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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Body mass index and human sperm quality: neither one extreme nor the other

E. M. Luque A , A. Tissera B , M. P. Gaggino B , R. I. Molina B , A. Mangeaud C , L. M. Vincenti A , F. Beltramone D , J. Sad Larcher D , D. Estofán D , M. Fiol de Cuneo A and A. C. Martini A E
+ Author Affiliations
- Author Affiliations

A Cátedra de Fisiología Humana, Instituto de Investigaciones en Ciencias de la Salud (INICSA), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina.

B Laboratorio de Andrología y Reproducción (LAR), Chacabuco 1089, X5000IIK Córdoba, Argentina.

C Cátedra de Estadística y Biometría, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Vélez Sarsfield 299, 5000 Córdoba, Argentina.

D Centro Integral de Ginecología, Obstetricia y Reproducción (CIGOR), Chacabuco 1123, X5000IIL Córdoba, Argentina.

E Corresponding author. Email: acmartini2000@yahoo.com

Reproduction, Fertility and Development 29(4) 731-739 https://doi.org/10.1071/RD15351
Submitted: 29 August 2015  Accepted: 17 November 2015   Published: 18 December 2015

Abstract

The aim of the present study was to investigate the still contentious association between body mass index (BMI) and seminal quality. To this end, 4860 male patients (aged 18–65 years; non-smokers and non-drinkers), were classified according to BMI as either underweight (UW; BMI <20 kg m–2; n = 45), normal weight (NW; BMI 20–24.9 kg m–2; n = 1330), overweight (OW; BMI 25–29.9 kg m–2; n = 2493), obese (OB; BMI 30–39.9 kg m–2; n = 926) or morbidly obese (MOB; BMI ≥40 kg m–2; n = 57). Conventional semen parameters and seminal concentrations of fructose, citric acid and neutral α-glucosidase (NAG) were evaluated. The four parameters that reflect epididymal maturation were significantly lower in the UW and MOB groups compared with NW, OW and OB groups: sperm concentration, total sperm count (103.3 ± 11.4 and 121.5 ± 20.6 and vs 157.9 ± 3.6, 152.4 ± 2.7 or 142.1 ± 4.3 spermatozoa ejaculate–1 respectively, P < 0.05), motility (41.8 ± 2.5 and 42.6 ± 2.6 vs 47.8 ± 0.5, 48.0 ± 0.4 or 46.3 ± 0.6 % of motile spermatozoa respectively, P < 0.05) and NAG (45.2 ± 6.6 and 60.1 ± 7.9 vs 71.5 ± 1.9, 64.7 ± 1.3 or 63.1 ± 2.1 mU ejaculate-1 respectively, P < 0.05). Moreover, the percentage of morphologically normal spermatozoa was decreased in the MOB group compared with the UW, NW, OW and OB groups (4.8 ± 0.6% vs 6.0 ± 0.8%, 6.9 ± 0.1%, 6.8 ± 0.1 and 6.4 ± 0.2%, respectively; P < 0.05). In addition, men in the MOB group had an increased risk (2.3- to 4.9-fold greater) of suffering oligospermia and teratospermia (P < 0.05). Both morbid obesity and being underweight have a negative effect on sperm quality, particularly epididymal maturation. These results show the importance of an adequate or normal bodyweight as the natural best option for fertility, with both extremes of the BMI scale as negative prognostic factors.

Additional keywords: asthenozoospermia, epididymal maturation, epididymis, oligozoospermia, obesity, morbid obesity, teratozoospermia, underweight.


References

Aitken, R. J., Keith, T. J., and Robertson, S. A. (2012). Reactive oxygen species and sperm function: in sickness and in health. J. Androl. 33, 1096–1106.
Reactive oxygen species and sperm function: in sickness and in health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvFaqsQ%3D%3D&md5=010ceeceed5ece4735d0c1e3f6b01b33CAS | 22879525PubMed |

Auger, J., and Eustache, F. (2000). Standarization of the morphological assessment of human spermatozoa according to modified David’s classification. Andrologie 10, 353–387.

