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Background/objectives: Several epidemiological studies have analyzed the associations between red and processed meat and bladder cancer risk but the shape and strength of the associations are still unclear. Therefore, we conducted a dose-response meta-analysis to quantify the potential association between red and processed meat and bladder cancer risk. Methods: Relevant studies were identified by searching the PubMed database through January 2016 and reviewing the reference lists of the retrieved articles. Results were combined using random-effects models. Results: Five cohort studies with 3262 cases and 1,038,787 participants and 8 cases-control studies with 7009 cases and 27,240 participants met the inclusion criteria. Red meat was linearly associated with bladder cancer risk in case-control studies, with a pooled RR of 1.51 (95% confidence interval (CI) 1.13, 2.02) for every 100 g increase per day, while no association was observed among cohort studies (P heterogeneity across study design = 0.02). Based on both case-control and cohort studies, the pooled relative risk (RR) for every 50 g increase of processed meat per day was 1.20 (95% CI 1.06, 1.37) (P heterogeneity across study design = 0.22). Conclusions: This meta-analysis suggests that processed meat may be positively associated with bladder cancer risk. A positive association between red meat and risk of bladder cancer was observed only in case-control studies, while no association was observe in prospective studies.
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Eur J Nutr (2018) 57:689–701
https://doi.org/10.1007/s00394-016-1356-0
ORIGINAL CONTRIBUTION
Red and processed meat consumption and risk of bladder cancer:
a dose–response meta‑analysis of epidemiological studies
Alessio Crippa1 · Susanna C. Larsson3 · Andrea Discacciati2 · Alicja Wolk3 ·
Nicola Orsini1
Received: 28 July 2016 / Accepted: 30 December 2016 / Published online: 22 December 2016
© The Author(s) 2016. This article is published with open access at Springerlink.com
both case–control and cohort studies, the pooled relative
risk (RR) for every 50 g increase of processed meat per day
was 1.20 (95% CI 1.06, 1.37) (P heterogeneity across study
design = 0.22).
Conclusions This meta-analysis suggests that processed
meat may be positively associated with bladder cancer risk.
A positive association between red meat and risk of bladder
cancer was observed only in case–control studies, while no
association was observe in prospective studies.
Keywords Red meat · Processed meat · Bladder cancer ·
Dose–response · Meta-analysis
Introduction
Bladder cancer is the fifth most common cancer among
men and the fourteenth among women with an estimated
number of 429,000 cases worldwide in 2012 [1]. Bladder
cancer is rather common in developed countries (North
America and Europe), and it is more frequent among per-
sons aged 75 or older [2]. Mortality rates have been sta-
ble over the last decade with 165,000 estimated deaths in
2012 [1]. A few risk factors have recently been linked to
the etiology of bladder cancer. Apart from age and gender,
cigarette smoking and specific occupational exposures are
considered the most important risk factors [3, 4]. Identifica-
tion of additional modifiable risk factors such as diet may
enhance primary prevention.
Recently two meta-analyses summarized the body of
evidence concerning red and processed meat consumption
and risk of bladder cancer [5, 6]. Results from the review
by Wang et al. [5] indicated an increased risk of bladder
cancer of 17 and 10% for high red meat and high processed
meat consumption, respectively. The more recent review by
Abstract
Background/objectives Several epidemiological studies
have analyzed the associations between red and processed
meat and bladder cancer risk but the shape and strength of
the associations are still unclear. Therefore, we conducted a
dose–response meta-analysis to quantify the potential asso-
ciation between red and processed meat and bladder cancer
risk.
Methods Relevant studies were identified by searching the
PubMed database through January 2016 and reviewing the
reference lists of the retrieved articles. Results were com-
bined using random-effects models.
Results Five cohort studies with 3262 cases and 1,038,787
participants and 8 cases–control studies with 7009 cases
and 27,240 participants met the inclusion criteria. Red meat
was linearly associated with bladder cancer risk in case–
control studies, with a pooled RR of 1.51 (95% confidence
interval (CI) 1.13, 2.02) for every 100 g increase per day,
while no association was observed among cohort studies
(P heterogeneity across study design = 0.02). Based on
Electronic supplementary material The online version of this
article (doi:10.1007/s00394-016-1356-0) contains supplementary
material, which is available to authorized users.
* Alessio Crippa
alessio.crippa@ki.se
1 Public Health Sciences, Karolinska Institutet,
Tomtebodavagen 18A, 171 77 Stockholm, Sweden
2 Unit of Biostatistics, Institute of Environmental Medicine,
Karolinska Institutet, Nobels Vag 13, 171 77 Stockholm,
Sweden
3 Unit of Nutritional Epidemiology, Institute of Environmental
Medicine, Karolinska Institutet, Nobels Vag 13, 171
77 Stockholm, Sweden
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690 Eur J Nutr (2018) 57:689–701
1 3
Li et al. [6], on the other hand, found a significant asso-
ciation for processed meat, with a 22% increased risk of
bladder cancer for high consumption but not for red meat
consumption. Both meta-analyses, however, were based
only on contrasting risk estimates for the highest vs. the
lowest category of meat consumption, and this has some
limitations when the exposure distribution vary substan-
tially across studies. In the review by Li et al. [6], one of
the included studies [7] conducted in Uruguay, for instance,
used 0–150 g/day of red meat consumption (median of
85 g/day) as the lowest category. In another study con-
ducted in the USA [8], >58.5 g/day was the highest cate-
gory for red meat consumption.
