Human Reproduction, Vol.29, No.6 pp.

1122 –1133, 2014

Advanced Access publication on April 29, 2014 doi:10.1093/humrep/deu072

ORIGINAL ARTICLE Andrology

Adherence to reporting guidelines

in observational studies concerning
exposure to persistent organic
pollutants and effects on semen
parameters
M. Serrano 1,2,*, M.C. Gonzalvo1, M.C. Sánchez-Pozo 3, A. Clavero1,

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M.F. Fernández 4, M.L. López-Regalado 1, J. Mozas 1, L. Martı́nez 1,
and J.A. Castilla 1,5,6
1
U. Reproducción, UGC de Obstetricia y Ginecologı́a, Hospital Universitario Virgen de las Nieves, Instituto de Investigación Biosanitaria de
Granada (IIBG), Granada, Spain 2Doctorado de Biomedicina de la Universidad de Granada, Granada, Spain 3Department of Clinical Biochemistry,
Virgen Macarena University Hospital, Sevilla, Spain 4Centro de Investigacion Médica, University of Granada; San Cecilio University Hospital,
Granada; CIBER Epidemiologı́a y Salud Pública (CIBERESP), Madrid, Spain 5Banco de Semen CEIFER, Granada, Spain 6Centro MasVida
Reproducción, Sevilla, Spain

*Correspondence address. E-mail: serranomolinamaria@gmail.com

Submitted on October 7, 2013; resubmitted on March 15, 2014; accepted on March 18, 2014

study question: Are studies on semen quality in men exposed to persistent pesticides reported according to the ‘strengthening the
reporting of observational studies in epidemiology’ (STROBE) recommendations and the guidelines for the appraisal of semen quality studies
(SEMQUA)?
summary answer: Most studies of the impact of pesticides on semen quality do not follow the STROBE and SEMQUA guidelines, thus
adherence is low, especially in methodological aspects.
what is known already: Much of the controversy about reduced semen quality in recent decades arises from a lack of standardization
in the methodology applied, despite the existence of several validated instruments for evaluating the quality of reporting. Indeed, SEMQUA was
purpose-designed for the particular characteristics of semen quality studies.
study design, size, duration: A structured literature search identified eligible articles reporting on persistent pesticides and human
semen quality, published in English before 1 September 2012. Opinion articles and reviews were excluded. We assessed the adherence to report-
ing guidelines of the articles, using and comparing the STROBE statement and the SEMQUA guidelines, in both cases with indicators relevant to
observational studies of semen quality.
participants/materials, setting, methods: A comprehensive bibliographic search in various electronic literature data-
bases using the key words ‘sperm’ and ‘pesticide’ obtained 1179 papers, of which 46 were valid for our purposes. The papers examined occu-
pational (26) and environmental exposure (20). Two of the present authors independently piloted the data extraction form for this review. The
articles were then evaluated by two researchers using the STROBE and SEMQUA checklists.
main results and the role of change: Although no significant differences were found between the overall degree of compliance
with STROBE and SEMQUA (47.0 + 18.5% versus 43.1 + 11.6%), there were significant differences when only methodological aspects were
considered (48.4 + 21.0% versus 39.5 + 17.4%; P , 0.001). We observed an increase over time in the degree of compliance, for SEMQUA
(r ¼ 0.61 and P , 0.001) and STROBE (r ¼ 0.45 and P , 0.01). The papers that reported a negative effect of exposure to persistent pesticides
on sperm concentration presented a lower level of compliance to SEMQUA (42.1 + 18.3% versus 57.6 + 14.2%; P , 0.01) and STROBE
(40.2 + 10.3% versus 49.5 + 11.6%; P , 0.05) than those which recorded no such influence. The year of publication and the observed effect
on sperm concentration were the only candidate variables included in the model of stepwise multiple regression model for the ‘degree of com-
pliance’ variables of SEMQUA and STROBE.

