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Pediatrics and Neonatology (2017) xx, 1e7

Available online at www.sciencedirect.com

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journal homepage: http://www.pediatr-neonatol.com

Original Article

No direct correlation between rotavirus

diarrhea and breast feeding: A meta-analysis
Jian Shen a,*, Bi-meng Zhang b, Sheng-guo Zhu a,
Jian-jie Chen c,**

a
Department of Pediatrics, SHUGUANG Hospital Attached to the Shanghai University of Traditional
Chinese Medical, Shanghai 201203, China
b
Department of Acupuncture and Moxibustion, Shanghai General Hospital, Shanghai Jiaotong
University School of Medicine, Shanghai 200080, China
c
Department of Infectious Diseases, SHUGUANG Hospital Attached to the Shanghai University of
Traditional Chinese Medical, Shanghai 201203, China

Received Aug 12, 2016; received in revised form May 4, 2017; accepted Jun 16, 2017
Available online - - -

Key Words Background: Some studies indicated that children with exclusive breast feeding had a reduction
breast feeding; in the prevalence of rotavirus diarrhea, while some others held the opposite views. In this study,
meta-analysis; we aimed to systematically find the associations between rotavirus diarrhea and breast feeding.
rotavirus diarrhea Methods: A literature search up to June 2016 in electronic literature databases, including
PubMed and Embase, was performed. The NewcastleeOttawa Scale was used to conduct the
quality assessment of all the selected studies. Statistical analyses were performed using the
R package version 3.12 (R Foundation for Statistical Computing, Beijing1, China, meta package),
and odds ratio (OR) and 95% confidence interval (CI) were used to assess the strength of the as-
sociation. The heterogeneity was assessed by Cochrans Q-statistic and I2 test, and the sensi-
tivity analysis was performed by trimming one study at a time.
Results: A total of 17 articles, which included 10,841 participants, were investigated in the pre-
sent meta-analysis. There was no significant difference between the case group and control
group (OR, 0.59 95% CI 0.33e1.07) in the meta-analysis of exclusive breast feeding, and no sig-
nificant difference was found between the case group and the control group (OR, 0.86; 95% CI
0.63e1.16) in the meta-analysis of breast feeding. No significant difference was found between
the case group and control group (OR, 0.78 95% CI 0.59e1.04) for all quantitative data.
Conclusions: There may be no direct correlation between rotavirus diarrhea and breast feeding.
Copyright 2017, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).

* Corresponding author. Fax: 86 021 54285989.

** Corresponding author. Fax: 86 021 54285989.
E-mail addresses: jianshen7878@163.com (J. Shen), sunniatony@126.com (J.-j. Chen).