Our aim is to describe variation in bladder cancer risk
across the whole range of the exposure distribution. A
dose–response analysis is more efficient and less sensitive
to heterogeneity of the exposure across different study pop-
ulations. Therefore, we conducted a dose–response meta-
analysis to clarify and quantify the potential association
between red and processed meat and bladder cancer risk.
Materials and methods
Literature search and selection
Eligible studies were identified by searching the PubMed
database through July 2016, with the terms [“bladder”
AND (“carcinoma” or “cancer” or “tumor” OR “neo-
plasms”)] AND (“meat” or “beef” or “pork” or “lamb”).
In addition, the reference lists of the retrieved articles were
examined to identify additional reports. The search was
restricted to studies written in English and carried out in
human. We performed this meta-analysis accordingly to
the Meta-Analysis of Observational Studies in Epidemiol-
ogy (MOOSE) guidelines [9]. Two authors (A.C. and A.D.)
independently retrieved the data from studies on the asso-
ciation between red and processed meat and risk of bladder
cancer. Discrepancies were discussed and resolved.
Studies were eligible if they met the following criteria: (1)
the study was a cohort or case–control study; (2) the expo-
sure of interest was red meat and/or processed meat; (3) the
outcome was incidence of bladder cancer; (4) the authors
reported measures of association (hazard ratio, relative risk,
odds ratio) with the corresponding confidence intervals for
three or more categories for red or processed meat consump-
tion. In case of multiple reports on the same study population,
we included only the most comprehensive or recent one.
Data extraction
From each study, we extracted the following information:
first author’s surname, year of publication, study design,
country where the study was conducted, study period,
exposure definition, unit of measurement, number of cases,
study size, confounding variables, and measure of associa-
tions for all the categories of meat consumption together
with their confidence intervals. Given the low prevalence
of bladder cancer, the odds ratios were assumed approxi-
mately the same as the relative risks (RRs). When several
risk estimates were available, we included those reflecting
the greatest degree of adjustment.
Statistical analysis
We used the method described by Greenland and Long-
necker [10] and Orsini et al. [11] to reconstruct study-spe-
cific trend from aggregated data, taking into accounts the
covariance among the log RR estimates. Risk estimates
from studies not reporting information about the number of
deaths and study size did not allow reconstruction of the
covariance and were assumed independent. Potential non-
linear associations were assessed by use of restricted cubic
splines with three knots located at the 10th, 50th, and 90th
percentiles of the exposure distribution. An overall P value
was calculated by testing that the regression coefficients
were simultaneously equal to zero. A P value for nonlinear-
ity was obtained by testing that the coefficient of the sec-
ond spline term was equal to zero [12].
Since studies used different units to express meat con-
sumption (e.g., servings/day, grams/day, grams per 1000 kcal/
day), we converted frequency of consumption using 120 and
50 g as the average portion sizes for red and processed meat,
respectively. We chose those values in accordance with previ-
ous meta-analyses on meat consumption and other types of
cancer [13, 14] and results from both the Continuing Survey
of Food Intakes by Individuals [15] and the European Pro-
spective Investigation into Cancer and Nutrition [16]. Meat
consumption reported in grams per 1000 kcal/day was con-
verted to g/day using the average energy intake reported in the
original articles. Within each exposure category, the median
or mean value was assigned to the corresponding RRs. If not
reported, we assigned the midpoint of the upper and lower
boundaries as average consumption. If the upper bound of
the highest category was not reported, we assumed that the
category had the same width as the contiguous one. When
RRs were reported only for single food items (e.g., separately
for beef and pork), we combined them using a fixed-effects
model and used the pool estimate as summary measure.
A random-effects meta-analysis was adopted to
acknowledge heterogeneity across study findings. Statisti-
cal heterogeneity was further assessed by using the Q test
(defined as a P value less than 0.10) and quantified by Rb
statistic [17]. Meta-regression models were employed
to explain residual heterogeneity. Differences in dose–
response curves between subgroups of studies were tested
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691Eur J Nutr (2018) 57:689–701
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as described by Berlin et al. [18]. Evaluation of goodness-
of-fit for the final models was assessed using the set of
tools presented by Discacciati et al. [19]. Publication bias
was investigated using the Egger asymmetry test [20].
We performed sensitivity analyses (1) excluding studies
where red meat definition included also some items of pro-
cessed meat; (2) excluding studies that did not adjust for
energy intake; (3) evaluating alternative average portion
sizes for red meat (100 and 140 g) and processed meat (30
and 70 g) consumption. All statistical analyses were con-
ducted with the dosresmeta [21] and metafor [22] packages
in R (R Foundation for Statistical Computing, Vienna, Aus-
tria) [23]. P values less than 0.05 were considered statisti-
cally significant.
Results
Literature search
The search strategy identified 146 articles, 108 of which
were excluded after review of the title or abstract (Fig. 1).
Of the 38 eligible papers 14 were excluded because they
did not meet the inclusion criteria (not original articles,
outcome different from bladder cancer, or not reporting
risk estimates with their confidence intervals). The refer-
ence lists of the remaining 24 articles were checked for
additional pertinent reports, and 5 additional papers were
identified. We further excluded 16 additional articles: 8 pre-
sented duplicated publications [2431]; 3 analyzed bladder
and other urinary cancer together [3234]; 3 did not report
enough data for a dose–response analysis [3537]; and 2
did not report results for red or processed meat consump-
tion [16, 38]. Thus, the meta-analysis included 13 inde-
pendent epidemiological studies [7, 8, 31, 3949].
