232 Review article
The association between BMI and cervical cancer risk: a
meta-analysis
Jalal Poorolajala and Ensiyeh Jenabib
The association between BMI and cervical cancer risk is not
clear. This meta-analysis was carried out to estimate the
association between overweight and obesity and cervical
cancer risk. We searched PubMed, Web of Science, Scopus,
ScienceDirect, LILACS, and SciELO for observational
studies addressing the association between BMI and
cervical cancer until February 2015. Data were
independently extracted and analyzed using odds ratios and
95% confidence intervals (CIs), on the basis of random-
effects models. We identified a total of 3543 references and
included nine studies with 128 233 participants. On the
basis of the results of case–control and cohort studies, the
association between cervical cancer and overweight was
estimated to be 1.03 (95% CI: 0.81, 1.25) and 1.10
(95% CI: 1.03, 1.17), respectively. According to the results of
case–control and cohort studies, the association between
cervical cancer and obesity was estimated to be 1.40 (95%
CI: 1.08, 1.71) and 1.08 (95% CI: 0.60, 1.52), respectively. No
evidence of heterogeneity and publication bias was
observed. The findings from this meta-analysis indicate that
Introduction
Cervical cancer is the third most common female cancer
in the world and the second most frequent cause of
cancer-related death among women (National Institutes
of Health, 2015). Epidemiological studies have indicated
that obesity and overweight are associated with risk for
many cancers (Guo et al., 1994). The association between
BMI and breast, endometrial, and ovarian cancers has
already been addressed (Cheraghi et al., 2012; Poorolajal
et al., 2014; Zhang et al., 2014).
Some etiologic factors of cervical cancer are well known
such as human papilloma virus infection, multiparity,
smoking, hormonal contraceptive use, and multiple sexual
partners (Bonneau et al., 2014). However, the association
between BMI and cervical cancer is not well established
(Schottenfeld and Fraumeni, 2006; Lee et al., 2013). Several
epidemiological studies have investigated the relationship
between BMI and cervical cancer, but the results are not
consistent. Some studies have reported a positive associa-
tion between obesity and cervical cancer (Albanes, 1987;
Parazzini et al., 1988; Lacey et al., 2003; Prompakay et al.,
2013) and some others have not (Brinton et al., 1987;
Brinton et al., 1993; Tornberg and Carstensen, 1994).
A review conducted in 2005 (Modesitt and van Nagell,
2005) reported that obesity has a significant effect on the
0959-8278 Copyright © 2016 Wolters Kluwer Health, Inc. All rights reserved.
Copyright r 2016 Wolters Kluwer Health, Inc. All rights reserved.
overweight is not associated with an increased risk of
cervical cancer, but obesity is weakly associated with an
increased risk of cervical cancer. However, more evidence,
based on large prospective cohort studies, is required to
provide conclusive evidence on whether or not BMI is
associated with an increased risk of cervical
cancer. European Journal of Cancer Prevention 25:232–238
Copyright © 2016 Wolters Kluwer Health, Inc. All rights
reserved.
European Journal of Cancer Prevention 2016, 25:232–238
Keywords: BMI, case–control studies, cohort studies, meta-analysis,
uterine cervical neoplasms
a
Department of Epidemiology & Biostatistics, Modeling of Noncommunicable
Diseases Research Center, School of Public Health, Hamadan University of
Medical Sciences and bDepartment of Midwifery, Toyserkan Branch, Islamic Azad
University, Toyserkan, Iran
Correspondence to Ensiyeh Jenabi, MSc, Department of Midwifery, Toyserkan
Branch, Islamic Azad University, Toyserkan, Hamadan 6517838695, Iran
Tel: + 98 81 34926634; fax: + 98 81 34925353; e-mail: en.jenabi@yahoo.com
Received 22 January 2015 Accepted 27 March 2015
incidence of gynecologic malignancies. Another review
on the same topic was conducted in 2008 (Lane, 2008)
and reported an increased risk of endometrial cancer
among overweight and obese women, but it did not
report the relationship between cervical cancer and
obesity because of a lack of evidence.
To our knowledge, no meta-analysis has addressed the
association between BMI and cervical cancer. Therefore,
this meta-analysis was carried out to estimate the overall
effect of overweight and obesity on cervical cancer risk
on the basis of current evidence.
Materials and methods
Criteria for including studies
Cohort, case–control, and cross-sectional studies addres-
sing the association between BMI and cervical cancer
were included, irrespective of age, race, country, pub-
lication date, and language. The exposure of interest was
overweight and obesity. BMI is the weight in kilograms
divided by the square of the height in meters. Individuals
are divided on the basis of BMI into the following cate-
gories: underweight (< 18.5 kg/m2), normal weight
(18.5–24.9 kg/m2), overweight (25–29.9 kg/m2), and
obese (≥30 kg/m2; World Health Organization, 2014).
DOI: 10.1097/CEJ.0000000000000164
 Association between BMI and cervical cancer risk Poorolajal and Jenabi 233
The outcome of interest was cervical cancer of any type,
which was diagnosed pathologically irrespective of the
