Fish consumption and risk of non-Hodgkin lymphoma: A meta-analysis of observational studies

Figures & data

Figure 1 High vs. low meta-analyses of fish intake and risk of non-Hodgkin lymphoma. Studies are subgrouped according to the design.

Table 1 Characteristics of studies of fish consumption and risk of non-Hodgkin lymphoma

Author/year/country	Study design	Case n, control, or participants, N	Type of questionnaire	Case ascertainment	Exposure details	RR (95% CI) (highest vs. lowest)	Adjustments
Chiu/1996/USA^Citation15	Cohort	N = 98 030	Self-administered, FFQ-126, validated	Cancer registries	Total fish	0.81(0.49–1.35)	Age, total energy intake
		n = 104			>6 vs. <4, servings/month
Fernandez/1999/Italy^Citation16	H-B	n = 200	Interviewer, FFQ 37 items, NA	Histological	Fresh fish	0.7 (0.5–1.1)	Age, sex, residence, education, smoking, alcohol consumption, BMI
		7990 controls			≥2 vs. <1, servings/week
Matsuo/2001/Japan^Citation17	H-B	n = 333	Self-administered questionnaire, NA	Histological	Total fish	0.89 (0.70–1.12)	Age. sex
		55904 controls			3–4 vs. less, servings/week
Cross/2006/USA^Citation18	P-B	n = 458	Self-completed FFQ-117, validated	Histological	Total fish	0.73 (0.49–1.10)	Age, sex, study site, physical activity, total caloric intake, alcohol consumption
		383 controls			Q4 vs. Q1
Hu/2008/ Canadia^Citation20	P-B	n = 1666	Self-completed FFQ-60, validated	Histological	Fresh fish	0.9 (0.7–1.1)	Age, province, education, BMI, alcohol use, smoking, vegetable and fruit intake, and total energy intake;
		5039 controls			≥0.9 vs. <0.5 Servings/week
CHIU/2008/USA^Citation19	P-B	n = 385	Self-completed FFQ-30, NA	Histological	Total fish	0.7 (0.4–1.5) t(14;18)-positive 0.5 (0.3, 1.0) t(14;18)-positive	Age, sex, type of respondent, family history of cancer, BMI
		1432 controls			≥1 vs. <0.5, servings/week
Daniel/2012/USA^Citation6	Cohort	N = 302 162	Self-completed FFQ-124, validated	Cancer registries	Total fish	1.07 (0.96–1.16)	Age, sex, education, family history of cancer, race, BMI, smoking, physical activity, intake of alcohol, fruit, vegetables, and total energy
		n = 3611			23.1 vs. 2.1 g/1000 kcal/day
Charbonneau/2013/USA^Citation14	H-B	n = 603	Self-administered FQ-128, validated	Histological	Fresh fish	0.61 (0.46–0.80)	Age, sex, total energy, residence
		1007 controls			>2.1 vs. none servings/month
Ollberding/2013/USA^Citation21	P-B	n = 336	Self-completed FFQ-117, validated	Histological	Total fish	0.8 (0.6–1.2)	Age, sex, education, total energy intake
		460 controls			>10.4 vs. <4.7 g/1000 kcal/day

H-B, hospital-based case–control study; P-B, population-based case–control study; BMI, body mass index; FFQ, food frequency questionnaire; NA, data not available.

Table 2 Stratified meta-analyses of fish consumption and risk of non-Hodgkin lymphoma

			Tests for heterogeneity
Characteristics	No. of studies	SRR (95% CI)	Q	Pheterogeneity	I^Citation2(%)	Pdifference
All	9	0.80 (0.68–0.94)	26.72	0.002	66.3
Design
Cohort	2	1.05 (0.90–1.22)	1.12	0.290	10.7	0.042
Case–control	7	0.77 (0.67–0.87)	8.39	0.300	16.5
Population-based	4	0.80 (0.68–0.94)	3.74	0.443	0
Hospital-based	3	0.73 (0.57–0.94)	4.30	0.117	53.5
Geographic locations
Italy	1	0.70 (0.68–1.45)	–	–	–	0.732
America	7	0.79 (0.64–0.98)	24.28	0.001	71.2
Japan	1	0.89 (0.70–1.12)	–	–	–
Validated FFQ
Yes	6	0.83 (0.67–1.02)	18.91	0.002	73.6	0.176
No	3	0.76 (0.61–0.95)	3.69	0.291	18.8
Adjustments
BMI, yes	4	0.84 (0.66–1.06)	12.15	0.016	67.1	0.430
No	5	0.77 (0.66–0.89)	4.33	0.363	7.6
Smoking, yes	3	0.93 (0.76–1.15)	5.66	0.059	64.7	0.085
No	6	0.75 (0.65–0.86)	6.2	0.401	3.2
Dietary energy intake, yes	6	0.83 (0.67–1.02)	18.91	0.002	73.6	0.176
No	3	0.76 (0.61–0.95)	3.69	0.291	18.8
Alcohol, yes	4	0.89 (0.73–1.10)	8.23	0.042	63.5	0.176
No	5	0.74 (0.63–0.88)	6.19	0.289	19.2

BMI, body mass index; FFQ, food frequency questionnaire. Note: Bold text indicates statistical significance

Figure 2 High vs. low meta-analyses of fish intake and risk of the subtypes of non-Hodgkin lymphoma. FL, follicular lymphoma; DLBCL, diffuse large B-cell lymphoma; SLL/CLL, small lymphocytic lymphoma/chronic lymphocytic leukemia.

Figure 3 Linear dose–response meta-analyses of fish intake (per three servings per week) and the risk of non-Hodgkin lymphoma.

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