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Studies of semen and pesticide exposure
limitations, reasons for caution: Other characteristics of reporting quality, such as legibility, were not evaluated.
wider implications of the findings: The low degree of compliance observed is consistent with that observed in other studies of
reproductive medicine and highlights the need to improve the design of studies of semen quality. SEMQUA proved to be a more specific tool than
STROBE for the field of semen quality. Editors, reviewers and authors should be aware of SEMQUA and apply it when assessing papers on semen
quality.
study funding/competing interest(s): No research funding was received and none of the authors have any conflict of inter-
ests.
Key words: pesticides / semen quality / SEMQUA / sperm / STROBE
Introduction
The decline in semen quality in men of reproductive age is a controversial
issue. The debate began when a review highlighted a decrease in sperm
counts, of up to 50%, during the period 1940–1990 (Carlsen et al., 1992)
and continued with several meta-analyses reporting a decline in semen
quality (Swan et al., 1997, 2000) around the world. Some recent
studies have corroborated this decline in semen quality (Jørgensen
et al., 2011; Mendiola et al., 2013; Rolland et al., 2013), whereas
others have found no such changes (Fisch et al., 1996; Thorup et al.,
2010; Fisch and Braun, 2013). Among the hypotheses proposed to
explain this phenomenon is that of exposure to endocrine-disrupting en-
vironmental pollutants, such as certain persistent organic pollutants
(POPs; Skakkebaek et al., 2001). Environmental contaminants such as
POPs are man-made bioaccumulative and lipophilic compounds, with
long half-lives, that are found throughout the world as a result of wide-
spread use in a variety of consumer products during the last century.
As a consequence, all populations worldwide bear a body burden of
POPs, with large inter-individual and inter-population differences
(Porta et al. 2008). Among POPs, persistent pesticides are a large
group of biologically active substances used for pest control in agriculture
(Porta et al., 2008; Diamanti-Kandarakis et al., 2009; Eskenazi et al.,
2009). Human exposure to persistent pesticides can take place from oc-
cupational exposure, as well as from pollution of the soil, water and food,
among other sources (environmental exposure).
Persistent pesticide compounds have different properties and can act
through diverse mechanisms, and their effects may be toxic or provoke
endocrine disruption (Mrema et al., 2013). In the past 40 years, many epi-
demiological studies have addressed the possible effects of exposure to
POPs on male reproductive health, but conflicting conclusions have been
drawn and at present there is no consensus as to the effect of exposure to
POPs exposure on semen quality (Jurewicz et al., 2009; Merzenich et al.,
2010; Mortimer et al., 2013; Vested et al., 2014).
To address concerns about the quality of published studies, the editor-
ial boards of many leading scientific journals now require compliance with
reporting guidelines (www.nlm.nih.gov/services/research_report_
guide.html). Samaan et al. (2013) observed that adherence to such
reporting guidelines is greater when they are more specific.
In order to improve the quality of reporting of observational studies, a
group of methodologists, researchers and journal editors developed
recommendations on what should be included in an accurate and com-
plete report of an observational study, and published them as the state-
ment ‘strengthening the reporting of observational studies in
epidemiology’ (STROBE), in the form of a checklist comprising 22
1123
items (38 questions; von Elm et al., 2007). Given the particularities of
semen quality studies, members of the ESHRE Special Interest Group
Andrology have developed a specific instrument, SEMQUA, for the ap-
praisal of seminal quality studies. This, too, is based on a checklist
scheme, comprised 18 items with 28 questions, and can be used to evalu-
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ate the adherence to reporting guidelines of research articles examining
the relationship between pesticide exposure and male gamete quality
(Sánchez-Pozo et al., 2013).
To the best of our knowledge, SEMQUA has not previously been com-
pared with the STROBE criteria. The aim of this study is to perform a
SEMQUA field test in the area of pesticide exposure to analyse its perform-
ance and compare it to STROBE, which is well validated.
Methods
We conducted a scoping review following the five stages proposed by Arksey
and O’Malley (2005): (i) identify the research question; (ii) find the relevant
studies; (iii) select the studies to be included; (iv) extract data from the studies
included and (v) summarize and report results. This strategy is recommended
for topics where there is a lack of uniformity in the methodology and when
objectivity must be ensured (Arksey and ÓMalley, 2005; Levac et al., 2010).
Systematic search
Combining the terms ‘sperm’ and ‘pesticide’, a systematic search was con-
