Does Helicobacter pylori infection play a role in iron deficiency anemia? A meta-analysis

Table 1 Summary characteristics of studies and participants

Ref.	Participants	Age group (yr)	Male (%)	Prevalence of H. pylori infection (%)		H. pylori test methods
Observational studies					Sampling mode
Milman et al[31]	2264	30-60	1153 (51)	32.0	Hospital/health examination	Serum IgG
Choe et al[32]	375	10-15	205 (55)	16.8	High school/questionnaires	Serum IgG
Cuoco et al[33]	362	16-58	115 (32)	21.0	Hospital diagnosed patients	Histological examination
Choe et al[34]	660	15-17	376 (57)	29.5	High school/physical examination	Serum IgG
Nahon et al[35]	210	57.4 (21.4) (SD)	80 (38)	NA	Hospital diagnosed patients	Histological examination
Choe et al[36]	937	10-18	475 (51)	20.8	-/physical examination	Serum IgG
Choi[37]	674	9-12	344 (51)	13.6	Middle-class families/physical examination	Serum IgG
Ciacci et al[38]	55	> 17	22 (40)	60.0	Hospital diagnosed patients	Histological examination/rapid urease test
Hershko et al[39]	210	16-77	NA	NA	Hospital diagnosed patients	UBT/Serum IgG
Gessner et al[40]	690	7-11	NA	87.0	8 most populous villages/physical examination	UBT
Baggett et al[41]	668	7-11	354 (53)	86.5	10 predominantly villages/physical examination	UBT
Cardenas et al[42]	7462	≥ 3	NA	27.1	NHANES/questionnaire, laboratory, examination data	Serum IgG
Süoglu et al[43]	70	4-16	NA	50.0	Hospital diagnosed patients	Histological examination
Haghi-Ashtiani et al[44]	209	2-14	111 (45)	47.8	Hospital diagnosed patients	Histological examination
Mulayim et al[45]	117	NA	0 (0)	61.5	Hospital diagnosed patients	UBT
Randomized controlled trials					Treatment therapies
Choe et al[46]	13	10-17	NA	19.7	B+A+M	Histology
Gessner et al[40]	201	7-11	NA	87.0	L+A+C	UBT
Chen et al[47]	86	18-76	50 (58)	NA	B+A+M	UBT
Vijayan et al[48]	22	> 13	NA	NA	L+T+C	Rapid urease test/histology
Sarker et al[49]	99	2-5	46 (46)	NA	O+A+C	UBT

UBT: Urea breath test; IgG: Immunoglobulin G; NHANES: National Health and Nutrition Examination Survey; B: Bismuth; A: Amoxicillin; M: Metronidazole; L: Lansoprazole; C: Clarithromycin; T: Tinidazole; O: Omeprazole.

Table 2 Methodological quality assessment based on MINORS¹

Source	Aim2	Rate3	Data4	Measure5	Bias6	Time7	Loss8	Size9	Total10
Milman et al[31]	2	2	2	2	2	1	1	0	12
Choe et al[32]	2	1	1	1	2	1	0	0	8
Cuoco et al[33]	1	1	1	2	2	0	0	1	8
Choe et al[34]	2	1	1	2	2	1	0	0	9
Nahon et al[35]	1	2	2	1	2	1	1	0	10
Choe et al[36]	2	2	1	1	0	0	0	0	6
Choi[37]	2	1	1	2	2	2	1	0	11
Ciacci et al[38]	1	1	2	1	2	1	0	0	8
Hershko et al[39]	1	1	1	1	2	1	1	0	8
Gessner et al[40]	2	2	2	1	2	2	2	1	14
Baggett et al[41]	2	1	2	1	2	1	1	0	10
Cardenas et al[42]	2	2	2	1	2	1	1	1	12
Süoglu et al[43]	1	1	1	1	2	1	0	0	7

¹Assessed with the adapted Methodological Index for Non-Randomized Studies (MINORS)[25];

²Clearly stated aim (0,1,2 points);

³Inclusion of consecutive patients and response rate (0,1,2);

⁴Prospective collection of data (0,1,2);

⁵Inclusion of employment measure (0,1,2);

⁶Unbiased assessment of study end points (0 or 2);

⁷Follow-up time appropriate (0,1,2);

⁸Loss to follow-up (0,1,2);

⁹Prospective calculation of the study size (0 or 1);

¹⁰Total: minimum equals 0; maximum equals 15 points.

Table 3 Quality evaluation of the included studies

RCT	Randomization	Blindness	Withdraw and dropout	Total
Choe et al[46]	2	2	0	4
Gessner et al[40]	2	1	1	4
Chen et al[47]	1	1	1	3
Vijayan et al[48]	2	2	1	5
Sarker et al[49]	2	0	1	3

Table 4 Summary of subgroup analyses of both observational studies and experimental studies

	Subjects (n)		95% CI	Heterogeneity (χ2)	P1
Observational studies		Odds ratio (OR)
H. pylori test methods
ELISA serum IgG	12372	2.16	1.49-3.14	9.27	0.10
Histological biopsy	906	2.17	0.90-5.26	28.85	< 0.0001
UBT	1475	5.88	2.27-15.23	1.53	0.47
Age
Child	1358	4.76	1.73-13.08	0.05	0.83
Adolescent	1972	2.85	1.68-4.31	0.22	0.89
Adult	3101	1.55	0.67-3.62	28.41	< 0.0001
Randomized controlled trials2		Weighted mean difference (WMD)
Hemoglobin (g/L)
Age
Child	300	0.65	-1.52-2.82	0.74	0.39
Adolescent and adult	35	25.03	9.69-40.37	0.67	0.41
Therapy
PPI	322	0.95	-2.98-4.87	3.71	0.16
Bismuth	13	32.00	9.37-54.63	-	-
H. pylori test methods
Histological biopsy	223	7.03	-9.41-23.47	2.79	0.10
UBT	35	25.03	9.69-40.37	0.67	0.41
Serum ferritin (μg/L)
Age
Child	300	0.70	-1.01-2.41	0.57	0.45
Adolescent and adult	121	14.79	2.53-27.05	17.91	0.0001
Therapy
PPI	322	7.15	-6.45-20.75	7.68	0.002
Bismuth	99	11.55	0.09-23.01	13.61	0.0002

¹P-value tested for heterogeneity of subgroups;

²Data were derived from hemoglobin changes and serum ferritin changes.