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©The Author(s) 2024.
World J Gastrointest Oncol. Feb 15, 2024; 16(2): 514-526
Published online Feb 15, 2024. doi: 10.4251/wjgo.v16.i2.514
Published online Feb 15, 2024. doi: 10.4251/wjgo.v16.i2.514
Inclusion criteria | Exclusion criteria |
Cohort studies | Metastatic or recurrent disease |
Studies in English language | Patients receiving palliative care |
Studies published over the past 10 yr (2013 to 2023) | Cancer other than adenocarcinoma |
Adult patients (over 18 years old) | Case-control studies |
Patients with histologically confirmed esophagogastric or gastric adenocarcinoma | Commentaries or letters to the editor |
Open or laparoscopic gastrectomy | |
Effect of preoperative PNI on OS as primary outcome |
Ref. | Selection | Comparability | Outcomes | Total | |||||
Representativeness of the exposed cohort | Selection of the non exposed cohort | Ascertainment of exposure | Outcome of interest not present at the start of the study | Assessment of outcome | Length of follow-up | Adequacy of follow-up | |||
Hashimoto et al[21] | * | * | * | * | * | * | 6/8 | ||
Hirahara et al[31] | * | * | * | * | * | * | * | * | 8/8 |
Hirahara et al[22] | * | * | * | * | * | * | 6/8 | ||
Ishiguro et al[23] | * | * | * | * | * | * | * | 7/8 | |
Kudou et al[12] | * | * | * | * | * | * | * | * | 8/8 |
Lee et al[13] | * | * | * | * | * | * | * | * | 8/8 |
Lin et al[15] | * | * | * | * | * | * | * | * | 8/8 |
Liu et al[24] | * | * | * | * | * | * | * | 7/8 | |
Murakami et al[1] | * | * | * | * | * | * | * | 7/8 | |
Saito et al[25] | * | * | * | * | * | * | * | 7/8 | |
Shen et al[26] | * | * | * | * | * | * | * | * | 8/8 |
Takechi et al[17] | * | * | * | * | * | * | 6/8 | ||
Toyokawa et al[27] | * | * | * | * | * | * | * | * | 8/8 |
Toyokawa et al[28] | * | * | * | * | * | * | * | * | 8/8 |
Wu et al[29] | * | * | * | * | * | * | * | 7/8 | |
Xu et al[30] | * | * | * | * | * | * | * | * | 8/8 |
Ref. | Institute | Period | Patients number | Sex | Age (yr) |
Hashimoto et al[21] | Sasebo City General Hospital, Japan | 2013-2020 | 109 | 68 M, 41 F | 83 (80-94) |
Hirahara et al[31] | Department of Digestive and General Surgery, Shimane University, Japan | 2009-2016 | 218 | 145 M, 77 F | Low PNI group (n = 109): 78 (46-91). High PNI group (n = 259): 69 (36-89) |
Hirahara et al[22] | Department of Digestive and General Surgery, Shimane University, Japan | 2010-2016 | 368 | 254 M, 114 F | Absent postoperative complications group (n = 265): 70 (36-91). Present postoperative complications group (n = 103): 73 (41-90) |
Ishiguro et al[23] | Department of Surgery in Yokohama City, Japan | 2015-2021 | 258 | 183 M, 75 F | 31-88 |
Kudou et al[12] | Department of Surgery and Science, Kyushu University; Department of Gastroenterological Surgery, National Kyushu Medical Center, Japan | 2005-2016; 2010-2019 (respectively to the 2 institutes) | 206 | 151 M, 55 F | 66.3 (35-92) |
