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Table 1 Characteristics of included studies according to report type

From: The relationship between physical activity and lymphoma: a systematic review and meta analysis

Authors, year, gender

Study Region

Case number Controls or cohort values

Median age, years (SD)

Lymphoma subtype

Physical activity domain, timing, definition of high vs. low PA

RR/OR/HR (95% CI), high vs. low PA

Adjustment Factors

Cohort Studies

 Barberio et al., 2018 [17] Men and women combined

Canada (North America)

91 (NHL) 285,787 person-years follow up

M: 57.8 (8.2) W: 55.9 (9.0) *all cancer cases

NHL

Total, recent (201.2–535.3 vs. 0–113.7 MET hours/wk)

HR 0.73 (0.40–1.36)

Age, sex, ethnicity (white/other), marital status, education level, total household income, geographic area of residence (urban/rural), smoking status, mean alcohol intake (g/d), mean energy intake (kCal/day), self-reported BMI, history of cardiovascular or respiratory condition, family history of cancer (breast or endometrial if female), other PA

Recreational, recent (35–255.3 vs. 0–7.4 MET hours/wk)

HR 0.86 (0.45–1.65)

Occupational, recent (116.8–463.4 vs. 0–34.6 MET hours/wk)

HR 0.68 (0.35–1.31)

 Cerhan et al., 2002 [22] Women

USA (North America)

261 (NHL) 137 (DLBCL) 58 (FL) 37,932 cohort 449,801 person years of follow up

61.7 (no SD reported)

NHL DLBCL FL

Recreational, recent (High vs. low)

NHL: RR 0.84 (0.62–1.15)

Age

DLBCL: RR 1.0 (0.66–1.52)

FL: RR 0.58 (0.29–0.18)

 Kabat et al., 2012 [23] Women

USA (North America)

1123 (NHL) 302 (DLBCL) 214 (FL) 298 (CLL/SLL) 157,852 cohort

Cases: 65.2 (6.9) Non-cases 63.2 (7.2)

NHL DLBCL FL CLL/SLL

Recreational, recent (≥17.5 vs. < 1.6 MET hours/wk)

NHL: HR 1.17 (0.98–1.39)

Age (continuous), alcohol intake, smoking (pack-years), caloric intake, education level, race/ethnicity, BMI, enrollment in OS/treatment arm assignment

DLBCL: HR 1.03 (0.73–1.45)

FL: HR 1.22 (0.83–1.80)

CLL/SLL: HR

1.18 (0.84–1.66)

 Lim et al., 2007 [24] Men and women combined

USA (North America)

1381 (NHL) 58 (HL) 472,545 non-cases

60.9–62.5 depending on covariate classification

NHL DLBCL FL CLL/SLL T cell HL

Recreational, recent (NHL ≥5 vs. < 1x/wk.; HL 3- ≥ 5 vs. < 1/wk. activities ≥20 min with increased heart rate and sweating)

NHL: RR 0.97 (0.81–1.16)

Age, race, education, BMI, caloric intake

DLBCL: RR 0.87 (0.61–1.25)

FL: RR 0.96 (0.63–1.46)

CLL/SLL: RR 0.80 (0.51–1.25)

T-cell: RR 1.25 (0.62–2.49)

HL: RR 1.60 (0.72–3.54)

 Lu et al., 2009 [25] Women

USA (North America)

574 (NHL) 155 (DLBCL) 121 (FL) 124 (CLL/SLL) 120,642 cohort

Cohort entry: 52.7 Diagnosis: 69.5

NHL DLBCL FL CLL/SLL

Recreational, lifetime

NHL: RR 1.00 (0.78–1.29)

Height, weight at cohort entry, age at menarche; recent PA also adjusted for long-term strenuous and moderate exercise

DLBCL: RR 0.97 (0.60–1.55)

FL: RR 1.29 (0.69–2.41)

CLL/SLL: RR 0.94 (0.55–1.60)

Recreational, Recent (≥4 vs. 0–0.5 h/wk./year of strenuous activity)

NHL: RR 1.11 (0.86–1.44)

DLBCL: RR 1.00 (0.62–1.62)

FL: RR 1.01 (0.57–1.79)

CLL/SLL: RR 1.50 (0.86–2.63)

 Pukkala et al., 2000 [26] Men

Finland (Europe)

6 (NHL) 3 (HL) 53,501 person years follow up

Modal age category 45–59 years

NHL HL

Recreational, lifetime (Athletes vs. Finnish population)

NHL: SIR 0.78 (0.29–1.70)

None

HL: SIR 1.33 (0.27–3.88)

 Teras et al., 2012 [27] Men Women

USA (North America)

2002 (NHL) 435 (DLBCL) 280 (FL) 482 (CLL/SLL) 326 (B-NHL) 110 (T-NHL) 26 (NHL NOS) 184,190 cohort

62.9 (6.4)