tumor stage. Cervical tumors are squamous-cell carcino-
mas (the most common), adenocarcinomas, adenosqua-
mous cell carcinomas, lymphomas, melanomas, and
sarcomas (Prompakay et al., 2013).
Search methods
We used a search strategy combining a set of keywords
including ‘cancer’ or ‘malignancy’ or ‘carcinoma’ or
‘tumor’ and ‘body mass index’ or ‘BMI’ or ‘body size’ or
‘obese’ or ‘obesity’ or ‘overweight’ and ‘cervical’ or ‘cer-
vix’. We searched electronic bibliographic databases
including PubMed, Web of Science, Scopus,
ScienceDirect, LILACS, and SciELO for studies until
February 2015. To find additional references, we
screened the reference lists of the included studies. In
addition, we contacted the authors of the studies for more
potentially eligible studies. Furthermore, the following
conference databases were searched:
(1) American Cancer Society; available at http://www.
cancer.org.
(2) International Agency for Research on Cancer; avail-
able at: http://www.iarc.fr.
(3) American Society of Clinical Oncology; available at:
http://www.asco.org.
Data collection and analysis
The two authors (E.J. and J.P.) independently took a
decision on which studies met the inclusion criteria for
the objective of this meta-analysis. Any disagreement was
resolved through discussion between the authors until a
consensus was reached. The two authors extracted the
data from the included studies. Any disagreement was
resolved through discussion between the authors until a
consensus was reached. The variables that were extracted
for analysis included the first author’s name, the year and
country of study conduction, the study design, the mean
age/age range (year), the sample size, and the effect
measure and its 95% confidence interval (CI).
We assessed the quality of the included studies using
Grades of Recommendation, Assessment, Development,
and Evaluation (GRADE) (Oxman, 2004), considering
the following key elements: limitations, consistency,
directness, imprecision, reporting bias, strength, gradient,
and confounding.
Heterogeneity and publication bias
Statistical heterogeneity was explored using the χ2-test at
a 5% significance level (P < 0.05). Inconsistency across
studies was quantified using the I2-statistic (Higgins and
Green, 2008). Publication bias was explored using
Egger’s (Egger et al., 1997) and Begg’s (Begg and
Mazumdar, 1994) tests and was visualized using the
funnel plot.
Copyright r 2016 Wolters Kluwer Health, Inc. All rights reserved.
Odds ratios (ORs) and hazard ratios (HRs), along with
their associated 95% CIs, were used to express the
measures of association between cervical cancer and
overweight and obesity, considering BMI less than
25 kg/m2 as the reference group. Wherever reported, we
used the full adjusted forms of the ORs, controlled for at
least one of the potential confounding factors such as age,
age at last pregnancy, smoking, contraceptive use, sexu-
ally transmitted infections, human papilloma virus
infection, occupational group, hypertension, parity, or
menopause. Data were analyzed, and the results were
reported, using a random-effects model (DerSimonian
and Laird, 1986). As the results of the included studies
were homogeneous and the number of included studies
was limited, no subgroup analysis was carried out. All
statistical analyses were carried out at a significance level
of 0.05 using Stata software, version 11 (StataCorp,
College Station, Texas, USA).
Results
Results of the search
We identified 3543 references, including 3217 references
through searching electronic databases and 326 refer-
ences through checking reference lists. No reference was
found through searching conference databases. We
excluded 1214 duplicate and 2299 irrelevant references
through reading titles and abstracts, and 21 after
reviewing full texts because they did not meet our
inclusion criteria (Fig. 1). In total, nine studies remained
eligible for our meta-analysis including two cohort (Rapp
et al., 2005; Bhaskaran et al., 2014), two cross-sectional
(López-Hernández, 2013; Prompakay et al., 2013), and
five case–control (Parazzini et al., 1988; Cusimano et al.,
1989; Lacey et al., 2003; Machova et al., 2007; Wilson
et al., 2013) studies. This meta-analysis involved 128 233
participants (Table 1).
Effects of exposure
The association between overweight and cervical cancer
is given in Fig. 2. On the basis of the results of
case–control studies, there was no significant association
between overweight and cervical cancer (OR = 1.03, 95%
CI: 0.81, 1.25). On the basis of the results of cohort stu-
dies, there was a weak association between overweight
and cervical cancer (HR = 1.10, 95% CI: 1.03, 1.17).
The association between obesity and cervical cancer is
given in Fig. 3. According to the results of case–control
studies, there was a significant association between cer-
vical cancer and obesity (OR = 1.40, 95% CI: 1.08, 1.71).
On the basis of the results of cohort studies, there was no
significant association between obesity and cervical can-
cer (HR = 1.08, 95% CI: 0.60, 1.52).
Heterogeneity and publication bias
The χ2-test and the I2-statistic revealed no evidence of
heterogeneity among the included studies that addressed
234 European Journal of Cancer Prevention 2016, Vol 25 No 3