Lee et al[13] | Severance Hospital, South Korea | 2001-2010 | 7781 | 5150 M, 2631 F | 57.1 ± 11.9 |
Lin et al[15] | Fujian Medical University Union Hospital, China | 2009-2014 | 2182 | 1643 M, 539 F | 60.8 (54-68.3) |
Liu et al[24] | Sun Yat-sen University Cancer Center, China | 2000-2012 | 1330 | 905 M, 425 F | 59 (19-89) |
Murakami et al[1] | Tottori University Faculty of Medicine, Japan | 2001-2013 | 254 | 186 M, 68 F | > 70, n = 128; < 70, n = 126 |
Saito et al[25] | Division of Surgical Oncology, Department of Surgery, School of Medicine, Tottori University Faculty of Medicine, Japan | 2005-2013 | 453 | 331 M, 122 F | Low PNI group (n = 188): 73.5. High PNI group (n = 265): 63.5 |
Shen et al[26] | General Surgery Department of the Jinling Hospital, China | 2010-2018 | 525 | 387 M, 138 F | Training set (n = 369): 58.53 ± 10.14. Validation set (n = 156): 57.87 ± 10.28 |
Takechi et al[17] | Onomichi General Hospital, Hiroshima, Japan | 2011-2014 | 182 | 130 M, 52 F | 70 (38-91) |
Toyokawa et al[27] | Osaka City University Hospital, Japan | 1997-2012 | 240 | 168 M, 72 F | 64.5 (58-71.3) |
Toyokawa et al[28] | Osaka City University Hospital, Japan | 1997-2012 | 225 | 147 M, 78 F | 68 (60-75) |
Wu et al[29] | Affiliated Hospital of Jiangnan University, Jiangsu Province, China | 2015-2017 | 77 | 59 M, 18 F | 62.58 ± 8.97 |
Xu et al[30] | Shantou University Medical College’s cancer hospital, China | 2016-2020 | 236 | 171 M, 65 F | 43.68 ± 4.62 |
Ref. | Tumor location | TNM stage | Operation | Chemotherapy |
Hashimoto et al[21] | NS | I, n = 53 (48.6%). II, n = 31 (28.4%). III, n = 25 (22.9%) | Open surgery 54 (49.5%), laparoscopic 55 (50.5%). Distal/total/proximal gastrectomy: 70/37/2. D2 lymphadenectomy, n = 38 (34.9%) | Adjuvant 13 (11.9%). Neoadjuvant NS |
Hirahara et al[31] | EGJ, n = 6. Upper, n = 41. Middle, n = 91. Lower, n = 80 | Ia-Ib, n = 92, IIa-IIb, n = 51, IIIa-IIIc, n = 75. T1/2/3/4: 80/27/45/66. N0/1/2/3: 120/30/33/35 | Laparoscopic total/laparoscopic partial/laparoscopy assisted distal gastrectomy: 60/14/144 | Adjuvant: Yes n = 79, no n = 139. Neoadjuvant chemotherapy in the exclusion criteria |
Hirahara et al[22] | EGJ, n = 11. U, n = 70. M, n = 162. L, n = 125 | IA-IB, n = 217. IIA-IIB, n = 65. IIIC-IIIC, n = 86. T1/2/3/4: 192/48/54/74. N0/1/2/3: 244/40/42/42 | Laparoscopic total/laparoscopic partial/laparoscopy assisted distal gastrectomy: 82/37/249 | Adjuvant: Yes n = 100, no n = 268 |
Ishiguro et al[23] | Upper, n = 63 (24.4%). Middle, n = 113 (43.8%). Lower, n = 82 (31.8%) | T1, n = 138 (53.5%). T2 or T3, n = 120 (46.5%). Lymphatic invasion positive/negative: 90 (34.9%)/168 (65.1%) | Total/distal/partial gastrectomy: 66/180/11. D1+/D2 lymphadenectomy: 139/112 | 77% of the patients in the high PNI group and 47% in the low PNI group (amongst stages II and III patients) |
