medical University, Shijiazhuang, Hebei Provence, P.R. China
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