ducted by two independent reviewers of the PubMed, ISI and Scopus elec-
tronic databases, for the period from January 1972 to September 2012. In
addition, we searched the listed references of the articles identified in
order to ensure no relevant citations were missed.
Inclusion and exclusion criteria
The following inclusion criteria were applied: (i) English language; (ii) research
articles on human populations; (iii) type of pesticide: only persistent pesti-
cides: (iv) type of exposure: occupational and environmental and (v) effect
on basic semen parameters. Reviews, duplicate publications and opinion
papers were excluded (Fig. 1).
Data charting
A data charting form was used to compile the different variables. The papers
were classified according to (i) year of publication; (ii) exposure type (occu-
pational and environmental); (iii) journal type (clinical and environmental
research) according to the area of application determined in Journal Citation
Reports (andrology, reproduction, urology, genetics, environmental science,
environmental and occupational health, toxicology and public health) and (iv)
the observed effect (increase, no change, decrease) of persistent pesticide
exposure on semen parameters (concentration, motility, morphology and
volume).
1124
Figure 1 Flow diagram for study selection.
Evaluation of the adherence to reporting
guidelines
All studies included were assessed independently by two researchers using
the guidelines SEMQUA (Sánchez-Pozo et al., 2013) and STROBE (von
Elm et al., 2007), to determine whether or not the studies complied with
each checklist item. Regular progress meetings were held, during which the
researchers pooled their results, reviewed the cases and discussed those
where the assessments diverged. Disagreements between the reviewers
were resolved by agreement. The degree of agreement between the two
reviewers was measured using the kappa index, and a value of 0.79 (95%
CI 0.72– 0.85) was achieved for STROBE and 0.83 (95% CI 0.77 – 0.88) for
SEMQUA.
Statistical analyses
Student’s t-test for paired samples was performed to compare the degree of
compliance with SEMQUA and STROBE (both overall and with respect only
Serrano et al.
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to the methodological items). The same test, for independent samples, was
also used to compare the degree of compliance by type of exposure (occu-
pational/environmental), type of journal and observed effect. The Pearson
correlation coefficient was used to analyse the relationship between
degree of compliance with SEMQUA and with STROBE, by year of publica-
tion. Finally, a stepwise multiple linear regression model was determined, to
assess the degree of compliance with SEMQUA and with STROBE.
Results
Literature search and study selection
The literature search yielded 1179 results. Duplicate citations were
removed manually. After consulting the titles and analysing the abstracts,
we excluded 1140 studies that did not meet the inclusion criteria. Of
these, 901 were based on an animal populations, 23 were not written
Studies of semen and pesticide exposure
in English, 67 were reviews and five were articles of opinion. Thus, a total
of 181 potentially relevant publications were analysed, of which 55 were
rejected because they studied exposure to non-persistent pesticides, 41
because they did not examine exposure to pesticides, 32 because they
did not analyse basic parameters of semen quality, 10 because no
semen analysis was performed and six because they were based on in
vitro research. A total of 39 articles were finally selected. In addition,
another seven relevant papers were identified from studying the refer-
ence lists (Fig. 1).
Charting data and evaluations of adherence
to reporting guidelines
Table I presents the data extracted from the studies in this review. Of the
46 included articles that analysed the relationship between semen quality
and exposure to persistent pesticides, 56.5% (26) examined occupation-
al exposure and 43.5% (20) examined environmental exposure.
The mean degree of compliance with the 28 items included in the
SEMQUA checklist was 47.0 + 18.5%, ranging from 97.8% compliance
with item 17.1 –0% with item 18 (Table II).
With respect to STROBE, the average degree of compliance with the
32 items included in the checklist was 43.1 + 11.6%, ranging from 100%
compliance with items 1b and 3–0% compliance with items 12c, 12d,
12e and 13c (Table III).
The mean degree of compliance with STROBE and SEMQUA was
similar in the studies analysed (47.0 + 18.5% versus 43.1 + 11.6%).
However, when only methodological issues were considered, there
was a higher degree of compliance with SEMQUA than with STROBE
(48.4 + 21.0% versus 39.5 + 17.4%; P , 0.001; Fig. 2). This difference
was much more evident among the studies of environmental exposure
(57.8 + 16.0% versus 45.8 + 14.2%; P , 0.001) than among those of
occupational exposure (39.6 + 20.4% versus 34.6 + 18.2%).
Study characteristics and adherence to
reporting guidelines
With respect to the year of publication of the study, the degree of general
