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Downloaded from http://bmjopen.bmj.com/ on February 3, 2015 - Published by group.bmj.com
PEER REVIEW HISTORY
BMJ Open publishes all reviews undertaken for accepted manuscripts. Reviewers are asked to
complete a checklist review form (http://bmjopen.bmj.com/site/about/resources/checklist.pdf) and
are provided with free text boxes to elaborate on their assessment. These free text comments are
reproduced below.
This paper was submitted to the JECH but declined for publication following peer review. The authors
addressed the reviewers’ comments and submitted the revised paper to BMJ Open. The paper was
subsequently accepted for publication at BMJ Open.
ARTICLE DETAILS
TITLE (PROVISIONAL)
Fruit and vegetable intake and risk of type 2 diabetes mellitus:
meta-analysis of prospective cohort studies
AUTHORS
Tang, Zhenyu; Li, Min; Fan, Yingli; Zhang, Xiaowei; Hou, Wenshang
VERSION 1 - REVIEW
REVIEWER
REVIEW RETURNED
GENERAL COMMENTS
Patrice Carter
Leicester Diabetes Centre, The University of Leicester, Leicester, UK
21-May-2014
This meta-analysis of prospective cohort studies provides an update
to previous reviews conducted on the same topic (Carter et al 2010,
Cooper et al 2012). The examination of potential dose response
between intake and risk of T2DM provides interesting data.
However, the findings do not show anything new; to provide more
novel and interesting data would it be possible to examine
categories of different fruit and vegetables, as done with green
leafy vegetables?
Major points to consider:
Methods. The paper appears to include the same population,
specifically The Nurses’ Health Study on multiple occasions (Colditz,
Bazzanno and Muraki)? Please clarify if this is the case or not.
A previous systematic review (Carter et al 2010) does not appear to
have been referenced adequately in certain parts of this review. For
example in the Validity Assessment, the tool used to score papers is
clearly the same as used by Carter et al, which the authors
themselves created, this needs acknowledging.
Minor points to consider:
Introduction. On page 3, line 30, it states that previous reviews
were restricted by language, this is not the case, please amend.
Discussion. The discussion does not provide any new insights to
Downloaded from http://bmjopen.bmj.com/ on February 3, 2015 - Published by group.bmj.com
mechanisms or interpretation than that discussed in previous
reviews.
I would highly recommend a statistician reviews the methods
section.
REVIEWER
REVIEW RETURNED
GENERAL COMMENTS
Peilin Shi
Harvard School of Public Health, USA
21-Jul-2014
Major Comments:
1. This article involved the Nurses’ Health Studies (NHS) established
in 1976 with funding from National Institutes of Health. The authors
in their study included three articles involved NHS, Colditz et al
1992, Bazzano et al 2008, and Muraki et al 2013. It is not clear if
same participants counted more than once. Authors should read
the original articles to check them carefully.
2. The PRISMA Guideline mainly focused on randomized trials,
although PRISMA can also be used as a basis for reporting
systematic reviews of other types of research, particularly
evaluations of interventions.
The MOOSE (Meta-analysis of Observational Studies in
Epidemiology) statement is intended for the reporting of metaanalyses of observational studies.
Thus the authors should use The MOOSE Guideline Check List other
than The PRISMA Guideline.
Minor Comments:
1. Last line on page 2: GLV should be spelled out the first time it is
used;
2. The authors should not use same tiles for the different figures,
for example, Fig 2 vs. Supplemental fig A, Fig 4 vs. Supplemental fig
B;
3. If random effects models were used in all analyses (irrespective
of I square or P-value) then it should be specified why.