http://dx.doi.org/10.1016/j.pedneo.2017.06.002
1875-9572/Copyright 2017, Taiwan Pediatric Association. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-
NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Shen J, et al., No direct correlation between rotavirus diarrhea and breast feeding: A meta-analysis,
Pediatrics and Neonatology (2017), http://dx.doi.org/10.1016/j.pedneo.2017.06.002
 + MODEL
2 J. Shen et al
1. Introduction
Rotavirus, the major cause of severe childhood acute
diarrhea, is the fourth most common cause of child mor-
tality globally.1 It is estimated that diarrhea causes 1.5
million deaths, with 21% of deaths in children aged < 5
years.2 Furthermore, 98% of cases of diarrhea in India
occurred before children reached 2 years of age.3
Currently, two available vaccines for human rotavirus,
including Rotarix (RV1, GlaxoSmithKline, FDA approved in
2008) and RotaTeq (RV5, Merck, FDA approved in 2006),
have reduced the incidence of rotavirus diarrhea in young
children; however, the efficacy varies by national economic
status and geographical regions.4,5 Thus, there is an urgent
need to develop strategies to prevent the occurrence of
rotavirus diarrhea.
Breast milk contains many substances, such as anti-
bodies, antioxidants, nutrients and hormones, which are
essential for the survival and development of children.6
Breast feeding is related to lower incidence of rotavirus
gastroenteritis, which may be due to the anti-infective
properties of breast milk.7 John et al. indicated that chil-
dren with exclusive breast feeding had a reduction in the
prevalence of rotavirus diarrhea.8 Furthermore, Prameela
et al. showed that exclusive breast feeding had a positive
influence on the incidence of diarrhea.9 In addition, Kur-
ugol et al. suggested that breast feeding augmented the
impact of rotavirus vaccines in preventing severe diarrhea
in children.10 However, some studies revealed that breast
feeding did not have protective effects on rotavirus diar-
rhea in infants. Breast feeding did not protect children
from rotavirus diarrhea in a study performed by Linhares
et al.11 Misra et al. also showed that exclusive breast
feeding did not give enough protection for infants in a
country with a high incidence of rotavirus diarrhea.12 Thus,
it is necessary to draw a consistent conclusion about the
relationships between rotavirus diarrhea and breast
feeding.
In this study, we searched the databases of PubMed and
Embase for studies published up to June 2016 to system-
atically understand the associations between rotavirus
diarrhea and breast feeding.
2. Material and methods
2.1. Source of material
A literature search in electronic literature databases,
including PubMed (http://www.ncbi.nlm.nih.gov/pubmed)
and Embase (http://www.embase.com), was performed
to find articles that assessed the association between
rotavirus diarrhea and breast feeding. The search was up
to June 2016, using the following terms: (breast feeding
OR breastfed OR breast-feeding OR breast-fed)
AND (rotavirus AND (diarrhea OR diarrhoea)).
2.2. Inclusion and exclusion criteria of studies
Diarrhea was defined as the passage of 3 loose/watery
stools within 24 h.13 Studies were included if they were
published in English medical journals and were about
Please cite this article in press as: Shen J, et al., No direct correlation between rotavirus diarrhea and breast feeding: A meta-analysis,
Pediatrics and Neonatology (2017), http://dx.doi.org/10.1016/j.pedneo.2017.06.002
rotavirus diarrhea (case group: children with rotavirus
diarrhea; control group: children without rotavirus diarrhea
or normal persons) and provided or calculated the quanti-
tative distribution of breast feeding in the case group and
the control group. Reviews, reports, letters and comments
were excluded.
2.3. Data extraction and quality assessment
Two investigators independently extracted the following
data from the eligible studies: first author, publication
year, study location, study year, study type, number of
participants in the case group and the control group, sex
ratio (male/female) and age. Any discrepancies were
resolved by discussion with the third investigator.
The NewcastleeOttawa Scale (NOS)14 was used to
conduct the quality assessment of all the selected articles.
Two investigators independently performed the quality
assessment, and any discrepancies were resolved by dis-
cussions with the third investigator.
2.4. Statistical analyses
Statistical analyses were performed using the R package
version 3.12 (R Foundation for Statistical Computing, Bei-
jing, China, meta package), and odds ratio (OR) and 95%
confidence interval (CI) were used to assess the strength of
the association. The heterogeneity was assessed by
Cochrans Q-statistic and I2 test.15 If a significant hetero-
geneity (p < 0.05 or I2 > 50%) was found, then the random-
effects model was used; otherwise, the fixed-effect model
was used. In addition, Eggers test was used to assess the
publication bias.16
2.5. Sensitivity analysis
The sensitivity analysis was performed by trimming one
study at a time, and the difference of pooled OR before and
after the trim was compared.
3. Results
3.1. Characteristics of eligible studies
The study selection process is shown in Fig. 1. A total of 337
articles were retrieved according to the search design.
After removing duplicates (42) and irrelevant titles and/or
abstracts (199), 96 studies remained for further screening
to be performed. Of these, 42 articles (8 letter, 7 case
report/series, 6 literature reviews and 21 conference/
duplicative papers) were excluded. A further 37 articles
(13 without a control group, 24 with no report on outcome
or published only as an abstract) were excluded by
screening for full-text. Finally, the remaining 17
articles2,7,8,12,17e29 were used in the present meta-analysis.
Thus, a total of 10841 participants (case group: 2522;
control group: 8319) were included. The characteristics of
these studies are presented in Table 1. The year of study of
these articles ranged from 1983 to 2012, and the study lo-
cations included Indonesia, India, Turkey, Brazil, Uganda
 Rotavirus diarrhea and breast feeding
Pediatrics and Neonatology (2017), http://dx.doi.org/10.1016/j.pedneo.2017.06.002
Please cite this article in press as: Shen J, et al., No direct correlation between rotavirus diarrhea and breast feeding: A meta-analysis,

Table 1 The characteristics of the contained studies.