Study characteristics
The main characteristics of the 13 epidemiological stud-
ies included in the meta-analysis are presented in Table 1.
Five cohort studies [3943] with 3262 cases and 1038,787
participants and 8 cases–control studies, of which 4 pop-
ulation-based [8, 44, 46, 47] and 4 hospital-based [7, 45,
48, 49], with 7009 cases and 27,240 participants evaluated
Fig. 1 Selection of studies for
inclusion in a meta-analysis
of red and processed meat
consumption and risk of bladder
cancer 1966–2016
146 Records Idenfied through PubMed
Database Search
38 Records Assessedfor Eligibility
108Records Excluded Because Title
and/or Abstract not Relevant
29 Arcles Eligible for Inclusion in the
Meta-Analysis
14 Arcles Excluded (Reviews, Different
Outcome, not Reporng Risk Esmates)
5Addional ArclesIdenfied from
Manual Searches
13 StudiesIncluded in the Meta-Analysis
16 Arcles Excluded fornot Sasfying
Inclusion Criteria:
8duplicate reports on same populaon
3analyzed other urinary cancer
3not reporng meat doses
2combined red and
p
rocessed meat
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692 Eur J Nutr (2018) 57:689–701
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Table 1 Characteristics of epidemiological studies of meat consumption and risk of bladder cancer in a meta-analysis, 1966–2016
References Study name Country Study
period
No. of
cases
Study
size
Exposure definition Exposure contrasts RR (95% CI) Adjustment variables
Cohort
Jakszyn [39] European
Prospective
Investigation
into Cancer and
Nutrition
Europe 1001 481,419 Red meat (fresh and
processed)
Red meat Age, gender, center,
educational level, BMI
(as continuous variable),
smoking status, lifetime
intensity of smoking
(number of cigarettes per
day), time since quitting or
duration of smoking, and
total energy intake
57.86–91.42 g/day versus 0–57.86 g/day 1.2 (0.96–1.49)
91.42–130.63 g/day versus 0–57.86 g/day 1.14 (0.91–1.41)
130.63–754.79 g/day versus 0–57.86 g/day 1.15 (0.9–1.45)
Ferrucci [40] NIH-AARP Diet
and Health
Study
USA 1995–2004 854 300,933 Red meat (bacon, beef,
cold cuts, ham, ham-
burger, hot dogs, liver,
pork, sausage, and
steak) and processed
meat (bacon, sausage,
luncheon meats, ham,
and hot dogs)
Red meat Age (continuous, years),
sex, smoking (never,
quit 10 years ago, quit
5–9 years ago, quit
1–4 years ago, quit
<1 year ago, or 20
cigarettes/day, 20–40
cigarettes/day, >40
cigarettes/day), and intakes
of fruit (continuous, cup
equivalents/1000 kcal),
vegetables continuous, cup
equivalents/1000 kcal),
beverages (continuous,
mL/day; sum of beer,
coffee, juice, liquor, milk,
soda, tea and wine), and
total energy (continuous,
kcal/day)
20.9 g per 1000 kcal versus 9.5 g per 1000 kcal 0.99 (0.78–1.25)
30.7 g per 1000 kcal versus 9.5 g per 1000 kcal 1.05 (0.83–1.33)
42.1 g per 1000 kcal versus 9.5 g per 1000 kcal 0.97 (0.77–1.23)
61.6 g per 1000 kcal versus 9.5 g per 1000 kcal 1.22 (0.96–1.54)
Processed meat
4.3 g per 1000 kcal versus 1.6 g per 1000 kcal 1.09 (0.85–1.39)
7.4 g per 1000 kcal versus 1.6 g per 1000 kcal 1.1 (0.86–1.41)
12.1 g per 1000 kcal versus 1.6 g per 1000 kcal 1.28 (1.01–1.62)
22.3 g per 1000 kcal versus 1.6 g per 1000 kcal 1.10 (0.86–1.40)
Larrson [41] Swedish Mam-
mography
Cohort and the
Cohort of Swed-
ish Men
Sweden 1998–2007 485 82,002 Red meat (meatballs or
hamburger, beef, pork,
veal, kidney, and liver)
and processed meat
(sausage, ham, salami,
and cold cuts)
Red meat Age, sex, education, smok-
ing status, pack-years of
smoking, and total energy
intake
1–4 servings/week versus 0–3 servings/month 1.11 (0.81–1.52)
5 servings/week versus 0–3 servings/month 1.00 (0.71–1.41)
Processed meat
1–4 servings/week versus 0–3 servings/month 0.87 (0.68–1.11)
5 servings/week versus 0–3 servings/month 1.91 (0.80–1.28)
Michaud
[42]
Health Profession-
als Follow-Up
Study and the
Nurses’ Health
Study
USA 1986–2002
and
1976–2002
808 135,893 Red meat (hamburger,
beef, pork, lamb as
main or mixed dish)
and processed meats
(bacon, hot dogs, sau-
sage, salami, bologna)
Hamburger Age, caloric intake (quin-
tiles), and pack-years of
smoking and for geo-
graphic region
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693Eur J Nutr (2018) 57:689–701
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Table 1 continued
References Study name Country Study
period
No. of
cases
Study
size
Exposure definition Exposure contrasts RR (95% CI) Adjustment variables
0 serving/month versus 1–3 servings/month 0.99 (0.72–1.36)
1 serving/week versus 1–3 servings/month 0.86 (0.68–1.08)
2–4 servings/week versus 1–3 servings/month 0.91 (0.70–1.17
Beef, pork, or lamb (main dish)