compliance increased over time for both SEMQUA (r ¼ 0.61, CI ¼
0.39 –0.76; P , 0.001) and STROBE (r ¼ 0.45, CI ¼ 0.18– 0.65; P ,
0.01; Fig. 3). However, for the increase in adherence to SEMQUA,
only the studies of occupational exposure showed statistical significance
(r ¼ 0.54, CI ¼ 0.19 –0.76 and P , 0.01; Fig. 4).
The adherence to reporting guidelines of the studies of occupational
exposure was significantly lower than that obtained for environmental
exposure studies, using both SEMQUA (39.6 + 18.2% versus 56.6 +
14.3%; P , 0.01) and STROBE (37.9 + 11.3% versus 50.0 + 7.0%;
P , 0.001). There were also significant differences between occupation-
al and environmental studies in the comparison of only the methodo-
logical items, both with SEMQUA (39.6 + 20.4% versus 57.8 +
16.0%; P , 0.01) and with STROBE (34.6 + 18.2% versus 45.8 +
14.2%; P , 0.05). The mean year of publication of the articles on occu-
pational exposure was earlier than that of the articles on environmental
exposure (1990 + 11 versus 2004 + 5; P , 0.001).
Of all the studies, 58.7% (27/46) were published in clinical journals
versus 41.3% (19/46) in environmental journals. There was no significant
difference in overall compliance between the two types of journal, either
with SEMQUA (48.7 + 20.1% versus 45.8 + 17.6%) or with STROBE
(42.6 + 11.3% versus 43.6 + 11.9%), for clinical and environmental
1125
journals, respectively. Neither were significant differences observed
when only the methodological items were considered.
The studies that reported a negative effect on sperm concentration of
exposure to persistent pesticides presented a lower level of compliance
than those which did not observe any such influence, both with SEMQUA
(42.1 + 18.3% versus 57.6 + 14.2%; P , 0.01) and with STROBE
(40.2 + 10.3% versus 49.5 + 11.6%; P , 0.05). No differences were
observed for the other semen parameters.
The year of publication and the observed effect on sperm concentra-
tion were the only variables included in the stepwise multiple regression
model taking as the dependent variable the degree of overall compliance,
according to SEMQUA and STROBE (Table IV).
Discussion
The results obtained in this study indicate that the compliance with the
reporting guidelines (STROBE and SEMQUA) of the articles on semen
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quality and exposure to persistent pesticides is generally low, especially
with respect to methodological characteristics. These low levels of
reporting are in accordance with those observed in similar studies in
healthcare literature in general (Galera et al., 2011; Samaan et al.,
2013) and in the area of reproductive medicine in particular (Coppus
et al., 2009). This inadequate adherence in reproductive research
studies underlies the ongoing debate about the relationship between
the increase or decrease in semen parameters and exposure to environ-
mental pollutants (Joffe, 2010). Genuine interdisciplinary collaboration
(basic, clinical and epidemiological) would facilitate the rigorous develop-
ment of semen quality studies and would prevent the occurrence of
much low-quality research. In addition, compliance with methodological
standards would make the analysis of semen quality a very useful marker
in clinical research and in healthcare services, regarding both reproduct-
ive health (Guzick and Swan, 2006) and general health issues (Jensen
et al., 2009).
Our results also indicate that with respect to methodological items,
the adherence to reporting guidelines is greater when the latter are
more specific, as for SEMQUA compared with STROBE. This finding is
in agreement with the conclusions of Samaan et al. (2013), who after
reviewing several articles regarding adherence to reporting guidelines
concluded that a useful strategy for increasing research quality would
be to develop new guidelines on specific clinical areas, as was done re-
cently with SEMQUA (Sánchez-Pozo et al., 2013). The SEMQUA check-
list includes questions that summarize the essential points that need to be
considered for the proper development of studies of semen quality. Most
of these items should be considered in any full, accurate report of an ob-
servational study, and included in other guidelines, such as STROBE, for
the reporting of observational studies.
The higher degree of compliance observed in the methodological
aspects of studies of environmental exposure, according to SEMQUA,
is because these studies have been published more recently. Other
authors, also, have noted that the date of publication is a factor that is
associated with better reporting quality (Ziogas and Zintzaras, 2009;
Montgomery et al., 2011). This may be due to three factors (i) studies
are ever larger and involve more authors; (ii) authors are gaining experi-
ence and writing skills and (iii) editors and reviewers are demanding
higher quality articles (Bath et al., 1998).
Not all the items included in the reporting quality guidelines have the
same weight in terms of their effect on the validity of the studies
1126 Serrano et al.

