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Article history: Objective: This study aimed to assess the prevalence of sexual dysfunction and Female Sexual Function
Received 16 February 2017 Index (FSFI) score in women with infertility.
Received in revised form 31 May 2017 Study design: A systematic search of the literature was conducted using PubMed, EMBASE, IBECS, and
Accepted 6 June 2017
LILACS. The search was limited to articles published from January 2000 to September 2016, without
Available online xxx
language restriction. Data were analyzed using Stata 12.0. Random effects meta-analyses in weighted
mean difference (WMD) were performed for six comparative studies (infertility versus fertility).
Keywords:
Heterogeneity was estimated using I2. Moreover, to explore the heterogeneity sources among the studies,
Female sexual function index
Sexual disorder
meta-regression analyses were also performed. Quality of evidence was assessed using the Grading of
Infertility Recommendations Assessment, Development, and Evaluation guidelines, and risk of bias, with a graphic
Women funnel.
Results: Meta-analysis was performed in 11 of 13 comparative studies. The result indicated a signicant
association between an increase in sexual dysfunction and infertility in women (WMD = 0.16, 95%
condence interval = 0.254 to 0.084, p < 0.001), and high heterogeneity between studies was noted
(I2 = 98.6%, p < 0.000). Meta-regression analysis did not indicate heterogeneity (I2 = 0.00%). We also
performed a meta-analysis of individual FSFI domains in 10 studies. Infertile women had problems with
lubrication, orgasm, and satisfaction. Meta-regression analysis also showed that heterogeneity had no
inuence on the nal results of all the analyses.
Conclusions: Infertility was associated with an increase in female sexual dysfunction. The most affected
areas of sexual function were lubrication, orgasm, and satisfaction.
2017 Elsevier B.V. All rights reserved.
Contents
1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 154
2 Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157
2.1 Search strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157
2.2 Eligibility criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
2.3 Study selection, data extraction, and quality of evidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
2.4 Statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
3 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159
3.1 Included studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159
3.2 Infertilitys effect on female sexual function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159
http://dx.doi.org/10.1016/j.ejogrb.2017.06.013
0301-2115/ 2017 Elsevier B.V. All rights reserved.
154 C.R. Mendona et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 153163
1 Introduction Literature shows that women with infertility have more sexual
dysfunctions than the general population [913]. Sexual dysfunc-
Infertility is a worldwide problem that could cause signicant tions may be the result of infertility or the cause of infertility [8].
emotional and psychological harm to women even when it is due Couples who undergo human reproduction treatment may have
to a male factor [1]. Diagnosis of infertility among women results decreased sexual desire, lubrication, orgasm, satisfaction, and
in negative emotions and psychological distress, may have frequency of sexual intercourse, which could be attributed to stress
negative effects on the marital relationship and quality of life due to the treatment or medications [9,11]. However, results of
[27], and can generate emotions, such as anxiety, anger, despair, several studies conducted to evaluate sexual function of infertile
and sadness, in most people. Consequently, sexual activity may be couples are contradictory and heterogeneous [2,12,1419]. Wisch-
affected [8]. mann et al. [20] reported that reaching denite conclusions about
sexual dysfunctions in infertile women is primarily challenging
Fig. 1. Flow diagram of the selection of comparative studies and non-comparative studies.
Table 1
Characteristics of the comparative studies on sexual dysfunction in infertile and fertile women included in the systematic review.
Author Study GRADE* Conict Ethics Infertility Diagnostic/type of infertility Country Sample size, Age Mean Score FSFI P value Women sexual P
design of committee number FSFI dysfunction value
interest approval prevalence
Mirblouk cross- *** No Yes Primary or secondary Iran 147 149 30.61 6.8 32.7 6.8 26.3 3.8 34.4 25.1 0.011 ND ND ND
et al. sectional
(2016)
C.R. Mendona et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 153163
Ozkan et al. NA ** No Yes Idiopathic male infertility Turkey 56** 48 2445 2445 19.1 5.5 20.0 3.4 0.293 94.5% 100% ND
(2016)
Turan et al. case- *** No Yes One year and a history of infertility. Turkey 352 301 29.2 4.3 28.7 4.0 26.2 2.5 28.2 1.7 < 0.001 32.9% 17.2% 0.001
(2014) control
Davari cross- * No Yes Primary and secondary infertility. Iran 320 87 30.4 ND 25.7 4.5 32.0 1.1 0.001 ND ND ND
Tanha sectional
et al.
