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Research Letters |

Obesity and Increased Risk for Oligozoospermia and Azoospermia FREE

Nathalie Sermondade, MD, MSc; Céline Faure, PhD; Léopold Fezeu, MD, PhD; Rachel Lévy, MD, PhD; Sébastien Czernichow, MD, PhD; and the Obesity-Fertility Collaborative Group
[+] Author Affiliations

Author Affiliations: Service d’Histologie-Embryologie-Cytogénétique-CECOS, Hôpital Jean Verdier (Assistance Publique–Hôpitaux de Paris [AP-HP]), Bondy, France (Drs Sermondade, Faure, and Lévy); Research Unit on Nutritional Epidemiology, UMR U557 INSERM, U1125 INRA, CNAM, Université Paris 13, Bobigny, France (Drs Sermondade, Faure, Fezeu, and Lévy); and Department of Nutrition, Ambroise Paré Hospital, University of Versailles St Quentin en Yvelines, Boulogne-Billancourt, France, and INSERM, U1018, Centre for Research in Epidemiology and Population Health, Villejuif, France (Dr Czernichow).


Arch Intern Med. 2012;172(5):440-442. doi:10.1001/archinternmed.2011.1382.
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The global obesity epidemic parallels a decrease in male fertility. Yet, the association between body mass index (BMI) and sperm parameters remains controversial. A negative correlation between BMI and sperm concentration or total sperm count was shown by several reports1,2 but not documented by others.3,4 The purpose of this report was to update the level of evidence on the association between BMI and sperm count through a systematic review and meta-analysis.

A systematic review of available literature was conducted to investigate the impact of BMI on sperm count in men according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) statement. A PubMed and EMBASE search identified relevant studies published until October 2010. Authors of relevant studies were contacted by e-mail and asked to complete a standardized data form regarding total sperm counts according to BMI categories. Unpublished data obtained from patients followed at the Infertility Center of Jean Verdier Hospital, Bondy, France, between January 2007 and December 2010 were also included.

The following BMI categories were used for analyses: lower than 18.5, 18.5 to 24.9, 25.0 to 29.9, and 30.0 or higher (calculated as weight in kilograms divided by height in meters squared). Data were stratified according to total sperm count as having normozoospermia (≥40 × 106 spermatozoa per ejaculate), oligozoospermia (<40 × 106 but >0 spermatozoa per ejaculate), and azoospermia (absence of spermatozoa), as specified in World Health Organization guidelines.5 We performed random effects models to obtain summary estimates to account for interstudy variation. Studies were weighted according to an estimate of statistical size defined as the inverse of the variance of the log odds ratio (OR). Prevalent ORs and 95% confidence intervals are presented. We calculated the ORs of overweight and obese men presenting with oligozoospermia or azoospermia compared with normal-weight men.

A total of 8873 articles were identified. In total, 31 articles were potentially appropriate to be included in the meta-analysis because they investigated the relationship between BMI and sperm parameters. A total of 14 eligible studies were included in the present meta-analysis, corresponding to a total study sample of 9779 individuals. Overweight men were at significantly increased odds of presenting with oligozoospermia (OR, 1.11; 95% CI, 1.01-1.20) or azoospermia (OR, 1.39; 95% CI, 0.98-1.97) compared with normal-weight men (Figure). Likewise, obese men were at increased risk of oligozoospermia (OR, 1.42; 95% CI, 1.12-1.79) or azoospermia (OR, 1.81; 95% CI, 1.23-2.66) compared with normal-weight men (Figure).

Place holder to copy figure label and caption
Graphic Jump Location

Figure. Association between oligozoospermia and azoospermia stratified by body mass index (BMI) categories. Normal weight: BMI between 18.5 and 24.9 (calculated as weight in kilograms divided by height in meters squared); overweight: BMI between 25.0 and 29.9; obese: BMI greater than 30.0. * P value for heterogeneity. OR indicates odds ratio.

This meta-analysis based on 9779 men showed an inverse association between overweight or obesity and abnormal sperm count. This relationship may be explained by different pathophysiological hypotheses: (1) hypogonadotropic hyperestrogenic hypogonadism due to aromatization of steroids in estrogens in peripheral tissues6; (2) direct alterations of spermatogenesis and Sertoli cell function7; (3) hip, abdominal, and scrotal fat-tissue accumulation leading to the increase of scrotal temperature8; and (4) accumulation of toxic substances and liposoluble endocrine disruptors in fatty tissue.2

Our strategy based on individual patient data and analysis of dichotomized sperm count made it possible to have a more homogeneous meta-analysis of the available evidence. Limitations of our study are the exclusion of 15 studies because of incomplete data or lack of response from authors and the variations in the study populations. Yet, this variability suggests that our findings may be generalizable to both infertile and general population. We were also reliant on BMI and conventional semen parameters as relevant measures of body fat content and assessment of fertility potential. However, even if they may not be the best indicators, they remain the gold standard for clinical evaluation of adiposity and male fertility, respectively, and allow a clear application of our findings. On the other hand, the strengths of our meta-analysis are a large sample size based on a collection of individual level data.