Kudou et al[12] | EGJ = 96, UGC = 110 | T1 97 (47.1%), T2 25 (12.1%), T3 55 (26.7%), T4 29 (14.1%). N0 136 (66.0%), N1 33 (16.0%), N2 13 (6.3%), N3 24 (11.7%). I/II/III: 113 (54.9%)/52 (25.2%)/41 (19.9%) | Total/proximal gastrectomy: 161/45. D1 lymphadenectomy (for T1 tumors), n = 97. D2 lymphadenectomy (for T2-4 tumors), n = 64 | Adjuvant: Yes, n = 51 (24.8%), no, n = 155 (75.2%). Neoadjuvant chemotherapy in the exclusion criteria |
Lee et al[13] | NS | T1 4182 (53.8%), T2 944 (12.1%), T3 913 (11.7%), T4a 1700 (21.9%), T4b 42 (0.5%). N0 4967 (63.8%), N1 941 (12.1%), N2 798 (10.3%), N3 1075 (13.8%). Stage I 4608 (59.2%), II 1286 (16.5%), III 1887 (24.3%) | Subtotal gastrectomy 5895 (75.8%). Total gastrectomy 1886 (24.2%) | Patients with stage II or higher disease were recommended for adjuvant chemotherapy (numbers not mentioned). Neoadjuvant chemotherapy in the exclusion criteria |
Lin et al[15] | Upper 521 (23.9%). Middle 465 (21.3%). Lower 923 (42.3%). Mixed 273 (12.5%) | TNM stage: I 632 (29.0), II 526 (24.1), III 1024 (46.9) | Total gastrectomy 1134 (52.0%). Distal gastrectomy 998 (45.7%). Proximal gastrectomy 50 (2.3%) | 1223 patients (56%): Adjuvant chemotherapy n = 1223 (56%). Neoadjuvant chemotherapy NS |
Liu et al[24] | Upper third 511 (38.4%). Middle third 278 (20.9%). Lower third 541 (40.7%) | I 220 (16.5%). II 334 (25.1%). III 776 (58.3%) | D2 gastrectomy with R0 resection | Adjuvant chemotherapy n = 817. Neoadjuvant chemotherapy in the exclusion criteria |
Murakami et al[1] | NS | T1 n = 147, T2/3/4 n = 107. N0 n = 181, N1/2/3 n = 73. Stage I n = 161, II/III n = 93 | Distal/proximal gastrectomy n = 181, total gastrectomy n = 73. D0/1/1+ lymphadenectomy n = 171, D2 lymphadenectomy n = 83 | NS |
Saito et al[25] | NS | T1 n = 284, T2/3/4 n = 169. Lymph node metastasis absent/present: 343/110 | Curative gastrectomy (R0 resection) with regional dissection of lymph nodes. Partial/proximal/total gastrectomy: 311/42/100 | Adjuvant chemotherapy n = 64, neoadjuvant chemotherapy n = 5, perioperative chemotherapy n = 10 |
Shen et al[26] | Upper 158. Middle 202. Lower 165 | Training/validation set: I 138 (37.40%)/64 (41.03%), II 84 (22.76%)/39 (25.00%), III 147 (39.84%)/53 (33.97%) | Robotic gastrectomy proximal/distal/total: 110/272/143 | Neoadjuvant chemotherapy n = 116, adjuvant n = 267 |
Takechi et al[17] | NS | Stage: I n = 114 (62.6%), II n = 38 (20.9%), III n = 30 (16.5%) | Distal/total/proximal gastrectomy: 124 (68.1%)/51 (28%)/7 (3.8%). D1/D1+/D2 lymphadenectomy: 32 (17.6%)/74 (40.7%)/76 (41.8%) | Postoperative patients with stages II and III GC n = 33 (18.1%). Neoadjuvant NS |
Toyokawa et al[27] | Upper n = 57 (23.8%). Middle n = 98 (40.8%). Lower n = 83 (34.6%). Whole n = 2 (0.8%) | Only stage II patients: IIA n = 111 (46.3%), IIB n = 129 (53.7%) | Total/proximal/distal gastrectomy: 72/1/167 | Adjuvant chemotherapy: Yes 62/no 178. Neoadjuvant in the exclusion criteria |
Toyokawa et al[28] | Upper/middle/lower n = 209 (92.9%). Whole 16 (7.1%) | IIIA 80 (35.6%), IIIB 72 (32.0%), IIIC 73 (32.4%) | Total/distal gastrectomy: 108 (48%)/117 (52%) | Adjuvant chemotherapy: Yes 41 (18.2%)/no 184 (81.8%) |