0 serving/month versus 1–3 servings/month 1.35 (0.94–1.96)
1 serving/week versus 1–3 servings/month 1.01 (0.78–1.33)
2–4 servings/week versus 1–3 servings/month 1.11 (0.85–1.45)
5 servings/week versus 1–3 servings/month 0.93 (0.57–1.52)
Beef, pork, or lamb (sandwich or mixed dish)
0 serving/month versus 1–3 servings/month 1.06 (0.79–1.43)
1 serving/week versus 1–3 servings/month 0.83 (0.65–1.06)
2–4 servings/week versus 1–3 servings/month 1.26 (0.98–1.63)
5 servings/week versus 1–3 servings/month 0.95 (0.51–1.75)
Hamburger:
0 serving/month versus 1–3 servings/month 1.07 (048–2.41)
1 serving/week versus 1–3 servings/month 1.13 (0.80–1.60)
2–4 serving/week versus 1–3 servings/month 0.96 (0.66–1.38)
Beef, pork, or lamb (main dish):
0 serving/month versus 1–3 servings/month 2.28 (0.88–5.92)
1 serving/week versus 1–3 servings/month 1.35 (0.76–2.39)
2–4 servings/week versus 1–3 servings/month 1.23 (0.71–2.11)
5 servings/week versus 1–3 servings/month 1.01 (0.56–1.65)
Beef, pork, or lamb (sandwich or mixed dish)
0 serving/month versus 1–3 servings/month 1.61 (0.92–2.81)
1 serving/week versus 1–3 servings/month 1.03 (0.75–1.41)
2–4 servings/week versus 1–3 servings/month 0.92 (0.66–1.27)
5 servings/week versus 1–3 servings/month 0.83 (0.40–1.71)
Processed meats (e.g., sausage, salami, bologna)
1–3 servings/month versus 0 serving/month 0.98 (0.76–1.25)
1 serving/week versus 0 serving/month 0.94 (0.71–1.23)
2–4 servings/week versus 0 serving/month 0.98 (0.74–1.30)
5 servings/week versus 0 serving/month 1.09 (0.71–1.69)
Bacon
1–3 servings/month versus 0 serving/month 1.08 (0.86–1.37)
1 serving/week versus 0 serving/month 1.09 (0.84–1.41)
2–4 servings/week versus 0 serving/month 1.10 (0.82–1.49)
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694 Eur J Nutr (2018) 57:689–701
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Table 1 continued
References Study name Country Study
period
No. of
cases
Study
size
Exposure definition Exposure contrasts RR (95% CI) Adjustment variables
5 servings/week versus 0 serving/month 1.63 (1.02–2.62)
Hot dog
1–3 servings/month versus 0 serving/month 1.02 (0.83–1.25)
1 serving/week versus 0 serving/month 1.02 (0.78–1.34)
2–4 servings/week versus 0 serving/month 0.86 (0.58–1.27)
Processed meats (e.g., sausage, salami, bologna)
1–3 servings/month versus 0 serving/month 1.07 (0.76–1.52)
1 serving/week versus 0 serving/month 1.25 (0.86–1.84)
2–4 servings/week versus 0 serving/month 0.98 (0.65–1.46)
5 servings/week versus 0 serving/month 0.81 (0.40–1.63)
Bacon
1–3 servings/month versus 0 serving/month 0.90 (0.65–1.25)
1 serving/week versus 0 serving/month 1.06 (0.74–1.51)
2–4 servings/week versus 0 serving/month 1.00 (0.67–1.51)
5 servings/week versus 0 serving/month 1.48 (0.70–3.16)
Hot dog
1–3 servings/month versus 0 serving/month 0.91 (0.66–1.24)
1 serving/week versus 0 serving/month 0.89 (0.63–1.27)
2–4 servings/week versus 0 serving/month 0.77 (0.47–1.24)
Nagano [43] Life-Span Study Japan 1979–1993 114 38,540 Red meat and processed
meat (ham, sausage)
Red meat Age, gender, radiation dose,
smoking status, education
level, body mass index,
and calendar time
2–4 servings/week versus 0–1 serving/week 0.68 (0.45–1.04)
5+ servings/week versus 0–1 serving/week 1.13 (0.53–2.19)
Ham and sausage
1 serving/week versus 0 serving/week 0.54 (0.31–0.92)
2+ servings/week versus 0 serving/week 0.73 (0.42–1.28)
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695Eur J Nutr (2018) 57:689–701
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Table 1 continued
References Study name Country Study
period
No. of
cases
Study
size
Exposure definition Exposure contrasts RR (95% CI) Adjustment variables
Case–control
Catsburg [44] USA 1987–1996 1660 3246 Processed meat (fried
bacon, ham, salami,
pastrami, corned beef,
bologna, other lunch
meats, hot dogs and
polish sausage)
Processed meat Age, sex, BMI (underweight/
normal <25, overweight
25–30, obese >30), race/
ethnicity (non-Hispanic
white/Hispanic/black or
other), education (high
school/1- to 4-year col-
lege/grad school), history
of diabetes (yes/no), total
vegetable intake per day,
vitamin A intake (IU per
day), vitamin C intake
(mg per week), carotenoid
intake (mcg per day), total
servings of food per day,
smoking duration (years
smoked) and smoking
intensity (cigarettes per
day)
1–2 times a week versus < Once a week 0.96 (0.76–1.23)
3 times a week versus < Once a week 1.11 (0.87–1.41)
4–6 times a week versus < Once a week 1.23 (0.96–1.58)
>1 time a day versus < Once a week 0.97 (0.74–1.27)
Isa [45] China 2005–2008 487 956 Red meat and preserved
meat