NHL DLBCL FL, CLL/SLL B-NHL T-NHL NHL NOS

Recreational, recent (≥17.5 vs. 0 MET hours/wk)

NHL- M: HR 1.02 (0.82–1.26) W: HR 0.69 (0.54–0.89)

Age at baseline, family history of hematopoietic cancer, education, smoking status, alcohol intake, height, BMI, sitting time

DLBCL- M: HR 1.14 (0.70–1.88) W: HR 0.71 (0.44–1.16)

CLL/SLL-M: HR 0.95 (0.62–1.46) W: HR 0.73 (0.44–1.20)

FL- M: HR 0.86 (0.49–1.51) W: HR 0.77 (0.41–1.43)

 Van Veldhoven et al., 2011 [28] Men Women Men and women combined

Europe

778 (NHL) 94 (DLBCL) 98 (FL) 142 (B-CLL) 109 (B-NOS) 521,457 cohort

Age at recruitment: 52.9 (9.8) men, 51.0 (10.9) women

NHL DLBCL FL B-CLL B-NOS

Total, recent (Active vs. inactive)

NHL- M: HR 0.83 (0.31–2.24) W: HR 1.50 (0.45–5)

Hypertension, hyperlipidemia, education, diabetes; age and centre stratified *No adjustment for subtypes of NHL

DLBCL- M: HR 2.03 (0.38–10.79) W: HR 5.03 (1.19–21.33)

FL- M: HR 2.82 (0.52–15.23) W: HR 2.59 (0.54–12.38)

B-CLL- M: HR 0.76 (0.23–2.53) W: HR 10.95 (1.55–77.48)

B-NOS- M: HR 0.16 (0.01–1.95) W: HR 1.60 (0.20–12.52)

Occupational, recent (Manual/heavy labor vs. sedentary)

NHL- M: HR 1.05 (0.46–2.41) W: HR 2.06 (0.65–6.51)

Recreational, recent (≥45.75 vs. < 14.25 MET hours/wk)

NHL- M: HR 1.11 (0.49–2.52) W: HR 1.25 (0.49–3.16)

 Walter et al., 2013 [18] Men and women combined

USA (North America)

441 (Mature B cell) 104 (CLL) 257 (Other mature B cell) 22 (HL) 65,322 cohort

61.5 (7.4)

Mature B cell neoplasms (including plasma cell disorders) CLL Other mature B cell

Recreational, lifetime (> 4.8 vs. 0.2–1.8 MET hours/wk)

*not reported for mature B cell

Age, sex, race/ethnicity, education, smoking, BMI at baseline, fatigue/lack of energy, self reported health, daily fruit consumption, daily vegetable consumption, history of anemia in year before baseline, family history of leukemia or lymphoma

CLL: HR 0.52 (0.26–1.03)

Other mature B cell: HR 0.80 (0.53–1.22)

Case- Control Studies

 Boyle et al., 2015 [15] Men Women Men and women combined

Canada (North America)

749 (NHL) 202 (DLBCL) 188 (FL) 268 (Other B cell) 70 (T cell) 818 controls

Modal age category 70+ years (cases), 60–69 years (controls)

NHL DLBCL FL Other B cell T cell

Total non-occupational, lifetime (≥85 vs. 0–35.9 MET hours/wk)

NHL- M/W: OR 1.16 (0.87–1.55) M: OR 1.14 (0.78–1.68) W: OR 1.07 (0.68–1.68)

Age group, sex, residential location, ethnicity

DLBCL: OR 1.22 (0.79–1.88)

FL: OR 1.26 (0.80–1.99)

Other B cell: OR 1.04 (0.69–1.57)

T cell: OR 1.19 (0.61–2.32)

 Brownson et al., 1991 [29] Men

USA (North America)

536 (NHL) 16,611 controls

Not reported

NHL

Occupational, recent (> 80% vs. < 20% active at work)

OR 0.83 (0.56–1.25)

Age, smoking

 Cerhan et al., 2005 [30] Men and women combined

USA (North America)

562 (NHL) 32 (DLBCL) 24 (FL) 468 controls* *Population with PA data (Total cases 1321, controls 1057 in study)

Cases: 56.1 years (12.9) Controls: 59.7 years (11.7)

NHL DLBCL FL

Occupational, lifetime (Mostly exercise vs. mostly sit at work)

NHL: OR 0.98 (0.55–1.74)

Age, sex, race and study center, BMI, height

DLBCL: OR 1.32 (0.63–2.76)

FL: OR 1.04 (0.45–2.37)

Non-occupational, lifetime (> 1080 vs. 0 MET hours/wk)

NHL: OR 0.83 (0.50–1.38)

DLBCL: OR 0.82 (0.41–1.66)

FL: OR 0.85 (0.39–1.83)

 Etter et al., 2018 [16] Men Women

USA (North America)

236 (NHL) 87 (HL) Controls 952 (NHL); 348 (HL)