(2014)
Mendona case- *** No Yes One year and a history of infertility. Brazil 168 110 33.4 4.6 31.3 6.7 27.7 4.5 28.1 4.2 0.290 36.3% 28.2% 0.30
et al. control
(2014)
Iris et al. case- ** No Yes Primary infertility. Turkey 174 635 31.2 3.8 32.0 3.2 22.8 0.6 22.6 0.3 > 0.05 ND ND ND
(2013) control
Aggarwal case- * No Yes Premature ovarian failure (POF). Endometriosis India 267 233 2442 2442 22.4 3.9 22.3 3.3 ND 63.7% 46.3% 0.0001
et al. control Tubal/PID
(2013) Unexplained
Polycystic ovarian disease (PCOD).
Furukawa case- * No Yes Inability to become pregnant within 12 months or 6 USA 75 210 1845 1845 29.4 29.3 0.630 37.3% 31.9% 0.390
et al. control months. Severe male factor, tubal factor, or
(2012) recognized ovulatory dysfunction. Treatment.
de Almeida cross- * No Yes POF. Brazil 58 58 39.4 6.5 39.0 6.8 24.0 6.0 27.3 4.8 0.004 62.1% 37.8% 0.0093
et al. sectional
(2011)
Oskay et al. case- *** No Yes Failure to conceive after 12 months of unprotected Turkey 308 308 30.4 5.5 30.7 6.1 24.6 5.4 26.9 4.7 0.0001 61.7% 42.9% 0.00
(2010) control sexual intercourse
Millheiser case- *** No Yes History of 12 months of infertility USA 119 99 35.8 32.6 27.1 28.7 0.022 40.0% 25.0% 0026
et al. control
(2010)
Hentschel cross- ** ND Yes Women subjected to procedures of assisted Brazil 96 119 31.5 5.8 34.4 6.0 27.2 4.3 26.4 5.5 0.229 ND ND ND
et al. sectional reproduction.
(2008)
Drosdzol & NA * No Yes One year and a history of infertility. Poland 206 190 29.8 4.1 30.9 6.4 29.5 6.0 31.1 3.8 0.005 17.5% 12.1% 0.13
Skrzypulec (2008) Primary or secondary.
ND: no data available; * Quality of evidence was GRADE in four categories: very low quality, low quality, moderate quality, or high quality; **Diagnosed with idiopathic male infertility.
155
156 C.R. Mendona et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 153163
Table 2
Characteristics of the non-comparative studies on sexual dysfunction in infertile women included in the systematic review.
Author Study GRADE* Conict Ethics Infertility Diagnostic/type of Country Patients Age Mean Score Women sexual
design of committee infertility number FSFI dysfunction
interest approval Infertile prevalence
women
Lo & Kok cross- ** No Yes One year and a history of China 159 32.8 3.81 24.99 4.22a 32.5%
(2016) sectional infertility. Primary or
secondary infertility.
Kucur Suna cross- *** No Yes One year and a history of Turkey 30 27.9 5.4 25.7 5.1 43.3%
et al. (2016) sectional infertility. Primary or
secondary infertility.
Eftekhar et al. cross- *** No Yes Polycystic Ovary Syndrome Iran 130 27.0 4.27 25.93 3.92 57.7%
(2014) sectional (PCOS)
Jamali et al. cross- *** No Yes One year and a history of Iran 122 30.9 6.8 21.6 1.7 87.1%
(2014) sectional infertility.
Tashbulatova cross- *** No Yes Women subjected to Turkey 200 30.9 6.1 31.6 4.5b 35.5%
et al. (2013) sectional procedures of assisted
reproduction.
Yeoh et al. cross- *** No Yes One year and a history of Malaysia 150 32.3 4.5 71.8 17.5c 11.3%
(2012) sectional infertility.
Pakpour et al. cross- *** No Yes One year and a history of Iran 604 30.1 7.8 21.6 3.8 35.6%
(2012) sectional infertility.
Keskin et al. NA ** No Yes Primary or secondary. Turkey 173 29.9 7.9 23.1 4.9 68.2%
(2011)
Carter et al. cross- *** No Yes Infertile women awaiting USA 50 40.2 4.3 24.1 2.4 46.8%
(2011) sectional oocyte donation
Nelson et al. cross- *** No Yes Heterosexual couples USA 121 32.0 5.0 28.0 6.8 26.0%
(2008) sectional presenting for initial
evaluation of infertility
*Quality of evidence was GRADE in four categories: very low quality, low quality, moderate quality, or high quality; a- The traditional Chinese version of the FSFI, cut-off was
23.45; b- Turkish translation FSFI, cut off 30 female sexual dysfunction; c- Malay translation FSFI, cut off 55 female sexual dysfunction.
Fig. 2. Results of the meta-analysis for total FSFI score comparative studies.
C.R. Mendona et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 153163 157
because of methodological deciencies of the studies, different Reviews and Meta-Analyses (PRISMA) statements [29]. The
instruments used to measure female sexual function, and protocol is registered in the PROSPERO registry
discrepancies among the samples. (CRD42016041652, http://www. crd.york.ac.uk/PROSPERO).