2–4 times/week versus 1 times/week 1.20 (0.90–2.10) Sex, age (categorical),
smoking status (categori-
cal), smoking duration
(continuous), smoking
amount (continuous), and
other food groups
5 times/week versus 1 times/week 1.80 (1.10–3.00)
Preserved meat
<1 times/month versus never 1.60 (1.00–2.80)
1–3 times/month versus never 1.70 (0.90–3.10)
1 times/week versus never 2.20 (1.00, 4.7)
Wu [46] USA 2001–2004
and
2002–2004
1171 2535 Red meat (beef, veal,
pork, and lamb) and
processed meat (ham,
bacon, sausage, hot
dog, cold cuts, turkey
sausages and hot dogs,
and poultry cold cuts)
Red meat Gender, age (0–54, 55–64,
65–74, 75+), region, race
(White/other), Hispanic
status, smoking status
(never, occasional, former,
current), usual BMI (con-
tinuous), and total energy
(kcal per day—continuous)
27.6 g per 1000 kcal versus 17.2 per 1000 kcal 0.97 (0.76–1.24)
37.4 g per 1000 kcal versus 17.2 per 1000 kcal 1.04 (0.81–1.33)
53 g per 1000 kcal versus 17.2 per 1000 kcal 1.14 (0.89–1.46)
Processed meat
6.1 g per 1000 kcal versus 2.9 per 1000 kcal 1.01 (0.78–1.30)
10.1 g per 1000 kcal versus 2.9 per 1000 kcal 1.19 (0.92–1.53)
18.4 g per 1000 kcal versus 2.9 per 1000 kcal 1.28 (1.00–1.65)
Lin [8] USA 1999 884 1762 Red meat (beef, veal,
lamb, pork and game)
and processed meat
(hot dogs or franks,
sausage or chorizo)
Red meat Age, sex, ethnicity, smoking
status, pack-year of smok-
ing, energy intake, total
vegetable intake, total fruit
intake, and BMI
0.55–1.10 once versus <0.55 once 1.17 (0.87–1.58)
1.11–2.05 once versus <0.55 once 1.47 (1.09–1.99)
2.06 once versus <0.55 once 1.95 (1.41–2.68)
Processed meat:
0.11–0.28 once versus <0.11 once 0.88 (0.66–1.18)
0.29–0.61 once versus <0.11 once 0.98 (0.73–1.31)
0.62 once versus <0.11 once 1.03 (0.76–1.39)
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Table 1 continued
References Study name Country Study
period
No. of
cases
Study
size
Exposure definition Exposure contrasts RR (95% CI) Adjustment variables
Aune [7] Uruguay 1996–2004 255 2287 Red meat (fresh meat
including beef and
lamb) and processed
meat (hot dogs,
sausages, ham, salami,
saucisson, mortadella,
bacon and salted
meat)
10–40 g/day versus 0–10 g/day 1.01 (0.70–1.46) Age, sex, residence, educa-
tion, income, interviewer,
smoking status, cigarettes
per day, duration of smok-
ing, age at starting, years
since quitting, alcohol,
dairy foods, grains,
fatty foods (butter, eggs,
custard, cake), fruits and
vegetables, fish, poultry,
mate drinking, BMI, and
energy intake
>40–258.8 versus 0–10 g/day 1.43 (0.93–2.20)
Hu [47] Canada 1994–1997 1209 6248 Red meat (beef, pork,
lamb as a main or
mixed dish and
hamburger) and
processed meat (hot
dogs, smoked meat,
corned beef, bacon
and sausage)
Red meat Age group (20–49, 50–59,
60–69, 70–76), province,
education, body mass
index (<25, 25–29.9,
30), sex, alcohol use (g/
day), pack-year smoking,
total of vegetable and fruit
intake, and total energy
intake
2.1–3.94 times/week versus 2 times/week 1.20 (1.00–1.60)
3.95–5 times/week versus 2 times/week 1.20 (090–1.50)
5.42 times/week versus 2 times/week 1.30 (1.0–1.70)
Processed meat:
0.95–2.41 times/week versus 0.94 times/week 1.20 (1.10–1.60)
2.42–5.41 times/week versus 0.94 times/week 1.50 (1.10–1.90)
5.42 times/week versus 0.94 times/week 1.60 (1.20–2.10)
Closas [48] Spain 1998–2001 912 1785 Red meat (beef, veal,
lamb, pork) and
processed meat
Red meat: Age (<55, 55–64, 65–69,
70–74, >74 years old),
gender, region, smoking
status (never, occasional,
former, current), duration
of smoking (<20, 20–<30,
30–<40, 40–<50, 50
years) and quintiles of fruit
and vegetable intake
(20–32) g per 1000 kcal versus <20 g per kcal 1.10 (0.80–1.50)
(33–43) g per 1000 kcal versus <20 g per kcal 1.10 (0.80–1.50)
(44–58) g per 1000 kcal versus <20 g per kcal 1.00 (0.70–1.30)
(>58) g per 1000 kcal versus <20 g per kcal 0.80 (0.60–1.10)
Processed meat:
(4–9) g per 1000 kcal versus <4 g per kcal 1.40 (1.00–1.90)
(10–12) g per 1000 kcal versus <4 g per kcal 1.20 (0.90–1.70)
(13–18) g per 1000 kcal versus <4 g per kcal 1.20 (0.80–1.60)
(>18) g per 1000 kcal versus <4 g per kcal 1.20 (0.90–1.70)
Tavani [49] Italy 1983–1996 431 8421 Red meat (beef, veal
and pork)
Red meat Age, year of recruitment,
sex, education, smoking
habits and alcohol, fat,
fruit and vegetable intakes
3–6 times/week versus 3/week 1.40 (1.20–1.80)
6 times/week versus 3 times/week 1.60 (1.20–2.10)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
697Eur J Nutr (2018) 57:689–701
1 3
the relation between red and/or processed meat and risk
of bladder cancer. Two articles [39, 49] reported results
only for red meat, while one [44] only for processed meat.