Table I Data charting.

Reference Type of Type of Effect on semen parameters Degree of

exposure journal compliance (%)
......................................................................... ...............................
Concentration Motility Morphology Volume SEMQUA STROBE
.............................................................................................................................................................................................
Abell et al. (2000) Occupational Environ Res Decline Unchanged Decline Unchanged 54 53
Aneck-Hahn et al. (2007) Environmental Clinic Decline Decline Unchanged Decline 68 53
Bonde et al. (2008) Environmental Environ Res Decline Decline Unchanged Unchanged 61 56
Bush et al. (1986) Environmental Environ Res Decline Decline No data No data 46 50
Celik-Ozenci et al. (2012) Occupational Clinic Unchanged Decline No data Decline 54 28
Charlier and Foidart (2005) Environmental Clinic Unchanged Unchanged Unchanged No data 50 53
Dallinga et al. (2002) Environmental Clinic Decline Decline Decline Unchanged 32 38
Dalvie et al. (2004) Occupational Environ Res Decline Unchanged Unchanged Unchanged 54 28
De Fleurian et al. (2009) Occupational Clinic Unchanged No data No data No data 64 50
De Jager et al. (2006) Environmental Clinic Unchanged Decline Decline Unchanged 64 47
De Jager et al. (2009) Environmental Clinic Decline Decline Decline Unchanged 75 44

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Duty et al. (2003) Environmental Environ Res Decline Decline Unchanged No data 61 47
Eaton et al. (1986) Occupational Environ Res Decline Unchanged Unchanged No data 29 41
Egnatz et al. (1980) Occupational Environ Res Decline No data Unchanged Unchanged 25 38
Emmett et al. (1988) Occupational Environ Res Unchanged No data No data No data 43 53
Giwercman et al. (2007) Environmental Clinic Decline Unchanged Unchanged Unchanged 75 56
Glass et al. (1979) Occupational Environ Res Decline No data No data No data 43 44
Hauser et al. (2002) Environmental Environ Res Decline Decline Decline No data 29 38
Hauser et al. (2003) Environmental Environ Res Unchanged Decline Decline No data 57 56
Kamijima et al. (2004) Occupational Environ Res Unchanged Decline Decline Unchanged 54 44
Khan et al. (2010) Environmental Environ Res Decline Decline No data Unchanged 46 41
Lantz et al. (1981) Occupational Clinic Decline Decline No data Unchanged 32 38
Larsen et al. (1999) Occupational Environ Res Unchanged Unchanged Unchanged Unchanged 71 53
Lerda and Rizzi (1991) Occupational Clinic Decline Decline Decline Unchanged 29 34
Lipshultz et al. (1980) Occupational Clinic Decline No data No data No data 29 38
Messaros et al. (2009) Environmental Environ Res Decline Decline Decline No data 43 47
Milby and Whorton (1980) Occupational Environ Res Decline No data No data No data 43 41
Multigner et al. (2008) Occupational Environ Res Decline Unchanged Unchanged Unchanged 68 53
Oliva et al. (2001) Environmental Clinic Decline Decline Unchanged Decline 75 59
Olsen et al. (1990) Occupational Environ Res Decline No data No data No data 36 41
Pant et al. (2007) Environmental Clinic Decline Unchanged Unchanged Unchanged 39 38
Potashnik (1983) Occupational Clinic Decline No data No data No data 11 25
Potashnik and Yanai-Inbar (1987) Occupational Clinic Decline No data No data No data 25 25
Potashnik and Porath (1995) Occupational Environ Res Decline No data No data No data 14 25
Rignell-Hydbom et al. (2004) Environmental Environ Res Unchanged Unchanged No data Unchanged 61 50
Richthoff et al. (2003) Environmental Clinic Unchanged Decline Unchanged Unchanged 64 59
Rozati et al. (2002) Environmental Clinic Decline Decline Decline Decline 46 47
Sandifer et al. (1979) Occupational Environ Res Decline No data Unchanged No data 36 32
Schenker et al. (1988) Occupational Environ Res Unchanged Decline Unchanged Unchanged 75 63
Slutsky et al. (1999) Occupational Environ Res Decline No data No data No data 18 22
Spanò et al. (2005) Environmental Clinic No data No data No data No data 68 59
Takahashi et al. (1981) Occupational Environ Res Decline Unchanged Unchanged Unchanged 54 41
Toft et al. (2006) Environmental Environ Res Unchanged Decline Unchanged Unchanged 71 62
Whorton et al. (1977) Occupational Clinic Decline No data No data No data 29 28
Whorton et al. (1979) Occupational Environ Res Decline No data No data No data 21 25
Whorton and Milby (1980) Occupational Environ Res Unchanged No data No data No data 21 25
Studies of semen and pesticide exposure 1127

Table II Degree of compliance with SEMQUA checklist items.