Author Public Study location Study year Study types Case Control M/F Age Fever Vomiting Dehydration Exclusive NOS
year (months) (Case/ (Case/ (Case/ or mixed
Control) Control) Control)
John BM 2014 India 2011e2012 Cross-sectional 60 190 123/127 1e24 831 1091 16/10 Exclusive 5
Kurugol Z 2003 Turkey 2000e2001 Cohort studies 366 554 NA 1e60 NA NA 164/105 Exclusive 8
Wobudeya E 2011 Uganda 2008.2e2008.4 Case control 91 91 114/68 NA 44/59 85/35 NA Exclusive/mixed 7
Strina A 2012 Brazil 2002e2004 Case control 390 1674 1100/964 1e12 4402 18372 NA Mixed 8
Salim H 2014 Indonesia 2009e2011 Cohort studies 327 329 400/256 1e60 302/276 9/21 310/291 Mixed 8
Prasetyo D 2015 Indonesia 2009e2012 Cross-sectional 60 74 88/46 1e6 NA NA 521 Exclusive 5
Nakawesi JS 2010 Uganda 2006e2007 Cross-sectional 177 213 235/155 3e59 NA NA 144/152 Mixed 6

+
Naficy AB 1999 Egypt 1995e1996 Cross-sectional 48 152 100/100 1e35 261 241 271 Mixed 4

MODEL
Misra S 2007 India NA Cohort studies 23 11 NA 1e12 12/7 17/7 10/5 Exclusive/mixed 7
Das S 2015 India NA Cross-sectional 145 28 NA 1e24 1021 1241 821 Mixed 4
de Palma O 2010 USA 2007e2009 Case control 251 753 539/465 1e25 NA NA NA Mixed 7
Mishra V 2009 India 2004e2008 Cross-sectional 79 333 255/157 1e36 NA NA NA Mixed 5
Bonkoungou IJ 2010 Burkina Faso 2008e2010 Cross-sectional 151 296 236/211 1e24 124/161 110/80 73/54 Mixed 4
Aminu M 2008 Nigeria 2002e2004 Cross-sectional 156 713 511/358 1e60 1211 1091 NA Exclusive/mixed 4
Clemens J 1993 Bangladesh 1985e1986 Case control 102 2587 1384/1305 1e24 NA NA NA Exclusive/mixed 7
Gianino P 2002 Italy 1999e2000 Case series 61 159 123/97 1e18 NA NA NA Exclusive 4
Duffy LC 1986 Italy 1983e1984 Case control 35 162 100/97 1e4 NA NA NA Exclusive 4
M: Male; F: Female; NOS: NewcastleeOttawa Scale; 1: Case; 2: Total.