Definition of meat and red meat varied across studies but
generally included beef, veal, pork, and lamb for red meat,
and bacon, ham, salami, sausages, and hot dogs for pro-
cessed meat. Two cohort studies [39, 40] included also
processed meat in the definition of red meat, and one study
[42] included only results for specific food items. One
study [44] reported results only for liver intake and was not
included in the analysis of red meat. Another study [45]
analyzed preserved meat consumption and, given the lim-
ited range of exposure (up to 1/week), was excluded from
the analysis of processed meat.
Only 3 studies [40, 46, 48] considered different cook-
ing methods and doneness levels for meat consumption.
None of them found evidence of an association between
preparation methods and bladder cancer. Different units
were used to report meat consumption: servings/week (7
studies), grams per 1000 kcal per day (3 studies), and
grams per day (3 studies). Five studies were conducted
in the USA, 4 in Europe, and 1 each in Canada, Uruguay,
China, and Japan. All the studies were carried out in
both men and women, and only one study [42] reported
results separately by gender. All the studies provided
measure of associations adjusted for age, gender, and
smoking. Four studies did not adjust for energy intake
[4345, 49]. Other common adjusting variables were
other food groups (8 studies), BMI (6 studies), education
(6 studies). Additional covariates were less consistent
across studies.
Association between red meat consumption and risk
of bladder cancer
We found a statistically significant association between red
meat consumption and risk of bladder cancer (P = 0.009;
P nonlinearity = 0.74) (Online Resource 1). The summary
RR for an increment of 100 g per day of red meat was 1.22
(95% CI 1.05, 1.41). There was substantial between-studies
heterogeneity (Rb = 67%, P < 0.01). Egger’s regression test
did not suggest the presence of substantial publication bias
(P = 0.14).
There was statistical heterogeneity according to study
design (P for heterogeneity = 0.02). The pooled RR
restricted to the cohort studies was 1.01 (95% CI 0.97,
1.06) for an increment of 100 g per day of red meat with
no significant heterogeneity (Rb = 0%, P = 0.62) (Fig-
ure 2). The deviance test did not detect lack of fit (D = 24,
df = 18, P = 0.17). In case–control studies, the corre-
sponding pooled RR was 1.51 (95% CI 1.13, 2.02) with
substantial heterogeneity among studies (Rb = 81%,
P < 0.01) and overall indication of poor fit (D = 44,
df = 18, P < 0.01).
No differences were found according to study location
(P for heterogeneity = 0.7), units of measurement (P for
heterogeneity = 0.38), and selection of controls (P for
heterogeneity = 0.65). Excluding those studies with also
processed meat in the definition of red meat, the pooled
RRs were 1.27 (95% CI 1.03, 1.57) overall and 0.95 (95%
CI 0.82, 1.11) restricted to cohort studies. The pooled
RR for an increment of 100 g of red meat per day was
1.14 (95% CI 0.99, 1.31) based on studies that adjusted
for energy intake. In the sensitivity analysis for alterna-
tive average portion sizes of red meat, the results did not
substantially change. The pooled RR for an increment of
100 g of red meat per day was 1.27 and 1.19 for assigned
portions of 140 g per day and 100 g per day, respectively.
For an increment of four servings per week of red meat
(120 g per servings), the summary RR of bladder cancer
was 1.15 (95% CI 1.03, 1.27) overall, 1.01 (95% CI 0.98,
1.04) for cohort studies, and 1.32 (95% CI 1.08, 1.62) for
case–control studies.