4. The title and legend in some figure are not clear to indicate the
study. For example, in Figure 2, Cooper (2012) and Cooper (201212)
should be, something like, Cooper (study a, 2012), Cooper (study b,
2012) ; Muraki (2013), Muraki (2013), Muraki (2013), should be
Muraki (Cohort a: 2013), Muraki (Cohort b: 2013), Muraki (Cohort c:
2013),…;
5. The title of Figs 2, 4, 5 should include the information “for
highest versus lowest intake of …”;
6. As compared with the fixed effect model, the weights assigned
under random effects are more balanced. Large studies are less
likely to dominate the analysis and small studies are less likely to be
trivialized. “Weight %” should be added in all forest plots for the
random effect models;
7. The line 5 from bottom of page 5, add “Cooper et al (study
a:2012) and Cooper et al (study b:2012) “;
Downloaded from http://bmjopen.bmj.com/ on February 3, 2015 - Published by group.bmj.com
8. Put “The analysis included 15 cohorts among the eleven articles,
where Ford et al and Kurotani et al study examined male and
female separately, Cooper et al have two studies in 2003 and
Muraki et al report included data from three independent cohorts.”
in footnote of Table A;
9. Page 5, authors indicated that “We considered low, moderate,
and high degrees of heterogeneity to be I2 values of 25%, 50%, and
75%, respectively.” It should be specified why.
10. The authors said, on page 9, that “Compared with the previous
meta-analyses, our study has several strengths. The present metaanalysis included 2.6-times more participants and 2.8-times more
T2D cases, which significantly increased the statistical power to
detect potential associations.”
I am not sure if the participants and T2D cases repeatedly counted
because several studies from same cohort (NHS).
11. The authors should use funnel plot to check for the existence of
publication bias in this systematic review and meta-analyse.
I would suggest ‘major/substantial revision’. It might take at least
one round of major revision before it might be acceptable for
publication.
VERSION 1 – AUTHOR RESPONSE
Reviewer #1 (Reviewer Name Patrice Carter):
Q: This meta-analysis of prospective cohort studies provides an update to previous reviews
conducted on the same topic (Carter et al 2010, Cooper et al 2012). The examination of potential
dose response between intake and risk of T2DM provides interesting data. However, the findings do
not show anything new; to provide more novel and interesting data.
R: Thank you for your careful review and very constructive suggestion. In fact, compared with the
previous meta-analyses (Carter et al 2010, Cooper et al 2012), our study has several strengths. We
included some new prospective studies (Kurotani et al 2013, Cooper et al 2012, and Muraki et al
2013). Therefore, this paper included 2.6-times more participants and 2.8-times more T2DM cases,
which significantly increased the statistical power to detect potential associations. In addition, we
also investigated a dose-response relation between fruit, vegetables, fruit and vegetables combined
consumption and risk of T2DM. Therefore, the results should be more novel and interesting.
Q: Would it be possible to examine categories of different fruit and vegetables, as done with green
leafy vegetables?
R: It is possible that different types of fruit and vegetables might have different effects on T2DM risk.
In fact, we tried to further investigate the association between categories of different fruit and
vegetables and risk of T2DM. However, due to the limited number of literature, we failed it. Another
possible explanation for the differences between the studies might be the classification of food
groups. For example, GLVs’criteria was inconsistent: some studies included spinach and lettuce;
some included spinach and greens; others did not provide specific description. If they were included
with an uniform definition of each groups, the effects on T2DM risk might differ. Future studies are
needed to be more specific about the role of different categories of fruit and vegetables and risk of
Downloaded from http://bmjopen.bmj.com/ on February 3, 2015 - Published by group.bmj.com
T2DM.
Major points
Q: Methods. The paper appears to include the same population, specifically The Nurses’ Health
Study on multiple occasions (Colditz, Bazzano and Muraki)? Please clarify if this is the case or not.
R: We are very sorry that we did not explain this critical point clearly. Among The Nurses’ Health
Studies, the same population was reported for the three studies (Colditz et al 1992, Bazzano et al
2008, Fung et al, 2004 (one of three prospective longitudinal cohort studies including Muraki et al’s
paper). As described in the Study selection. If data were reported more than once, we included the
study with the longest follow-up time. Therefore, we included the study by Bazzano et al, which
followed for 18 years. Accordingly, we have made corrections in the revised manuscript.