3
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4 J. Shen et al
Figure 1 The study selection process.
and Egypt. Furthermore, the study designs incorporated
observational, case control, cohort and cross-sectional
studies. A greater number of males were included in
these studies than females, and the ages were between 1
and 60 months. The results of the NOS quality assessment
were 4e8, indicating that the overall quality was relatively
high.
3.2. Meta-analysis of all quantitative data
Significant heterogeneity across studies for the pooled
analysis (I2 Z 74.1%, p < 0.05) was found, thus the random-
effects model was used. There was no significant difference
between the case group and the control group (OR, 0.78,
95% CI, 0.59e1.04) (Fig. 2). As indicated by Eggers test,
there was no significant publication bias for this
Figure 2 Forest plot for meta-analysis of all quantitative data.
Please cite this article in press as: Shen J, et al., No direct correlation between rotavirus diarrhea and breast feeding: A meta-analysis,
Pediatrics and Neonatology (2017), http://dx.doi.org/10.1016/j.pedneo.2017.06.002
meta-analysis (t Z 1.1061, p Z 0.286), indicating that the
results were stable. The sensitivity analysis showed that
after trimming one study at a time, the pooled OR reversed,
indicating that the results were unstable (Fig. 3). There-
fore, relevant studies are still needed to confirm the
results.
3.3. Meta-analysis of exclusive breast feeding
There was significant heterogeneity across studies for the
pooled analysis (I2 Z 7 6.6%, p < 0.05); thus, the random-
effects model was used. There was no significant difference
between the case group and the control group (OR, 0.59;
95% CI, 0.33e1.07) (Fig. 4). It suggested that there was no
correlation between rotavirus diarrhea and exclusive breast
feeding. As indicated by Eggers test, there was no signifi-
cant publication bias for this meta-analysis (t Z 0.060;
p Z 0.953), indicating that the results were stable. The
sensitivity analysis showed that after trimming one study at
a time, the pooled OR reversed and it indicated that the
results were unstable (Fig. 5). Therefore, relevant studies
are still needed to confirm the results.
3.4. Meta-analysis of breast feeding (exclusive
breast feeding and non-exclusive breast feeding)
Significant heterogeneity was found between studies
(I2 Z 70.3%; p < 0.05), thus the random-effects model was
used. No significant difference was found between the case
group and the control group (OR, 0.86; 95% CI, 0.63e1.16)
(Supplementary Figure 1), indicating that there was no
correlation between rotavirus diarrhea and breast feeding.
No publication bias for this meta-analysis was found by
Eggers test (t Z 0.426; p Z 0.679). The sensitivity analysis
showed that after trimming one study at a time, the pooled
OR did not reverse, indicating that the results were stable
(Supplementary Figure 2).
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Rotavirus diarrhea and breast feeding 5

Figure 5 Sensitivity analyses for meta-analysis of exclusive

breast feeding.

In a previous study, Heinig et al.33 indicated that the

Figure 3 Sensitivity analyses for meta-analysis of all quan-
titative data.
4. Discussions
This meta-analysis of 17 articles suggested that there was
no direct correlation between rotavirus diarrhea and breast
feeding. The present study showed that there was no sig-
nificant difference between the case group and the control
group in the meta-analysis of exclusive breast feeding, and
no significant difference was found between the case group
and the control group in the meta-analysis of breast
feeding. Furthermore, no significant difference was found
between the case group and the control group for all
quantitative data. An age matched case-control study
conducted by Wobudeya et al. found that breast feeding
did not provide any protection against rotavirus diarrhea in
infants.30 Salim et al. indicated that there was no differ-
ence in rotavirus infection rates between breast-fed and
bottle-fed infants.28 Prasetyo et al. showed that exclusive
breast feeding was not associated with severe dehydration
in rotavirus diarrhea.27 Studies conducted in India and in
Brazil among 0e3 years old children showed that breast
feeding did not protect children from rotavirus diar-
rhea.31,32 Thus, the findings of the present meta-analysis
were in line with those of previous studies and suggested
that there might be no direct correlation between rotavirus
diarrhea and breast feeding.
duration of breast feeding of at least 3 months was
commonly related to a reduced risk for infants illnesses,
and exclusive breast feeding for at least 3 months
conferred greater protection than did breast feeding for
less than 3 months. Morrow et al.34 showed that children
with <1-month duration of breast feeding did not alter the
association between milk oligosaccharides and diarrhea
outcomes. In addition, one study reported that infection-
related morbidity and mortality in developing countries
were lower in infants with longer duration of breast feeding
than those with early weaning.35 However, no relevant data
about the association of the duration of exclusive breast
feeding with the prevention of rotavirus diarrhea were
included in the 17 articles used for the present meta-
analysis. Thus, we did not perform the meta-analysis on
the association between rotavirus diarrhea and the dura-
tion of exclusive breast feeding in this study. Taking the
findings of previous studies into consideration, we infer
that longer duration of exclusive breast feeding may be
able to prevent rotavirus diarrhea.
The source of heterogeneity might be due to different
detection methods of rotavirus diarrhea, differences by
countries and ethnic regions, and the effect of de-
mographic data, such as sex and age. It has been reported
that the peak age for rotavirus diarrhea is 6e11 months, but
the rates of breast feeding declined from 6 month.36 One
study showed that breast feeding played protective roles
for children <1 year old.29 Exclusive breast feeding does
not provide overall protection during the first 2 years of

Figure 4 Forest plot for meta-analysis of exclusive breast feeding.