Association between processed meat consumption
and risk of bladder cancer
We found a statistically significant association between pro-
cessed meat intake and bladder cancer with no departure
from linearity (P = 0.005, P nonlinearity = 0.92) (Online
Resource 2). Every 50 g increase in processed meat per week
was associated with a 20% (95% CI 6, 37) increase in risk
of bladder cancer with moderate heterogeneity (Rb = 38%,
P = 0.07). Egger’s regression test did not detect publica-
tion bias (P = 0.21). No evidence of lack of fit was observed
(D = 43, df = 34, P = 0.14). The test did not detect signifi-
cant differences between case–control and cohort studies (P
for heterogeneity = 0.22). Stratified analysis provided a RR
of 1.10 (95% CI 0.95, 1.27) and 1.31 (95% CI 1.06, 1.63) for
cohort and case–control studies, respectively (Fig. 3).
The associations were similar across strata of study loca-
tion (P for heterogeneity = 0.68), units of measurement
(P for heterogeneity = 0.71), and selection of controls (P
for heterogeneity = 0.46). Exclusion of studies that did not
adjust for energy intake provided a pooled RR of 1.24 (95%
CI 1.07, 1.43). Similar results were observed for alternative
average portion sizes of 30 g per day and 70 g per day with
pooled RR, respectively, of 1.14 and 1.36 for an increment
of 50 g per day of processed meat.
For an increment of four servings per week of processed
meat (50 g per servings), the summary RR of bladder can-
cer was 1.11 (95% CI 1.03, 1.20) overall, 1.06 (95% CI
0.97, 1.15) for cohort studies, and 1.17 (95% CI 1.03, 1.32)
for case–control studies.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
698 Eur J Nutr (2018) 57:689–701
1 3
Discussion
Findings from this dose–response meta-analysis of five
cohort and eight case–control studies suggest that pro-
cessed meat consumption is positively associated with risk
of bladder cancer. An increment of 50 g of processed meat
per day was associated with 20% increased risk of bladder
cancer. Red meat consumption was associated with bladder
cancer only in case–control studies, with a 51% increased
risk of an increment of 100 g per day, while no association
was observed among the prospective studies.
Meat, in particular processed meat, is a potential risk
factor for several cancers, with the most convincing evi-
dence for colorectal cancer [50]. In 2015, the International
Agency for Research on Cancer classified processed meats
as carcinogenic to humans (Group 1) and red meat as prob-
ably carcinogenic to humans [51]. The contribution of
meat to the etiology of bladder cancer may be explained
by different mechanisms, given that many nutrients are
excreted through the urinary tract [52]. The most estab-
lished mechanism involves the formation of endogenous
nitrosamines from nitrites that are particularly abundant
in processed meats [53]. Experimental studies have shown
that some nitrosamine metabolites induce bladder tumors
in rodents [54, 55]. Further support for at potential role
of nitrosamines in bladder carcinogenesis is that cigarette
smoking is a strong risk factor for bladder cancer and
tobacco smoke is a main source of exogenous exposure to
nitrosamines. Consumption of red meat could potentially
increase the risk of bladder cancer through heterocyclic
amines and polycyclic aromatic hydrocarbons, which can
be generated from high temperature cooking [56]. Hetero-
cyclic amines and polycyclic aromatic hydrocarbons have
been consistently shown to be carcinogenic in animal stud-
ies [56, 57].
A direct comparison with the results of previous reviews
[5, 6] is difficult since they were based on study-specific
risk estimates for high versus low categories of meat con-
sumption, which varied substantially across studies. The
directions of the associations, however, were consistent,
even though an association was found only for processed
meat in the meta-analysis by Lin et al. [6]. As in the review
by Wang et al. [5], case–control studies provided stronger
risk estimates as compared to prospective studies.
Among several potential explanations, case–control
studies generally assess the exposure after diagnosis, and
therefore, recall bias may lead to differential misclassifica-
tion between cases and controls. Considering the limited
knowledge of the role of meat consumption on the develop-
ment of bladder cancer [44], such classification errors are
Overall (Rb = 67%, p < 0.01)
0.65 1.001.502.003.50
Nagano et al., 2000
Michaud et al., 2006
Michaud et al., 2006
Larsson et al., 2010
Ferrucci et al., 2010
Jakszyn et al., 2011
Tava ni et al., 2000
Closas et al., 2007
Hu et al., 2008
Aune et al., 2009
Lin et al., 2012
Wu et al., 2012
Isa et al., 2013
3.24% 0.84 [ 0.42 , 1.70 ]
7.04% 0.94 [ 0.67 , 1.34 ]
8.56% 1.03 [ 0.79 , 1.33 ]
8.74% 0.91 [ 0.71 , 1.16 ]
9.07% 1.21 [ 0.96 , 1.52 ]
11.37% 1.01 [ 0.96 , 1.06 ]
6.95% 2.13 [ 1.50 , 3.04 ]
9.51% 0.84 [ 0.68 , 1.02 ]
8.91% 1.40 [ 1.10 , 1.77 ]
9.02% 1.34 [ 1.07 , 1.69 ]
5.37% 2.85 [ 1.79 , 4.55 ]
7.36% 1.23 [ 0.88 , 1.71 ]
4.86% 1.94 [ 1.16 , 3.24 ]
100.00% 1.22 [ 1.05 , 1.41 ]
Cohort
Case−control
Author(s), Year RR [95% CI]Weight
1.51 [ 1.13 , 2.02 ]
Subtotal (Rb = 81%, p < 0.01)
1.01 [ 0.97 , 1.06 ]
Subtotal (Rb = 0%, p = 0.62)
Red meat and bladder cancer
for every 100 g per day increment
Fig. 2 Relative risks of bladder cancer with 100 g per day increment in red meat consumption separately for cohort and case–control studies
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
699Eur J Nutr (2018) 57:689–701
1 3
likely to be similar among cases and controls. On the other
hand, half of the control studies used hospital-based con-
trols which may inflate the pooled association in case con-
trols have been recruited for conditions linked with changes
in meat consumption. Although based on limited number of
studies, we did not observed differences in results between
hospital-based and population-based case–control studies.