Fig. 1

Identification

No. of records identified through No. of additional records identified

database searching (n = 3217) through other sources (n = 326)

Screening

No. of records after duplicates removed (n = 2329)

No. of records screened (n = 2329) No. of records excluded (n = 2299)

Eligibility

No. of full-text articles assessed for No. of full-text articles excluded,

eligibility (n = 30) with reasons (n = 21)

Included
No. of studies included in qualitative synthesis (n = 9)

No. of studies included in quantitative synthesis (meta-analysis) (n = 9)

Flow of information through the different phases of the systematic review.

Table 1 Summary of study results

References Country Study design Age (years) Measure Adjustment Sample size

Bhaskaran et al. (2014) UK Cohort 16 + Hazard ratio Crude 1389

Cusimano et al. (1989) Italy Case–control 30–79 Odds ratio Crude 185
Lacey et al. (2003) USA Case–control 18–69 Odds ratio Adjusted 570
López-Hernández (2013) Mexico Cross-sectional 18.79 Odds ratio Crude 20 236
Machova et al. (2007) Czech Case–control 30–64 Odds ratio Adjusted 17 102
Parazzini et al. (1988) Italy Case–control 30–70 Odds ratio Adjusted 448
Prompakay et al. (2013) Thailand Cross-sectional 30–69 Odds ratio Crude 7720
Rapp et al. (2005) Australia Cohort 35–54 Hazard ratio Adjusted 78 484
Wilson et al. (2013) UK Case–control 52.9 Odds ratio Crude 2099