Q: A previous systematic review (Carter et al 2010) does not appear to have been referenced
adequately in certain parts of this review. For example in the Validity Assessment, the tool used to
score papers is clearly the same as used by Carter et al, which the authors themselves created, this
needs acknowledging.
R: We are very sorry that we did not discriminate this original reference clearly. In the Validity
assessment, the statement has been edited as you suggested.
Minor points
Q: Introduction. On page 3, line 30, it states that previous reviews were restricted by language, this
is not the case, please amend.
R: We are very sorry that we did not explain the difference accurately. The sentence has been
revised as you suggested.
Q: Discussion. The discussion does not provide any new insights to mechanisms or interpretation
than that discussed in previous reviews.
R: Thank you very much for your suggestion. In the Discussion, the paragraph has been revised you
suggested. We hope it meets your requirement.
Q: I would highly recommend a statistician reviews the methods section.
R: Thank you very much for your suggestion. Accordingly, we have invited an expert statistical
scientist to review the manuscript. We believe that the manuscript has been significantly improved
and hope it meets your requirement.
Reviewer #2 (Reviewer Name Peilin Shi):
Major points
Q1: This article involved the Nurses’ Health Studies (NHS) established in 1976 with funding from
National Institutes of Health. The authors in their study included three articles involved NHS, Colditz
et al 1992, Bazzano et al 2008, and Muraki et al 2013. It is not clear if same participants counted
more than once. Authors should read the original articles to check them carefully.
R1: We are very sorry that we did not explain this critical point clearly. Among The Nurses’ Health
Studies, the same population was reported for the three studies (Colditz et al 1992, Bazzano et al
2008, Fung et al, 2004 (one of three prospective longitudinal cohort studies including Muraki et al’s
paper). As described in the Study selection. If data were reported more than once, we included the
study with the longest follow-up time. Therefore, we included the study by Bazzano et al, which
Downloaded from http://bmjopen.bmj.com/ on February 3, 2015 - Published by group.bmj.com
followed for 18 years. Accordingly, we have made corrections in the revised manuscript.
Q2: The PRISMA Guideline mainly focused on randomized trials, although PRISMA can also be used
as a basis for reporting systematic reviews of other types of research, particularly evaluations of
interventions. The MOOSE (Meta-analysis of Observational Studies in Epidemiology) statement is
intended for the reporting of meta-analyses of observational studies. Thus the authors should use
The MOOSE Guideline Check List other than The PRISMA Guideline.
R2: Thank you very much for your suggestion. In the Supplementary file, the MOOSE Guideline Check
List has been edited you suggested.
Minor points
Q1: Last line on page 2: GLV should be spelled out the first time it is used;
R1: Thank you for your suggestion. We have made correction accordingly in page 2, last line, and the
name “GLV” has corrected as “green leafy vegetables”.
Q2: The authors should not use same tiles for the different figures, for example, Fig 2 vs.
Supplemental fig A, Fig 4 vs. Supplemental fig B;
R2: In Figs and Supplemental figs, the titles have been revised as you suggested.
Q3: If random effects models were used in all analyses (irrespective of I square or P-value) then it
should be specified why.
R3: Taking into account the within-study and between-study variability, we pooled relative risks and
their standard errors with random effects model (DerSimonian R, Laird N. Meta-analysis in clinical
trials. Control Clin Trials 1986;7:177-88.).
Q4: The title and legend in some figure are not clear to indicate the study. For example, in Figure 2,
Cooper (2012) and Cooper (201212) should be, something like, Cooper (study a, 2012), Cooper
(study b, 2012) ; Muraki (2013), Muraki (2013), Muraki (2013), should be Muraki (Cohort a: 2013),
Muraki (Cohort b: 2013), Muraki (Cohort c: 2013),…;
R4: In Figures, the title and legend have been revised as you suggested.
Q5: The title of Figs 2, 4, 5 should include the information “for highest versus lowest intake of …”;
R5: In Figs 2, 4, 5, the titles have been revised as you suggested.