In conclusion, overweight and obesity are associated with an increased risk of azoospermia or oligozoospermia. These data strongly suggest that excess body weight affects sperm production.

Correspondence: Dr Czernichow, Department of Nutrition, Ambroise Paré Hospital (AP-HP), 9 Ave Charles-de-Gaulle, 92100 Boulogne-Billancourt, France (sebastien.czernichow@apr.aphp.fr).

Author Contributions: Drs Sermondade, Fezeu, and Czernichow had full access to all data in the study and take responsibility for the integrity of the data and the accuracy of the data analyses. Drs Lévy and Czernichow contributed equally to the manuscript. Study concept and design: Sermondade, Lévy, and Czernichow. Acquisition of data: Sermondade. Analysis and interpretation of data: Sermondade, Faure, Fezeu, Lévy, and Czernichow. Drafting of the manuscript: Sermondade and Czernichow. Critical revision of the manuscript for important intellectual content: Sermondade, Faure, Fezeu, and Czernichow. Statistical analysis: Fezeu and Czernichow. Administrative, technical, and material support: Sermondade, Faure, and Lévy. Study supervision: Lévy and Czernichow.

The Obesity-Fertility Collaborative Group: Nathalie Sermondade, MD, MSc, Céline Faure, PhD, Léopold Fezeu, MD, PhD, and Rachel Lévy, MD, PhD (Hôpital Jean Verdier, Bondy, France & Université Paris 13, Bobigny, France); Sébastien Czernichow, MD, PhD (Ambroise Paré Hospital & University of Versailles Saint Quentin en Yvelines, Boulogne-Billancourt, France, and INSERM, U1018, Centre for Research in Epidemiology and Population Health, Villejuif, France); Tina Kold Jensen, MD, PhD (Rigshospitalet, Copenhagen, Denmark); Madelon Van Wely, PhD (Academic Medical Centre, Amsterdam, the Netherlands); Jia Cao, PhD (Third Military Medical University, Chongqing, China); Ana Carolina Martini, PhD (Universidad Nacional de Córdoba, Córdoba, Argentina); Jorge Chavarro, MD, PhD (Brigham and Women's Hospital & Harvard Medical School, Boston, Massachusetts); Sandor Koloszar, MD, PhD (University of Szeged, Szeged, Hungary); Cecilia H. Ramlau-Hansen, MHSc, PhD (Aarhus University, Aarhus C, Denmark); Régine P. M. Steegers-Theunissen, MD, PhD (Erasmus University Medical Center, Rotterdam, the Netherlands); Branko Zorn, MD, PhD (University Medical Center, Ljubljana, Slovenia); Alex J. Polotsky, MD, MSc (University of Colorado Denver, Aurora); Brenda Eskenazi, PhD (UC Berkeley School of Public Health, Berkeley, California); Elin V. Magnusdottir, MSc (University of Iceland, Reykjavik); Imre Fejes, MD, PhD (University of Szeged, Szeged, Hungary); and Serge Hercberg, MD, PhD (Hôpital Avicenne, Bobigny, France & Université Paris 13, Bobigny).

Financial Disclosure: None reported.

Funding/Support: Dr Chavarro was supported in part by National Institute of Diabetes and Digestive and Kidney Diseases grant 5P30DK046200-19 and Dr Eskenazi was supported in part by National Institutes of Health grant P42ES04705.

Additional Contributions: The following individuals or departments performed the data collection in each of their centers: Niels Jorgensen, Rigshospitalet, Copenhagen, Denmark; Yafei Li, Third Military Medical University, Chongqing, China; Zhihong Cui, Third Military Medical University, Chongqing, China; Rosa Molina, Laboratorio de Andrologia y Reproduccion, Córdoba, Argentina; Ruben Daniel Ruiz, Facultad de Ciencias Medicas, Universidad Nacional de Córdoba, Córdoba, Argentina; Thomas L. Toth, Harvard Medical School, Boston, Massachusetts; Russ Hauser, Harvard School of Public Health, Boston; Janos Szollosi, University of Szeged, Szeged, Hungary; Ane Marie Thulstrup, Aarhus University Hospital, Aarhus, Denmark; Joop Laven, Marijana Vujkovic, and Fatima Hammiche, Erasmus University Medical Center, Rotterdam, the Netherlands; Gregor Majdic, Center for Animal Genomics, Veterinary Faculty, University of Ljubljana, Ljubljana, Slovenia; Rosana Hernandez Weldon, UC Berkeley School of Public Health, Berkeley, California; Andrew J. Wyrobek, Lawrence Berkeley National Laboratory, Berkeley; Department of Assisted Reproduction, Landspitali University Hospital, Landspitali, Iceland; and Zoltan Zavaczki, Landstinget Gavleborg, Hudiksvall, Sweden.