the association between cervical cancer and overweight Discussion

(21.2%, P = 0.268) and obesity (13.7%, P = 0.326).
The presence of publication bias was explored using
Begg’s and Egger’s tests and visualized using the funnel
plot. Begg’s and Egger’s tests revealed no evidence of
publication bias among the included studies addressing
the association between cervical cancer and overweight
(P = 0.835 and 0.945) and obesity (P = 0.404 and 0.169),
respectively. No evidence of publication bias was
observed in the funnel plots of studies addressing the
association between cervical cancer and overweight
(Fig. 4) and obesity (Fig. 5).
The quality of the included studies was assessed
using GRADE and is presented in Table 2. The quality
of four studies was moderate and that of five studies
was low.
This meta-analysis indicated that overweight was not
associated but obesity was weakly associated with an
increased risk of cervical cancer. Although no evidence of
heterogeneity was observed across the included studies,
the results were inconsistent. Some studies (Parazzini
et al., 1988; Machova et al., 2007; López-Hernández,
2013; Prompakay et al., 2013) reported a positive asso-
ciation between overweight and cervical cancer, whereas
some others (Cusimano et al., 1989; Lacey et al., 2003;
Rapp et al., 2005; Wilson et al., 2013) reported a negative
association. To explore the sources of discrepancy we
compared the studies on the basis of the mean age of the
participants, the country where the studies were carried
out, the adjusted/unadjusted estimates, and the design of
the studies (cross-sectional, case–control, cohort); how-
ever, we found no clear evidence that could explain the
discrepancy across the studies. However, in two of the

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 Association between BMI and cervical cancer risk Poorolajal and Jenabi 235

Fig. 2

Study Effect size, %

ID Random (95% CI) Weight

Odds ratio
Cusimano et al. (1989) 0.54 (0.19, 1.45) 10.42
Lacey et al. (2003) 0.95 (0.56, 1.34) 21.81
López-Hernández (2013) 1.39 (0.85, 2.31) 8.07
Machova et al. (2007) 1.35 (0.76, 2.41) 6.45
Parazzini et al. (1988) 2.20 (1.00, 4.70) 1.39
Prompakay et al. (2013) 1.30 (0.91, 1.83) 17.17
Wilson et al. (2013) 0.91 (0.68, 1.21) 34.69
Subtotal (I2 = 21.2%, P = 0.268) 1.03 (0.81, 1.25) 100.00
.
Hazard ratio
Bhaskaran et al. 2014 1.10 (1.03, 1.17) 98.32
Rapp et al. 2005 0.85 (0.47, 1.54) 1.68
Subtotal (I2 = 0.0%, P = 0.364) 1.10 (1.03, 1.17) 100.00
.
Note: weights are from random effects analysis

−4 −2 0 2 4

Forest plot of the association between cervical cancer and overweight.

Fig. 3

Study Effect size, %

ID Random (95% CI) Weight

Odds ratio
Cusimano et al. (1989) 1.33 (0.50, 3.48) 4.40
Lacey et al. (2003) 1.78 (0.96, 2.60) 13.10
López-Hernández (2013) 1.49 (0.92, 2.47) 14.35
Machova et al. (2007) 1.72 (0.92, 3.22) 7.13
Parazzini et al. (1988) 4.80 (2.20, 10.50) 0.59
Prompakay et al. (2013) 1.69 (1.00, 2.76) 11.52
Wilson et al. (2013) 1.11 (0.84, 1.47) 48.91
2 = 13.7%, P = 0.326)
Subtotal (I 1.40 (1.08, 1.71) 100.00
.
Hazard ratio
Bhaskaran et al. 2014 1.21 (1.06, 1.37) 71.44
Rapp et al. 2005 0.69 (0.29, 1.66) 28.56
Subtotal (I2 = 52.5%, P = 0.147) 1.06 (0.60, 1.52) 100.00
.
Note: weights are from random effects analysis

−6 −3 0 3 6

Forest plot of the association between cervical cancer and obesity.