Female sexual dysfunction can be diagnosed based on self-
report or interview and using validated instruments [21]. The main
instruments used in sexual dysfunction evaluation in infertile 2.1 Search strategy
couples are the following: Brief Index of Sexual Functioning [22],
Sexual Function Questionnaire [23], Sexual History Questionnaire A systematic search in ve available databases (PubMed,
[24], and Female Sexual Function Index (FSFI) [6,15,18,25]. Here, we EMBASE, IBECS, LILACS, and Cochrane Library) was conducted to
focus on FSFI, which is a 19-item self-report instrument created in identify all relevant studies published between 2000 and 2016,
2000 that evaluates sexual function in women in six dimensions without language restriction. Relevant additional studies identi-
(i.e., desire, excitement, lubrication, orgasm, satisfaction, and pain) ed in the reference list of primary and event studies were also
[26,27]. It was validated and translated into various languages, has analyzed (Fig. 1).
been widely used to measure sexual dysfunction in infertile We used the following terms to search in PubMed: (((((sexual
women, and has been accepted and used worldwide in both function) AND infertility) AND women)) OR (((sexual dysfunction)
clinical practice and research [6,15,18,19,25,28]. AND infertility) AND women)) OR ((female sexual function index)
Therefore, our study aimed to evaluate the FSFI score and sexual AND infertility). The following lter was applied: publication date,
dysfunction prevalence in women with infertility. Given the i.e., from January 1, 2000, to September 10, 2016. This same
current literature gaps, a systematic review that could provide combination of words was used to search in IBECS, LILACS, and
an overview of studies addressing sexual dysfunctions in infertile Cochrane Library.
women and valuable information to practitioners dealing with The terms used to search in EMBASE were the following:
reproductive and sexual health and infertile couples is necessary. ('female'/exp AND infertility'/exp OR female infertility'/exp OR
subfertility'/exp) AND ('sexual dysfunction'/exp OR female sexual
dysfunction'/exp OR psychosexual disorder'/exp OR frigidity'/exp
2 Materials and methods
OR dyspareunia'/exp OR sexuality'/exp OR Female Sexual
Function Index) AND ('human'/exp) AND NOT ('editorial'/it OR
This systematic review was developed based on the recom-
letter'/it).
mendations from the Preferred Reporting Items for Systematic
158 C.R. Mendona et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 153163
2.2 Eligibility criteria consensus. Potentially eligible articles were obtained and read in
full. Disagreements on study inclusion were addressed by a third
The inclusion criteria were as follows: a) studies measuring reviewer (PMOC). The data collected were the following: authors
sexual dysfunction in women of heterosexual couples; b) studies and year of publication, study design, country where the study was
reporting total FSFI score and all domains individually; c) studies conducted, group size, age, mean FSFI score and standard deviation
describing sexual dysfunction prevalence and mean; d) observa- (SD), and female sexual dysfunction prevalence. Data from
tional studies (cross-sectional, case-control, or cohort) including comparative and non-comparative studies were collected sepa-
comparative studies (infertile versus fertile women) and non- rately. Additional information was obtained by contacting authors
comparative studies (only infertile women); and e) studies on through e-mail. Study quality was assessed using the Grading of
women diagnosed as having infertility due to female or male Recommendations, Assessment, Development, and Evaluations
factors (primary or secondary infertility) who were undergoing (GRADE) [30]. The quality of evidence of the studies was classied
human reproduction treatment at the time of data collection or into four categories: high, moderate, low, or very low quality [31].
those that dened infertility as the failure to achieve clinical We also analyzed the inuence of possible conicts of interest and
pregnancy after 12 months of regular, unprotected sexual any information on ethical approval of the studies [32].
intercourse, which is based on the denition of the World Health
Organization. Moreover, sexual dysfunction was established when 2.4 Statistical analysis
the total FSFI score was <26.55 [27]. We excluded articles a) that
used other questionnaires or without clear identication of the Statistical analyses were performed using STATA 12.0 software
questionnaires used to measure female sexual function; b) that (Stata Corporation, College Station, TX, USA). For the meta-analysis,
were case reports; c) that assessed other illnesses; e) that failed to the population size and the mean and SD of the parameters that
mention infertility and sexual dysfunction in couples with reect the FSFI score for both infertile and fertile women were
infertility, or infertility and sexuality in children and teenagers; considered. The percentage of variability attributable to heteroge-
f) that had incomplete data even after we contacted the authors neity was estimated with the I2 test, which was deemed signicant
through e-mail; and g) that had a sample size <20. when p < 0.05. I2 values of 25, 50, and 90% corresponded,
respectively, to low, moderate, and high levels of heterogeneity.