Wu et al[29] | NS | Only stage III: n = 77 (100%) | Partial gastrectomy (n = 15), total gastrectomy (n = 62) | The average number of chemotherapy cycles was 6.77 ± 4.14, and all patients completed > 2 chemotherapy cycles. Neoadjuvant chemotherapy in the exclusion criteria |
Xu et al[30] | EGJ | I 48 (20.3%), II 53 (22.4%), III 135 (57.2%) | Curative gastro-esophageal resection with R0 resection | NS |
Ref. | PNI calculation | PNI cut-off value and groups | PNI range | Follow up (months) | Outcome |
Hashimoto et al[21] | ROC curve analysis | 44.2. PNI > 44.2 (n = 72), PNI < 44.2 (n = 37) | NS | 23.9 (0.4-81.9) | The 30-d, 180-d, 1-yr, and 3-yr cumulative OS rates were 100%, 97.0%, 91.6%, and 74.7%, respectively |
Hirahara et al[31] | ROC curve analysis | 44.3. PNI < 44.3 (n = 109), PNI > 44.3, n = 109 | NS | Observation period from date of surgery till day of death | 5-yr OS: Low PNI, 50.9%; high PNI, 73.6% (P < 0.001). In elderly patients (age > 70) 5-yr OS: Low PNI 52.5%, high PNI 82.5%. Non elderly patients (age < 70), 5-yr OS: Low PNI 46.6%, high PNI 54.7% |
Hirahara et al[22] | ROC curve analysis | 44.5. PNI < 44.5 n = 114, PNI > 44.5, n = 254 | NS | NS | NS |
Ishiguro et al[23] | Set according to previous reports | 47. PNI < 47 (n = 75), PNI > 47 (n = 183) | NS | NS | 5-yr OS: A: 44.7%; B: 77.2% (P < 0.001) |
Kudou et al[12] | ROC curve analysis | 44.7. PNI < 44.7 (n = 167, 81.1%), PNI > 44.7 (n = 39, 18.9%) | NS | 60 | Worse 5-year OS rates were associated with PNI < 44.7 (vs > 44.7) (OS: 41.7% vs 84.5%, HR = 5.460, P < 0.0001). In subgroup analysis PNI < 44.7 (vs > 44.7) was significantly associated with poor prognosis in patients with stages II and III disease |
Lee et al[13] | ROC curve analysis | 46.7. PNI < 46,7 (n = 779), PNI > 46,7, n = 7002 | 54.2 ± 5.9 | 60 | The low PNI group had a poor prognosis for all stages of disease (for all stages and stages I, II, and III: P < 0.001) |
Lin et al[15] | Set according to previous reports | 46. PNI ≤ 46 (n = 1348, (61.8%), PNI > 46 (n = 834, 38.2%) | NS | 52 (1-118) | Low PNI 5-yr OS = 55.5%, high PNI 5-yr OS = 75.4% |
Liu et al[24] | Set according to previous reports | 45. Low PNI group PNI < 45. Number of patients NS | 35 (range 1-179). Final follow-up June 2015, 806 patients were alive by then | NS | |
Murakami et al[1] | ROC curve analysis | Preoperative PNI of ≥ 52 (pre-PNIhigh) n = 82, preoperative PNI < 52 (pre-PNIlow) n = 172, postoperative PNI ≥ 49 (post-PNIhigh) n = 95, postoperative PNI < 49 (pre-PNIlow) n = 159. Group A, patients with pre-PNIhigh and post-PNIhigh; group B, patients with either pre-PNIhigh and post-PNIlow or pre-PNIlow and post-PNIhigh; group C, patients with pre-PNIlow and post-PNIlow | Preoperative PNI range 30.6-63.6. Postoperative range 24.2-61.7 | NS | 5-yr OS prePNIhigh 95.8%, prePNIlow 70% (P < 0.0001). 5-yr OS postPNIhigh 91.4%, postPNIlow 70.1% (P < 0.0001). 5-yr OS prePNIlow and postPNIhigh 80.1%, prePNIlow and postPNIlow 67.1% (P = 0.031). 5-yr OS prePNIhigh and postPNIhigh 100%, prePNIhigh and postPNIlow 83.4% (P = 0.0021) |