SEMQUA checklist Degree of compliance (%)

........................................................................................................................... ...............................................................
Item Occupational Environmental Total
(n 5 26) (n 5 20) (n 5 46)
.............................................................................................................................................................................................
Participants 53 70 60
1. Are selection criteria clearly described? 46 65 54
2. 1 Are the individuals selected to participate in the study representative of the target population? 38 45 41
2.2 Are withdrawals and dropouts accounted for? 15 30 22
3. Does the study take into account the place of enrolment for the study (e.g. fertility clinic, maternity 62 90 74
clinic, workplace, donor sperm bank)?
4. Has geographic heterogeneity been considered? 46 90 64
5.1 Have explanatory variables and/or confounders been considered? 54 90 70
5.2 Has a clinical background study and appropriate physical examination been carried out by skilled 81 60 72
medical personnel?
6. Have factors related to reproductive capacity been considered? 77 90 83

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7.1 Have pre-analytical confounders been characterized? 50 75 61
7.2 Is the period of sexual abstinence known? 77 85 80
7.3 Has the location where the semen sample was obtained been taken into consideration? 46 60 52
7.4 Have pre-analytical instructions been followed? 42 55 48
Laboratory methods 24 52 36
8. Is the number of samples appropriate for the type of study? 4 20 11
9.1 Does the laboratory carry out internal quality control tests? 12 45 26
9.2 Is the laboratory part of an external quality control programme based on recommended methods? 4 35 17
10. Are the persons carrying out and interpreting the tests qualified (accredited)? 23 50 35
11.1 Are standardized reference values and methods used? 35 90 59
11.2 Is information provided concerning when and where measurements were obtained? 38 35 34
11.3 Are sufficient technical specifications reported concerning the materials and methods used? 54 90 70
Statistical methods 29 47 37
12. Has the study design been specified? 15 55 33
13. Have appropriate statistical tests been used? 85 95 90
14. Have confounding factors been adjusted for? Has a test with confounding factors being carried out? 35 60 46
15. Have outliers been identified, excluded and accounted for? 4 5 4
16. Has measurement uncertainty been quantified? 8 20 13
Results 39 38 39
17.1 Are results expressed in relation to the participants, test methods and statistical treatment of the 96 100 98
data obtained?
17.2 Have conclusions and values beyond the actual data generated been derived? 62 45 54
17.3 Can the results be generalized? 0 5 2
18. Has any applicability of the study findings been achieved? 0 0 0

evaluated. In this regard, our results reveal important deficiencies in
some of the main characteristics necessary for any study of semen
quality. First, the features and the description of the study population
were only reported in 60% of the papers. In our opinion, this percentage
is not high enough. A missing or incomplete description of the study
population (including inclusion and exclusion criteria) affects the ex-
trapolation of study results to the general population. In addition,
some authors have suggested that this may lead to an overestimation
of the effect observed (Sackett, 1979; Grimes and Schulz, 2002;
Dawson and Trapp, 2004).
Second, most of the studies included (89%) did not inform of the
number of semen samples analysed per individual or analysed only one
sample. Several authors have suggested that to obtain a reliable determin-
ation of an individual’s semen quality several samples must be analysed,
due to the variability encountered in semen parameters (Jeyendran,
2000; Carlsen et al., 2004; Castilla et al., 2006). Semen parameters (con-
centration, motility and morphology) have a high intra-individual variability
both in healthy men (Álvarez et al., 2003) and in subfertile men (Leushuis
et al., 2010). This methodological deficiency is therefore crucial and limits
the applicability of the results obtained.
1128 Serrano et al.

Table III Degree of compliance with STROBE checklist items.