Belloc, S., Cohen-Bacrie, M., Amar, E., Izard, V., Benkhalifa, M., Dalléac, A., and de Mouzon, J. (2014). High body mass index has a deleterious effect on semen parameters except morphology: results from a large cohort study. Fertil. Steril. 102, 1268–1273.
High body mass index has a deleterious effect on semen parameters except morphology: results from a large cohort study.Crossref | GoogleScholarGoogle Scholar | 25225071PubMed |

Braga, D. P., Halpern, G., Figueira, R. C., Setti, A. S., Aconelli, A., and Borges, E. (2012). Food intake and social habits in male patients and its relationship to intracytoplasmic sperm injection outcomes. Fertil. Steril. 97, 53–59.
Food intake and social habits in male patients and its relationship to intracytoplasmic sperm injection outcomes.Crossref | GoogleScholarGoogle Scholar | 22078783PubMed |

Cabler, S., Agarwal, A., Flint, M., and du Plessis, S. S. (2010). Obesity. Modern man’s fertility nemesis. Asian J. Androl. 12, 480–489.
Obesity. Modern man’s fertility nemesis.Crossref | GoogleScholarGoogle Scholar | 20531281PubMed |

Campbell, J. M., Lane, M., Owens, J. A., and Bakos, H. W. (2015). Paternal obesity negatively affects male fertility and assisted reproduction outcomes: a systematic review and meta-analysis. Reprod. Biomed. Online 31, 593–604.
Paternal obesity negatively affects male fertility and assisted reproduction outcomes: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 26380863PubMed |

Carlsen, E., Giwercman, A., Keidingand, N., and Skakkebaek, N. F. (1992). Evidence for decreasing quality of semen during the past 50 years. BMJ 305, 609–613.
Evidence for decreasing quality of semen during the past 50 years.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s%2Fgs1Citw%3D%3D&md5=a9b89d12c61ac6a358a947665e886865CAS | 1393072PubMed |

Chauvin, T. R., and Griswold, M. D. (2004). Androgen-regulated genes in the murine epididymis. Biol. Reprod. 71, 560–569.
Androgen-regulated genes in the murine epididymis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgurw%3D&md5=5bdadc7a4cacc38d079dd9c19cc431e4CAS | 15115731PubMed |

Cooper, T. G., Yeung, C. H., Nashan, D., and Nieschlang, E. (1988). Epididymal markers in human infertility. J. Androl. 9, 91–101.
| 1:STN:280:DyaL1c3ls1ynuw%3D%3D&md5=d7f3c5683cd2d24613522a0ec74214a5CAS | 3290172PubMed |

Cooper, T. G., Yeung, C. H., Nasham, D., Jockenhovel, F., and Nieschlag, E. (1990). Improvement in the assesment of human epididymal function by the use of inhibitors in the assay of α-glucosidase in seminal plasma. Int. J. Androl. 13, 297–305.
Improvement in the assesment of human epididymal function by the use of inhibitors in the assay of α-glucosidase in seminal plasma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpslWjtg%3D%3D&md5=34a9a9b6bd2bdb5a0ac939ae9e6a5b3eCAS | 2201650PubMed |

Dadoune, J. P., Mayaux, M. J., and Guilhard-Moscato, M. L. (1988). Correlation between defects in chromatin condensation of human spermatozoa stained by anilin blue and semen characteristics. Andrologia 20, 211–217.
Correlation between defects in chromatin condensation of human spermatozoa stained by anilin blue and semen characteristics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2Fitl2qsQ%3D%3D&md5=a64daac03c49fd99bb23213565ab212cCAS | 3177899PubMed |

Dandona, P., Aljada, A., Chaudhuri, A., Mohanty, P., and Garg, R. (2005). Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 111, 1448–1454.
Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation.Crossref | GoogleScholarGoogle Scholar | 15781756PubMed |