NHL: 56.31 (15.42)

NHL HL

Recreational, lifetime (≥1 vs. < 1 exercise session/wk)

NHL: OR 0.74 (0.55–0.99)

Age, sex, BMI, family history of lymphoma, smoking (pack-years), education level (HL only)

HL: 32.90 (10.59)

HL: OR 0.53 (0.32–0.87)

 Keegan et al., 2006 [31] Women

USA (North America)

312 (HL) 325 controls

35 (SD not reported)

HL

Recreational, lifetime

19–44 years: OR 0.71 (0.48–1.05)

Age, race/ethnicity, educational level, Jewish upbringing, smoking status 1 year before diagnosis/interview, nursed children, number of miscarriages, having a first or second degree relative hx of lymphoma, Jewish heritage, single room at age 11, living in a single family home at age 8 years, living in a rented family home at age 8 years

45–79 years: OR 0.35 (0.09–1.36)

Recreational, recent (≥2 vs. < 2 strenuous activities/wk. for > 1 month)

19–44 years: OR 0.58 (0.39–0.87)

45–79 years: OR 0.45 (0.19–1.06)

 Kelly et al., 2012 [32] Men Women Men and women combined

USA (North America)

950 (NHL) 181 (DLBCL) 242 (FL) 302 (CLL/SLL) 1146 controls

63 (SD not reported)

NHL FL CLL/SLL DLBCL

Recreational, recent (> 45 vs. 1.08 MET hours/wk) *also reported recreational, early adulthood (not listed)

NHL: M/W- OR 1.03 (0.80–1.33) M- OR 1.37 (0.98–1.92) W- OR 0.71 (0.47–1.07)

Age at enrollment, gender and county of residence

DLBCL: M/W- OR 0.99 (0.62–1.59) M- OR 1.19 (0.64–2.21) W- OR 0.80 (0.38–1.69)

FL: M/W- OR 0.98 (0.65–1.48) M- OR 0.96 (0.53–1.72) W- OR 0.90 (0.49–1.67)

CLL: M/W- OR 1.09 (0.75–1.58) M- OR 1.71 (1.08–2.70)

W- OR 0.53 (0.27–1.06)

 Pan et al., 2005 [33]

Men

Women

Men and women combined

Canada (North America)

1030 (NHL)

419 (DLBCL)

242 (FL)

100 (SLL)

269 (NHL NOS)

3106 controls

Men-

Cases: 56.7 (12.5)

Controls: 57.9 (14.6)

NHL

DLBCL

FL

SLL

NHL Not otherwise specified (NOS)

Recreational, recent

(≥34.4 vs. < 6.3 MET hours/wk)

NHL:

M- OR 0.79 (0.59–1.05)

W- OR 0.59 (0.42–0.81)

Age, province of residence, education, alcohol consumption, pack-years of smoking, total calorie intake, self-reported exposure to some chemicals, ever employment in some occupations, BMI, total calorie intake

Women-

Cases: 57.1 (12.6)

56.2 (12.2)

DLBCL: OR 0.84 (0.62–1.13)

FL: OR 0.64 (0.42–0.97)

SLL: OR 0.74 (0.41–1.33)

NHL NOS: OR 0.64 (0.45–0.92)

 Parent et al., 2011 [34]

Men

Canada (North America)

215 (NHL)

54 (HL)

533 controls

Cases: 58.9 (8.01)

Controls: 59.6 (7.91)

NHL

HL

Occupational, recent

(≥75% active vs. ≥75% sedentary at work)

NHL: OR 0.56 (0.26–1.20)

HL: OR 0.84 (0.17–4.23)

Age, ethnicity, educational level, socioeconomic status, respondent status, BMI, smoking, other PA

Recreational, recent

(≥1 vs. <1x/wk. sports or activity)

NHL: OR 1.17 (0.81–1.69)

HL: OR 0.97 (0.45–2.08)

Overall, recent

(Intermediate activity at work + recreational PA or high PA at work vs. other)

NHL: OR 0.85 (0.60–1.21)

HL: OR 1.20 (0.58–2.47)

 Zahm et al., 1999 [35]

Men

Women

USA (North America)

1177 (NHL)

3625 control

Median not reported.

Modal age category 45–84 years (cases), 75+ years (1162 controls)

NHL

Occupational, lifetime or “usual” occupation

(M > 12 vs. < 8; W > 8 vs. < 5 k Joules/min)

M: OR 1.0 (0.7–1.3)

W: OR 1.7 (0.2–11.5)

Age, state of residence

  1. **PA Physical activity, M Men, W Women, M/W Men/Women Combined, NHL Non-Hodgkin lymphoma, DLBCL Diffuse large B cell lymphoma, FL Follicular lymphoma, CLL/SLL Chronic lymphocytic leukemia/small lymphocytic lymphoma, NOS Not otherwise specified, HL Hodgkin lymphoma, BMI Body mass index