STROBE checklist Degree of compliance (%)

...............................................................
Item Occupational Environmental Total
(n 5 26) (n 5 20) (n 5 46)
.............................................................................................................................................................................................
Title and abstract 54 68 60
1.1 Indicate the study’s design with a commonly used term in the title or the abstract 8 35 20
1.2 Provide in the abstract an informative and balanced summary of what was done and what was found 100 100 100
Introduction 96 98 97
2. Explain the scientific background and rationale for the investigation being reported 92 95 93
3. State specific objectives, including any pre-specified hypotheses 100 100 100
Methods 35 48 39
4. Present key elements of study design early in the paper 77 85 80
5. Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, 38 35 40
follow-up, and data collection
6. Give the eligibility criteria, and the sources and methods of selection of participants 35 65 48

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7. Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give 50 80 63
diagnostic criteria, if applicable
8. For each variable of interest, give sources of data and details of methods of assessment 54 70 61
(measurement). Describe comparability of assessment methods if there is more than one group
9. Describe any efforts to address potential sources of bias 4 15 9
10. Explain how the study size was arrived at 12 15 13
11. Explain how quantitative variables were handled in the analyses. If applicable, describe which 85 95 89
groupings were chosen and why
12.1 Describe all statistical methods, including those used to control for confounding 38 55 46
12.2 Describe any methods used to examine subgroups and interactions 58 80 67
12.3 Explain how missing data were addressed 0 0 0
12.4 If applicable, describe analytical methods taking account of sampling strategy 0 0 0
12.5 Describe any sensitivity analyses 0 0 0
Results 24 37 29
13.1 Report numbers of individuals at each stage of study—e.g. numbers potentially eligible, examined 12 10 11
for eligibility, confirmed eligible, included in the study, completing follow-up and analysed
13.2 Give reasons for non-participation at each stage 4 5 4
13.3 Consider use of a flow diagram 0 0 0
14.1 Give characteristics of study participants (e.g. demographic, clinical, social) and information on 38 90 61
exposures and potential confounders
14.2 Indicate number of participants with missing data for each variable of interest 12 15 13
15. Report numbers of outcome events or summary measures 92 95 93
16.1 Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision 54 95 72
(e.g. 95% confidence interval). Make clear which confounders were adjusted for and why they were
included
16.2 Report category boundaries when continuous variables were categorized 4 5 4
16.3 If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time 0 15 7
period
17. Report other analyses done—e.g. analyses of subgroups and interactions, and sensitivity analyses 49 69 58
Discussion 12 40 24
18. Summarize key results with reference to study objectives 96 100 98
19. Discuss limitations of the study, taking into account sources of potential bias or imprecision. Discuss 27 70 46
both direction and magnitude of any potential bias
20. Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of 92 100 97
analyses, results from similar studies and other relevant evidence
21. Discuss the generalizability (external validity) of the study results 19 35 26
Other information 19 70 41
22. Give the source of funding and the role of the funders for the present study and, if applicable, for the 19 70 41
original study on which the present article is based
Studies of semen and pesticide exposure 1129

Figure 2 Degree of compliance with the SEMQUA and STROBE

methodological items.

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Figure 4 Overall degree of compliance with SEMQUA by type of
exposure to persistent pesticides.

Table IV Multiple linear regression model of

compliance with SEMQUA and STROBE.

Beta CI (95%) P
........................................................................................
SEMQUA
Year of publication 0.86 0.47– 1.26 ,0.001
Effect on sperm concentration 29.51 218.12-(20.91) ,0.05
STROBE
Year of publication 0.35 0.08– 0.63 ,0.05
Effect on sperm concentration 27.13 213.13-(21.14) ,0.05