Saito et al[25] | ROC curve analysis | 46.7. PNI ≥ 46.7 (n = 265, 58.5%) and PNI < 46.7 (PNIlow, n = 188, 41.5%) | Range 27.7-63.6 | NS | 5-yr OS PNIlow 59.5%, PNIhigh 88.2% (P < 0.0001) |
Shen et al[26] | X-tile 3.6.1 software1 (Yale University, New Haven, CT, United States) | 45.39. Training set low PNI n = 48 (13.01%), high PNI 321 (86.99%), validation set low PNI n = 29 (18.59%), high PNI n = 127 (81.41%). Patients were randomly divided into the training set and the validation set at a 7:3 ratio | NS | 41 (range 2-102) training set and 38 (range 1-101) validation set | 3-yr and 5-yr OS rates were 80.9% and 74.8% in the training set, and 81.6% and 73.5% in the validation set |
Takechi et al[17] | Set according to previous reports | 45. PNI < 45 (n = 97), PNI ≥ 45 (n = 85) | NS | 39 (range, 1-72) | NS |
Toyokawa et al[27] | ROC curve analysis | 49.2. PNI ≤ 49.2 (n = 136), PNI > 49.2) (n = 104) | NS | 100.5 (70.0-136.8) | The 5-yr OS rate for the entire study population was 78.8% |
Toyokawa et al[28] | ROC curve analysis | 45.6. PNI ≤ 45.6 (n = 90, 40%), PNI > 45.6 (n = 135, 60%) | 46.8 (IQR: 42.5-49.9) | Median 80 (69-124) | The 5-yr OS rate for the entire study population was 48.7%. |
Wu et al[29] | ROC curve analysis | 42.3. Low PNI group PNI < 42.3. Number of patients NS | NS | Shortest 30, longest 64 | 3-yr OS low PNI group < 40%, high PNI group > 60%. Exact number NS (only survival curves available) |
Xu et al[30] | ROC curve analysis | 45.6. Propensity matching patients. PNI < 45.6 (n = 58), PNI > 45.6 (n = 85) | NS | Every 3 months first 2 yr, every 12 months for 3rd-5th yr, once per year after that. Final follow-up December 2022 | Low PNI group had a 5-yr OS rate of 46.9%, high PNI group had a 5-yr OS rate of 71.30% |
Ref. | Univariate analysis | Multivariate analysis |
Hashimoto et al[21] | Low PNI associated with poor OS (P = 0.049) | Low PNI was an independent prognostic factor for poor OS (P = 0.044) |
Hirahara et al[31] | Low PNI value was a significant risk factor for shorter OS (P < 0.001) | PNI was confirmed as an independent prognostic factor for OS (P < 0.001) |
Hirahara et al[22] | PNI was significantly associated with OS (HR = 3.316, 95%CI: 2.133-5.196, P < 0.001) | In patients with high PNI, only CEA was was independently associated with OS (P = 0.002) |
Ishiguro et al[23] | PNI was significantly associated with OS (P < 0.001) | PNI was an independent predictor of OS (HR = 3.452, 95%CI: 2.042-5.836, P = 0.007) |
Kudou et al[12] | PNI < 44.7 (vs > 44.7) was associated with worse OS (P < 0.0001) | PNI (P < 0.0001, HR = 8.946) was independently associated with OS |
Lee et al[13] | Low PNI was significantly associated with worse OS (HR = 2.864, 95%CI: 2.544-3.223, P < 0.001) | Low PNI was independently associated with OS (HR = 1.383, 95%CI: 1.221-1.568, P < 0.001) |