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236 European Journal of Cancer Prevention 2016, Vol 25 No 3

Fig. 4 required to draw conclusions on the association between

BMI and the risk of cervical cancer. The association
Begg’s funnel plot with pseudo 95% confidence limits
between obesity and cancer risk may be explained by
1
excessive adipose tissue and alterations in the metabo-
lism of endogenous hormones and the production of
log[OR overweight]

0.5 cytokines, by adipose-related inflammatory reactions, and

by additional genetic risk factors that can promote the
0 growth of cancer cells (Gu et al., 2013). It seems that
cervical adenocarcinoma represents a hormonal cancer
and it may potentially be more responsive to the mito-
−0.5
genic effect of increased estrogen on glandular cervical
cancers (Modesitt and van Nagell, 2005). The vast
−1 majority of cervical cancers are squamous-cell cancers and
0 0.2 0.4 0.6 about 15% are adenocarcinomas. Nonetheless, there is
SE of: log[OR overweight] evidence supporting a significant increase in the inci-
dence of cervical adenocarcinomas in recent years (Kjaer
Funnel plot of the included studies addressing the association between
cervical cancer and overweight.
and Brinton, 1993; Vizcaino et al., 1998).

Animal studies have indicated that obesity is linked to

impaired immune function (Lamas et al., 2004; Bandaru
Fig. 5 et al., 2011). Human studies have indicated that excess
adiposity has a negative effect on immune function and
Begg’s funnel plot with pseudo 95% confidence limits
may impair the ability of the host defense system (Milner
2
and Beck, 2012; Sheridan et al., 2012). However, current
evidence suggests that human papilloma virus-related
cancers, including cervical cancer, are more common
log[OR obesity]

1 among immunodeficient patients (Frisch et al., 2000).

Indeed, any factor promoting human papilloma virus
infection or proliferation, or limiting its clearance, may be
0 a risk factor for cervical cancer (Bonneau et al., 2014).
Furthermore, evidence based on several observational
studies suggests an inverse association between obesity
−1
and cervical cancer screening. In other words, obese
women are less likely to undergo cancer screening than
0 0.2 0.4 0.6
women of normal weight (Meisinger et al., 2004;
SE of: log[OR obesity]
Maruthur et al., 2009). Therefore, nonadherence to rou-
Funnel plot of the included studies addressing the association between tine cancer screening may put obese women at a greater
cervical cancer and obesity. risk of death from cervical cancer.

This meta-analysis has a few limitations and potential

four studies that reported a negative association between
overweight and cervical cancer risk, the number of cases
was limited, including 36 cases in the study by Cusimano
et al. (1989) and 64 in the study by Rapp et al. (2005).
Thus, the negative association reported by these studies
may be attributed to the possibility of random error due
to sparse data. However, the association between BMI
and cervical cancer reported by Parazzini et al. (1988) was
much higher than in other studies. Again, the number of
cases in this study was limited (including 39 cases) and
thus random error may have played a role.
There is sufficient evidence that BMI is associated with
increased risk of other gynecologic malignancies such as
ovarian cancer (Poorolajal et al., 2014) and endometrial
cancer (Zhang et al., 2014). However, more evidence is
biases. The main limitation of this meta-analysis is the
limited number of eligible studies. Because of the lim-
itation of evidence, this meta-analysis could not provide
strong evidence based on current investigations for con-
clusive estimation of the association between BMI and
cervical cancer risk. Second, we attempted to use an
adjusted form of the OR estimates. However, some stu-
dies did not report adjusted forms of the measure of
effect. This issue may have raised the possibility of
information bias. Third, a majority of the included stu-
dies reported overall cervical cancer risk without distin-
guishing between squamous-cell carcinoma and
adenocarcinoma. Whereas obesity may have no associa-
tion with squamous-cell carcinoma, it may have an asso-
ciation with adenocarcinoma. Finally, we found two
studies that seemed potentially eligible to be included in
our meta-analysis, but we could not access the full texts