Hammoud AO, Wilde N, Gibson M, Parks A, Carrell DT, Meikle AW. Male obesity and alteration in sperm parameters.  Fertil Steril. 2008;90(6):2222-2225
PubMed   |  Link to Article
Magnusdottir EV, Thorsteinsson T, Thorsteinsdottir S, Heimisdottir M, Olafsdottir K. Persistent organochlorines, sedentary occupation, obesity and human male subfertility.  Hum Reprod. 2005;20(1):208-215
PubMed   |  Link to Article
Chavarro JE, Toth TL, Wright DL, Meeker JD, Hauser R. Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic.  Fertil Steril. 2010;93(7):2222-2231
PubMed   |  Link to Article
Jensen TK, Andersson AM, Jørgensen N,  et al.  Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men.  Fertil Steril. 2004;82(4):863-870
PubMed   |  Link to Article
Cooper TG, Noonan E, von Eckardstein S,  et al.  World Health Organization reference values for human semen characteristics.  Hum Reprod Update. 2010;16(3):231-245
PubMed   |  Link to Article
Schneider G, Kirschner MA, Berkowitz R, Ertel NH. Increased estrogen production in obese men.  J Clin Endocrinol Metab. 1979;48(4):633-638
PubMed   |  Link to Article
Winters SJ, Wang C, Abdelrahaman E, Hadeed V, Dyky MA, Brufsky A. Inhibin-B levels in healthy young adult men and prepubertal boys: is obesity the cause for the contemporary decline in sperm count because of fewer Sertoli cells?  J Androl. 2006;27(4):560-564
PubMed   |  Link to Article
Shafik A, Olfat S. Scrotal lipomatosis.  Br J Urol. 1981;53(1):50-54
PubMed   |  Link to Article

Figures

Place holder to copy figure label and caption
Graphic Jump Location

Figure. Association between oligozoospermia and azoospermia stratified by body mass index (BMI) categories. Normal weight: BMI between 18.5 and 24.9 (calculated as weight in kilograms divided by height in meters squared); overweight: BMI between 25.0 and 29.9; obese: BMI greater than 30.0. * P value for heterogeneity. OR indicates odds ratio.

Tables

References

Hammoud AO, Wilde N, Gibson M, Parks A, Carrell DT, Meikle AW. Male obesity and alteration in sperm parameters.  Fertil Steril. 2008;90(6):2222-2225
PubMed   |  Link to Article
Magnusdottir EV, Thorsteinsson T, Thorsteinsdottir S, Heimisdottir M, Olafsdottir K. Persistent organochlorines, sedentary occupation, obesity and human male subfertility.  Hum Reprod. 2005;20(1):208-215
PubMed   |  Link to Article
Chavarro JE, Toth TL, Wright DL, Meeker JD, Hauser R. Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic.  Fertil Steril. 2010;93(7):2222-2231
PubMed   |  Link to Article
Jensen TK, Andersson AM, Jørgensen N,  et al.  Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men.  Fertil Steril. 2004;82(4):863-870
PubMed   |  Link to Article
Cooper TG, Noonan E, von Eckardstein S,  et al.  World Health Organization reference values for human semen characteristics.  Hum Reprod Update. 2010;16(3):231-245
PubMed   |  Link to Article
Schneider G, Kirschner MA, Berkowitz R, Ertel NH. Increased estrogen production in obese men.  J Clin Endocrinol Metab. 1979;48(4):633-638
PubMed   |  Link to Article
Winters SJ, Wang C, Abdelrahaman E, Hadeed V, Dyky MA, Brufsky A. Inhibin-B levels in healthy young adult men and prepubertal boys: is obesity the cause for the contemporary decline in sperm count because of fewer Sertoli cells?  J Androl. 2006;27(4):560-564
PubMed   |  Link to Article
Shafik A, Olfat S. Scrotal lipomatosis.  Br J Urol. 1981;53(1):50-54
PubMed   |  Link to Article

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