Lin et al[15] | PNI was significantly associated with OS (P < 0.001) | PNI was independently associated with OS (P = 0.004) and the 5-yr OS rate in the low PNI group was significantly lower than that in the normal PNI group (55.5% vs 75.4%, P < 0.05) |
Liu et al[24] | PNI was associated with OS (HR = 1.627, 95%CI: 1.274-2.078, P < 0.001) | PNI (HR = 1.356, 95%CI: 1.051-1.748, P = 0.019) was independently associated with OS. In stage stratified analysis PNI was not significantly associated with OS |
Murakami et al[1] | 5-yr survival rates were 100.0, 83.0, and 67.1% for groups A, B, and C, respectively | 5-yr OS 100%, 92.4%, and 78.3% for groups A, B, and C, respectively, in non-elderly patients (age < 70) (P = 0.017). 5-yr OS 100%, 75.1%, and 59% for groups A, B, and C, respectively, for elderly patients (age > 70) (P = 0.0029). Group stratification mentioned in Table 4 |
Saito et al[25] | NS | 5-yr OS PNI low group 59.5%, PNI high group 88.2% (P < 0.0001). Median age of the PNI high group (63.5 yr) was significantly younger than of the PNI low group (73.5 yr) |
Shen et al[26] | PNI was an independent prognostic factor for OS. PNI (≤ 45.39 vs > 45.39) (HR = 0.439, 95%CI: 0.236-0.734, P = 0.002) | PNI was an independent prognostic factor for OS. PNI (≤ 45.39 vs > 45.39) (HR = 0.553, 95%CI: 0.306-0.993, P = 0.048) |
Takechi et al[17] | Low PNI was significantly associated with worse OS (HR = 4.261, 95%CI: 1.734-10.47, P = 0.002). Stage I GC patients in the high PNI group showed significantly better OS than patients in the low PNI group (P < 0.001). No significant difference in OS between PNI groups in stage II and III GC patients | Only PNI score was an independent prognostic factor for OS (HR = 2.889, 95%CI: 1.104-7.563, P = 0.031) |
Toyokawa et al[27] | PNI was significantly associated with OS (HR = 0.381, 95%CI: 0.219-0.662, P = 0.001) | PNI was an independent prognostic factor for OS (HR = 0.415, 95%CI: 0.234-0.736, P = 0.003) |
Toyokawa et al[28] | PNI was not significantly associated with OS (P = 0.073) | PNI was not significantly associated with OS (P = 0.676) |
Wu et al[29] | - | The group with high pre-chemotherapy PNI values had significantly better overall survival than the group with low pre-chemotherapy PNI values (HR = 0.485, 95%CI: 0.255-0.920; P = 0.027) |
Xu et al[30] | Lower PNI was a significant predictor of shorter OS (P = 0.004) | In comparison to the high PNI group, the hazard of endpoint mortality was 2.442 times greater in the low PNI group (P = 0.003) |
- Citation: Fiflis S, Christodoulidis G, Papakonstantinou M, Giakoustidis A, Koukias S, Roussos P, Kouliou MN, Koumarelas KE, Giakoustidis D. Prognostic nutritional index in predicting survival of patients with gastric or gastroesophageal junction adenocarcinoma: A systematic review. World J Gastrointest Oncol 2024; 16(2): 514-526
- URL: https://www.wjgnet.com/1948-5204/full/v16/i2/514.htm
- DOI: https://dx.doi.org/10.4251/wjgo.v16.i2.514