Figure 3 Overall degree of compliance with SEMQUA and STROBE

over time.
Due to the specific characteristics of semen quality studies, it is neces-
sary to control for additional variables such as period of abstinence, the
time elapsed from sample collection until the beginning of analysis, and/
or the place of sample collection (Stokes-Riner et al., 2007). Failure to
include this information in the study makes it impossible to distinguish
the real effect of exposure to pesticides from biological or physiological
variation. Proof of the importance of these factors is the fact that the only
semen parameter whose decline is associated with low reporting quality
is that of low concentration, i.e. the parameter which is most affected by
biological variability (Álvarez et al., 2003; Carlsen et al., 2004).
Third, deficiencies in participation in quality control procedures, both
internal and external, in identifying outliers and in quantifying the uncer-
tainty of the observed values, are all weaknesses of the studies evaluated.
The results obtained in this respect coincide with the poor implementa-
tion of the principles of quality control in the andrology laboratory
described by two surveys of andrology laboratory practice (Keel et al.,
2002; Riddell et al., 2005). This may be due to the fact that laboratory
scientists do not fully understand the statistical basis on which accurate
measurements are made (Pacey, 2010). Without the proper quantifica-
tion of the variability of each measure and of its associated error, the
measurement process is inherently unreliable (Bjorndahl et al., 2010).
The calculation of uncertainty of the values obtained in semen analysis
started to be recommended from 1999 (WHO, 1999), but 45.7% of
the papers selected for this study were published before that date.
However, analysis of the degree of compliance in this particular aspect
showed that, among the papers published subsequently, the percentage
of studies that breached this requirement decreased only slightly (95.2%
versus 80.0%). Furthermore, the methods for calculating the accuracy of
semen parameters are readily available in the literature and are essential
1130
for the detection and correction of systematic and random errors, and
thus for ensuring the reliability of the results obtained (Castilla et al.,
2006; WHO, 2010).
Our study highlights the need to unify the indexing of articles on
semen quality, as 15% (7) of the articles included were not revealed
in the first search strategy, but from an extensive review of the bibli-
ography cited in the articles analysed. Of these seven papers that were
not identified with the keywords ‘sperm’ and ‘pesticides’, two were
identified using the term ‘sperm quality’. SEMQUA, unlike other spe-
cific guidelines such as the STAndards for the Reporting of Diagnostic
accuracy (STARD; Bossuyt et al., 2003), does not include any recom-
mendation on the use of indexing terms. To facilitate the retrieval
of semen quality studies, authors should use the same terms, such
as sperm or semen quality in the title or abstract, as well as in the
keywords.
There are limitations of this study assessing the quality of the informa-
tion reported. Although we analysed the methodological and design
aspects of studies, we did not consider other features such as the
clarity of the language used (legibility), consistency or the absence of am-
biguity (González et al., 2004). Moreover, the risk of publication bias
should be taken into account, i.e. the possibility that more studies on per-
sistent pesticides showing a significant effect on seminal parameters have
been published.
Another limitation is that we were unable to assess whether the high
degree of non-compliance with the SEMQUA and STROBE guidelines
was due to an oversight in the preparation of articles by their authors
or during the editorial process, including the peer-review process of jour-
nals in which authors need to satisfy the requirements of reviewers, or at
both stages. The fact that we found no relation between the scope of the
journal (clinical versus environmental research) and the adherence to
reporting guidelines suggests that low levels of adherence are more
strongly related to the authors of the study than to the editorial
process. However, in other areas of healthcare (Balasubramanian
et al., 2006; Lumbreras et al., 2006), a relationship between reporting
quality and the scope of the journal has been observed, which suggests
that the editorial process needs to be standardized.
We firmly believe that compliance with the SEMQUA recommenda-
tions would substantially increase the quality of the design, development
and presentation of semen quality studies, and that this would lead to a
higher rate of their publication in the future, as has occurred after the
publication of similar guidelines in other areas of health research (Begg
et al., 1996; Areia et al., 2010; Capili et al., 2010). The checklist items
should be addressed in sufficient detail and clarity in the drafting of
such papers. Nevertheless, the aspects referred to in these checklists
should not be construed as an attempt to fit observational research infor-
mation into a rigid format; on the contrary, the order and the format must
continue to reflect the preferences of the author, the journal style and the
traditions of the research field.
In conclusion, the low level of compliance observed is consistent
with that observed in other studies in the field of reproductive medi-
cine, and highlights the need to improve the design of studies of semen
quality. Developing specific checklists for each field is critical.
SEMQUA has proven to be a more specific tool than STROBE for
the field of semen quality and therefore it is essential for editors,
reviewers and authors to be familiar with SEMQUA and to put it
into practice in the preparation and assessment of research papers
on semen quality.
Serrano et al.
Acknowledgements
This article is related to the Ph.D. Doctoral thesis by M. Serrano.
Authors’ roles
M.S. and M.C.G. carried out the bibliographic search and revised the
paper critically according to SEMQUA and STROBE. All authors contrib-
uted to the conception and design of the study, to the analysis and inter-
pretation of data, to drafting the article, to revising it critically for
important intellectual content and to giving their final approval of the
version to be published.
Funding
No research funding was received by the authors in regard to this manu-
script.
Downloaded from http://humrep.oxfordjournals.org/ by guest on October 21, 2016
Conflict of interest
None of the authors have received any funding or other payments or gifts
that had any influence on the content of this manuscript.
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