Please cite this article in press as: Shen J, et al., No direct correlation between rotavirus diarrhea and breast feeding: A meta-analysis,
Pediatrics and Neonatology (2017), http://dx.doi.org/10.1016/j.pedneo.2017.06.002
 + MODEL
6 J. Shen et al
life, and it does not prevent the outcome, but temporarily
postpones it.37 In contrast, the study by Krawczyk et al.
revealed that exclusive breast feeding had a significant
benefit in the prevention of rotavirus diarrhea among
children under 6 months.38 In our present study, the age of
children was between 1 and 60 months. Thus, age may
affect the results of our study. In addition, there were more
males than females in the 17 eligible articles, thus sex may
also affect the outcomes of the study. Therefore, further
studies that exclude the effect of age and sex are needed
to find the correlations between rotavirus diarrhea and
breast feeding.
One advantage of this meta-analysis was that the cor-
relation between rotavirus diarrhea and breast feeding was
re-examined using meta-analysis. However, there were
some limitations in this study. Firstly, some sources of un-
known heterogeneity might have affected the results of our
meta-analysis. Secondly, the demographic data in the
eligible studies were incomplete, and further subgroup
meta-analysis and meta-regression were not performed.
Thirdly, all the eligible studies were observational studies,
and the relationship between rotavirus diarrhea and breast
feeding could not be verified. Lastly, longer duration of
exclusive breast feeding might be able to prevent rotavirus
diarrhea; however, the meta-analysis about the association
between rotavirus diarrhea and the duration of exclusive
breast feeding was not performed because there were no
relevant studies among the eligible articles. Thus, further
studies to investigate the effect of a longer duration of
exclusive breast feeding in the prevention of rotavirus
infection are needed.
5. Conclusions
This meta-analysis suggests that there may be no direct
correlation between rotavirus diarrhea and breast feeding.
It provides certain theoretical basis for preventing the
rotavirus diarrhea, and suggests that another preventive
method against rotavirus diarrhea, such as rotavirus vacci-
nation, is needed. However, because of the limitations of
this study, such as some sources of unknown heterogeneity,
incomplete demographic data, no verification of the rela-
tionship between rotavirus diarrhea and breast feeding,
and no relevant studies about the association between
rotavirus diarrhea and the duration of exclusive breast
feeding in the selected articles, further rigorous studies
with complete demographic data, verification, and relevant
data about the association between rotavirus diarrhea and
the duration of exclusive breast feeding are needed to have
a clearer understanding of the correlation between rota-
virus diarrhea and breast feeding.
Competing interests
The authors have no conflicts of interests relevant to this
article.
Acknowledgements
Grant numbers and sources of support: National Natural
Science Foundation Study on the Gegen Qinlian Decoction
Please cite this article in press as: Shen J, et al., No direct correlation between rotavirus diarrhea and breast feeding: A meta-analysis,
Pediatrics and Neonatology (2017), http://dx.doi.org/10.1016/j.pedneo.2017.06.002
in Treating Rotavirus Virus Mechanism of Damp and Hot
have Diarrhoea with the Mucous Membrane of Intestine-
lung Immune and the Signal Transduction (81302924);
Science and Technology Commission of Shanghai TCM Um-
bilical Therapy Standardized Solution Research for the
Treatment of Infantile Diarrhea (15401971100); Shanghai
Municipality Traditional Chinese Medicine (TCM specialist)
Specialized Personnel Plan (ZY3-RCPY-3-1027); National
the Twelfth five-year Science and Technology Major
Special Projects (2012ZX10004301004).
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Appendix A. Supplementary data
Supplementary data related to this article can be found at
http://dx.doi.org/10.1016/j.pedneo.2017.06.002.