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 Table 2 Quality assessment of studies addressing the association between BMI and cervical cancer risk
Quality assessment No. of participants Relative effect (95% CI)
a b c d e f g h i
Studies Design Limitation Consistency Directness Imprecision Reporting bias Strength Gradient Confounding Cases Controls Overweight Obesity Quality
Bhaskaran et al. Cohort 0 0 0 0 0 0 +1 0 1389 5 240 000 1.10 (1.03, 1.17) 1.21 (1.06, 1.37) Moderate
(2014)
Cusimano et al. Case–control 0 −1 0 −1 0 0 +1 0 36 149 0.54 (0.19, 1.45) 1.33 (0.50, 3.48) Low
(1989)
Lacey et al. (2003) Case–control 0 −1 0 0 0 0 +1 +1 260 298 0.95 (0.56, 1.34) 1.78 (0.97, 2.60) Low
López-Hernández Cross-sectional 0 0 0 0 0 0 +1 0 131 20 105 1.39 (0.85, 2.31) 1.49 (0.92, 2.47) Moderate
(2013)
Machova et al. Case–control 0 0 0 0 0 0 +1 +1 106 19 996 1.35 (0.76, 2.41) 1.72 (0.92, 3.22) Moderate
(2007)
Parazzini et al. Case–control 0 0 0 −1 0 +1 +1 +1 39 409 2.20 (1.00, 4.70) 4.80 (2.20, 10.50) Low
(1988)
Prompakay et al. Cross-sectional 0 0 0 0 0 0 +1 0 165 7555 1.30 (0.91, 1.83) 1.69 (1.00, 2.76) Moderate
(2013)
Rapp et al. (2005) Cohort 0 −1 0 0 0 0 0 +1 64 78 484 0.85 (0.47, 1.54) 0.69 (0.29, 1.66) Low
Wilson et al. Case–control 0 −1 0 0 0 0 +1 0 367 1742 0.91 (0.68, 1.21) 1.11 (0.84, 1.47) Low
(2013)

Quality of evidence and definitions:

High quality: further research is very unlikely to change our confidence in the estimate of effect.
Moderate quality: further research is likely to have an important impact on our confidence in the estimate of effect and may change the estimate.
Low quality: Further research is very likely to have an important impact on our confidence in the estimate of effect and is likely to change the estimate.
Very low quality: Any estimate of effect is very uncertain.
a
Refers to the basic study design, which we have broadly categorized as randomized trials (high), observational (cohort/case–control) studies (low), and other evidence (very low).
b
Refers to the detailed study methods and execution [serious (− 1) or very serious (− 2) limitation].
c
Refers to the similarity in the estimates of effect across studies [important inconsistency (− 1)].
d
Refers to the extent to which the ‘people’, ‘interventions’, and ‘outcome measures’ are similar to those of interest [some (− 1) or major (− 2) uncertainty about directness].
e
Refers to imprecise or sparse data (− 1).
f
Refers to the high risk of reporting bias (− 1).
g
Refers to the strong (relative risk > 2 or < 0.5; + 1) or very strong (relative risk > 5 or < 0.2; + 2) evidence of association with no plausible confounders.
h
Refers to evidence of a dose–response gradient (+ 1).
i
Refers to all plausible confounders that would have reduced the effect (+ 1).

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Association between BMI and cervical cancer risk Poorolajal and Jenabi 237
238 European Journal of Cancer Prevention 2016, Vol 25 No 3
of these studies. This issue may raise the possibility of
selection bias.
Conclusion
The findings from this meta-analysis indicate that over-
weight is not associated with an increased risk of cervical
cancer, but obesity is weakly associated with an increased
risk of cervical cancer. However, more evidence, based
on large prospective cohort studies, is required to yield
conclusions on whether or not BMI is associated with an
increased risk of cervical cancer.
Acknowledgements
The authors thank the Vice-chancellor of Research and
Technology of Hamadan University of Medical Sciences
for approval of this study. Hamadan University of
Medical Sciences supported this study.
Conflicts of interest
There are no conflicts of interest.
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