Different participation rates related to exposure or sever-
ity of diseases may also be a selection bias among case–
control studies. In addition, the time between diagnosis
and the exposure assessment is generally shorter for case–
control studies; hence, it may not reflect long-term expo-
sure because of changes in dietary patterns. On the other
hand, in cohort studies participants may alter their dietary
intake during the follow-up, which may bias results toward
the null hypothesis of no association. One of the included
cohort studies [42] analyzed repeated dietary measure-
ments over time and observed stronger associations when
using cumulative update date and when removing partici-
pant who had change their meat consumption.
Strength of this review is the dose–response analysis,
which better takes into account the quantitative nature and
heterogeneity of the exposure. In our analysis, all the infor-
mation about meat consumption, including intermediate
categories, contributed to the pooled associations. Another
strength is the large number of cases that provided high
statistical power to detect associations of moderate magni-
tude. Lastly, no evidence of publication bias was observed.
This meta-analysis also had potential limitations. Pool-
ing results from epidemiological studies do not solve the
problem of residual confounding, which inherently affects
individual studies. All of the included studies, however,
adjusted for main known risk factors for bladder cancer such
as age, gender, and smoking, and some studies also adjusted
for energy intake, BMI, education, and other food groups.
Excluding those studies not adjusting for energy intake did
not change the overall results, suggesting that energy intake
may have a limited impact on developing bladder cancer.
Second, red and processed meat definition varied across
study and this may partially contribute to the observed het-
erogeneity. Different units of measurements were also used
to report risk estimates for meat consumption, and we had
to assume average portion sizes when meat consumption
was reported as servings. Nevertheless, stratified analysis for
different types of measurements and sensitivity analysis for
alternative portion sizes did not find substantial differences
in results. Third, it was not possible to investigate the asso-
ciation between different meat-cooking methods and bladder
Overall (Rb = 38%, p = 0.07)
0.65 1.001.502.003.50
Nagano et al., 2000
Michaud et al., 2006
Michaud et al., 2006
Larsson et al., 2010
Ferrucci et al., 2010
Closas et al., 2007
Hu et al., 2008
Aune et al., 2009
Lin et al., 2012
Wu et al., 2012
Catsburg et al., 2014
0.71% 0.60 [ 0.13 , 2.75 ]
7.49% 0.96 [ 0.65 , 1.43 ]
11.87% 1.19 [ 0.91 , 1.56 ]
12.53% 1.07 [ 0.83 , 1.38 ]
11.08% 1.13 [ 0.85 , 1.51 ]
11.64% 1.06 [ 0.81 , 1.40 ]
12.17% 1.82 [ 1.40 , 2.37 ]
9.23% 1.31 [ 0.93 , 1.83 ]
3.20% 1.22 [ 0.62 , 2.41 ]
6.07% 1.68 [ 1.06 , 2.65 ]
14.02% 1.05 [ 0.84 , 1.31 ]
100.00% 1.20 [ 1.06 , 1.37 ]
Cohort
Case−control
Author(s), Year RR [95% CI]Weight
1.31 [ 1.06 , 1.63 ]
Subtotal (Rb = 58%, p = 0.02)
1.10 [ 0.95 , 1.27 ]
Subtotal (Rb = 0%, p = 0.83)
processed meat and bladder cancer
for every 50 g per day increment
Fig. 3 Relative risks of bladder cancer with 50 g per day increment in processed meat consumption separately for cohort and case–control studies
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
700 Eur J Nutr (2018) 57:689–701
1 3
cancer because only three articles reported such information.
However, none of them found an increase in bladder can-
cer risk with any of the cooking methods. Fourth, statistical
heterogeneity was observed in our analysis as in the previ-
ous two reviews [5, 6] but was mainly explained by differ-
ent study design. After stratification, moderate heterogeneity
was still observed among case–control studies, while cohort
studies provided more homogenous results.
In conclusion, results from this dose–response meta-
analysis suggest that processed meat consumption may be
positively associated with risk of bladder cancer. Positive
association between red meat and risk of bladder cancer
was observed only in case–control studies, while no asso-
ciation was observed in prospective studies.
Acknowledgements This work was partly supported by Young
Scholar Award from the Karolinska Institutet’s Strategic Program in
Epidemiology.
Authors’ contribution All authors (AC, SL, AD, AW, and NO) par-
ticipated both in the study design and in writing the manuscript. AC
and AD participated in the data collection. AC analyzed the data and
wrote the manuscript under the supervision of NO. SL and AW inter-
preted the results and critically reviewed the paper. All authors read
and approved the final manuscript.
Compliance with ethical standards
Conflict of interest Authors declare that they have no conflict of
interest.
Open Access This article is distributed under the terms of the Crea-
tive Commons Attribution 4.0 International License (http://crea-
tivecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if changes were
made.
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