Q6: As compared with the fixed effect model, the weights assigned under random effects are more
balanced. Large studies are less likely to dominate the analysis and small studies are less likely to be
trivialized. “Weight %” should be added in all forest plots for the random effect models;
R6: In all forest plots, the “Weight%” has been added as you suggested.
Q7: The line 5 from bottom of page 5, add “Cooper et al (study a:2012) and Cooper et al (study
b:2012)”;
R7: Thank you for your suggestion. The statement has been added as you suggested. Additionally,
we have made corrections accordingly in the main text, table and figures, and the name “Copper et
al” has corrected as “Cooper et al (study a:2012)” and “Cooper et al (study b:2012)”, respectively.
Downloaded from http://bmjopen.bmj.com/ on February 3, 2015 - Published by group.bmj.com
Q8: Put “The analysis included 15 cohorts among the eleven articles, where Ford et al and Kurotani
et al study examined male and female separately, Cooper et al have two studies in 2003 and Muraki
et al report included data from three independent cohorts.” in footnote of Table A;
R8: Thank you for your careful review and very constructive suggestion. In Table A, the sentence in
footnote has been added as you suggested.
Q9: Page 5, authors indicated that “We considered low, moderate, and high degrees of
heterogeneity to be I2 values of 25%, 50%, and 75%, respectively.” It should be specified why.
R9: Thank you for your careful review. A naïve categorisation of values for I2 would not be
appropriate for all circumstances, although we would tentatively assign adjectives of low, moderate,
and high to I2 values of 25%, 50%, and 75%. Quantification of heterogeneity is only one component
of a wider investigation of variability across studies, the most important being diversity in clinical
and methodological aspects. Meta-analysts must also consider the clinical implications of the
observed degree of inconsistency across studies. For example, interpretation of a given degree of
heterogeneity (25%, 50%, and 75%) across several studies will differ according to whether the
estimates show the same direction of effect. (Higgins JP, Thompson SG, Deeks JJ, Altman DG.
Measuring inconsistency in meta-analyses. BMJ 2003;327:557-60; Higgins JP. Commentary:
Heterogeneity in meta-analysis should be expected and appropriately quantified. Int J Epidemiol.
2008 37:1158-60.)
Q10: The authors said, on page 9, that “Compared with the previous meta-analyses, our study has
several strengths. The present meta-analysis included 2.6-times more participants and 2.8-times
more T2D cases, which significantly increased the statistical power to detect potential associations.”
I am not sure if the participants and T2D cases repeatedly counted because several studies from
same cohort (NHS).
R10: We are very sorry that we did not explain this critical point clearly. Among The Nurses’ Health
Studies, the same population was reported for the three studies (Colditz et al 1992, Bazzano et al
2008, Fung et al, 2004 (one of three prospective longitudinal cohort studies including Muraki et al’s
paper). As described in the Study selection. If data were reported more than once, we included the
study with the longest follow-up time. Therefore, we included the study by Bazzano et al, which
followed for 18 years. Accordingly, all amendments have been highlighted in red in the page 9.
Q11: The authors should use funnel plot to check for the existence of publication bias in this
systematic review and meta-analyses.
R11: Thank you for your careful review and very constructive suggestion. In fact, the possibility of
publication bias was also evaluated using visual inspection of a funnel plot except the Begg rank
correlation test and Egger’s regression test (figures not shown).
Downloaded from http://bmjopen.bmj.com/ on February 3, 2015 - Published by group.bmj.com
Fruit and vegetable intake and risk of type 2
diabetes mellitus: meta-analysis of
prospective cohort studies
Min Li, Yingli Fan, Xiaowei Zhang, Wenshang Hou and Zhenyu Tang
BMJ Open 2014 4:
doi: 10.1136/bmjopen-2014-005497
Updated information and services can be found at:
http://bmjopen.bmj.com/content/4/11/e005497
These include:
Supplementary Supplementary material can be found at:
Material http://bmjopen.bmj.com/content/suppl/2014/11/05/bmjopen-2014-005
497.DC1.html
References
This article cites 59 articles, 23 of which you can access for free at:
http://bmjopen.bmj.com/content/4/11/e005497#BIBL
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