2.3 Study selection, data extraction, and quality of evidence Data were pooled using a random effects model. Meta-regression
analysis was performed using the population size and mean FSFI
The articles included were reviewed by two investigators (CRM score of the infertile group to determine the association between
and JTA). Relevant data were extracted and differences resolved by infertility and female sexual dysfunction. The meta-analysis and
C.R. Mendona et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 153163 159
meta-regression analysis were performed at 95% condence 3.2 Infertilitys effect on female sexual function
interval (CI). Publication bias was assessed with a visual inspection
of a funnel plot. All statistical tests were with a signicance level of Based on the comparative studies, sexual dysfunction preva-
0.05. lence was higher in women with infertility. For most of the studies,
signicant differences in characteristics existed between infertile
and fertile women (Table 1). Among the 10 non-comparative
3 Results studies, 6 reported on sexual dysfunction in infertile women
(Table 2) [6,9,10,39,40,42]. Sexual dysfunction prevalence in
3.1 Included studies infertile women varied from 35.6 to 87.1%.
and thus was excluded. Based on the random effects model, observational studies. All studies reported ethical approval, and
infertile women had problems with lubrication (WMD = 0.267, no conict of interest among the authors existed.
95% CI = 0.471 to 0.064, p = 0.010) (I2 = 96.6%, P for heterogene-
ity = 0.000) (Fig. 3), orgasm (WMD = 0.272, 95% CI = 0.540 to 4 Discussion
0.003, p = 0.047) (I2 = 97.8%, P for heterogeneity = 0.000) (Fig. 4),
and satisfaction (WMD = 0.216, 95% CI = 0.418 to 0.015, This systematic review is the rst to evaluate sexual dysfunc-
p = 0.036) (I2 = 96.9%, P for heterogeneity = 0.000) (Fig. 5), and tion prevalence and sexual dysfunction score in women with
high evidence of heterogeneity was observed. Meanwhile, meta- infertility. Although the issue of infertility and its effect on female
regression analysis revealed the following: lubrication (tau2 = sexual function is not new, most of the studies were contradictory,
2.843, I2 = 0.00%, adjusted R2 = 43.40%), orgasm (tau2 = 3.273, which motivated us to conduct a systematic review. The results
I2 = 0.00%, adjusted R2 = 34.83%), and satisfaction (tau2 = 4.241, from the meta-analysis conrmed that women with infertility had
I2 = 0.00%, adjusted R2 = 15.56%). The analysis showed that hetero- an increase in sexual dysfunction. The most affected sexual
geneity had no inuence on the results of all the analyses. function domains were lubrication, orgasm, and satisfaction.
The meta-analysis showed that infertility was not associated Our ndings are signicant and could help professionals
with sexual desire dysfunction (WMD = 0.099, 95% CI = 0.406 to dealing with sexual and reproductive health; the diagnosis of
0.207, p = 0.526) (I2 = 97.9, P for heterogeneity = 0.000) (Fig. 6), infertility, treatment period, and drugs used in the treatment
excitation (WMD = 0.241, 95% CI = 0.568 to 0.086, p = 0.149) possibly contributed to the increase in sexual dysfunction [9,11,16].
(I2 = 98.5%, P for heterogeneity = 0.000) (Fig. 7), and pain (WMD = The treatment phases could also result in marital problems as
0.281, 95% CI = 0.608 to 0.046, p = 0.092) (I2 = 98.7%, P for sexual relation is now focused on conception, which in turn could
heterogeneity = 0.000) (Fig. 8). High evidence of heterogeneity was interfere with sexual satisfaction [16]. Other studies that were
observed. Meta-regression analysis showed that heterogeneity excluded reported on the inuence of sexual desire, problems with
was corrected in all analyses: desire (tau2 = 74.1, I2 = 0.00%, adjusted arousal, dyspareunia, inability to reach orgasm, and negative body
R2 = 98.52%), excitation (tau2 = 3.638, I2 = 0.00%, adjusted image in infertile women related to sexual dysfunction
R2 = 27.57%), and pain (tau2 = 4.197, I2 = 0.00%, adjusted R2 = 16.43%). [2,6,7,45,46].
The FSFI questionnaire was created in 2000; however, studies
3.4 Publication bias on sexual dysfunction in infertile couples were published after
2008. Since then, several researchers have used the FSFI. We found
The funnel plot revealed a symmetric pattern, suggesting no a predominance of studies published in developing countries,
publication bias in our meta-analysis (Fig. 9). Analysis of the including Iran and Turkey, whose culture treats topics on sexuality
methodological quality of the studies performed using GRADE and sexual function as unacceptable and taboo [47,48]. A recent
indicated low to moderate quality, which is expected in study has shown that the patriarchal characteristics of the Turkish
C.R. Mendona et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 215 (2017) 153163 161
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