Davì, G., and Falco, A. (2005). Oxidant stress, inflammation and atherogenesis. Lupus 14, 760–764.
Oxidant stress, inflammation and atherogenesis.Crossref | GoogleScholarGoogle Scholar | 16218483PubMed |

Du Plessis, S. S., Cabler, S., McAlister, D. A., Sabanegh, E., and Agarwal, A. (2010). The effect of obesity on sperm disorders and male infertility. Nat. Rev. Urol. 7, 153–161.
The effect of obesity on sperm disorders and male infertility.Crossref | GoogleScholarGoogle Scholar | 20157305PubMed |

Eisenberg, M. L., Kim, S., Chen, Z., Sundaram, R., Schisterman, E. F., and Buck Louis, G. M. (2014). The relationship between male BMI and waist circumference on semen quality: data from the LIFE study. Hum. Reprod. 29, 193–200.
The relationship between male BMI and waist circumference on semen quality: data from the LIFE study.Crossref | GoogleScholarGoogle Scholar | 24306102PubMed |

El-Hefnawy, T., Ioffe, S., and Dym, M. (2000). Expression of the leptin receptor during germ cell development in the mouse testis. Endocrinology 141, 2624–2630.
| 1:CAS:528:DC%2BD3cXlt1Wmurc%3D&md5=37fa31159e9378f5c2f6565b74a9cf28CAS | 10875267PubMed |

Eliasson, R. (1977). Supravital staining of human spermatozoa. Fertil. Steril. 28, 1257.
| 1:STN:280:DyaE1c%2FktlOgug%3D%3D&md5=e0c623e4ee8e245444465a6ee420035cCAS |

European Association for the Study of Obesity (EASO). (2014). ‘Obesity, Perception And Policy: Multi-country Review and Survey of Policymakers 2014.’ (C3 Collaborating for Health: London.)

Fan, Y., Liu, Y., Xue, K., Gu, G., Fan, W., Xu, Y., and Ding, Z. (2015). Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier. PLoS One 10, e0120775.
Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier.Crossref | GoogleScholarGoogle Scholar | 25886196PubMed |

Hammoud, A. O., Wilde, N., Gibson, M., Parks, A., Carrell, D. T., and Meikle, A. W. (2008a). Male obesity and alteration in sperm parameters. Fertil. Steril. 90, 2222–2225.
Male obesity and alteration in sperm parameters.Crossref | GoogleScholarGoogle Scholar | 18178190PubMed |

Hammoud, A. O., Gibson, M., Peterson, C. M., Meikle, A. W., and Carrell, D. T. (2008b). Impact of male obesity on infertility: a critical review of the current literature. Fertil. Steril. 90, 897–904.
Impact of male obesity on infertility: a critical review of the current literature.Crossref | GoogleScholarGoogle Scholar | 18929048PubMed |

Hirsh, A. (2003). ABC of subfertility. BMJ 327, 669–672.
ABC of subfertility.Crossref | GoogleScholarGoogle Scholar | 14500443PubMed |

Jensen, T. K., Andersson, A. M., Jorgensen, N., Andersen, A. G., Carlsen, E., Petersen, J. H., and Skakkebaek, N. E. (2004). Body mass index in relation to semen quality and reproductive hormones among 1558 Danish men. Fertil. Steril. 82, 863–870.
Body mass index in relation to semen quality and reproductive hormones among 1558 Danish men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFOjtrg%3D&md5=2de5a21da6774f4036a75eaa661cf2c0CAS | 15482761PubMed |

Jeyendran, R. S., Van der Ven, H. H., Perez-Pelaez, M., Crabo, B. G., and Zaneveld, L. J. D. (1984). Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics. J. Reprod. Fertil. 70, 219–228.
Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c7hsVKntA%3D%3D&md5=06d09ee95da479410f73e5f8e09ac368CAS | 6694140PubMed |

Jouannet, P., Wang, C., Eustache, F., Kold-Jensen, T., and Auger, J. (2001). Semen quality and male reproductive health: the controversy about human sperm concentration decline. APMIS 109, 333–344.
Semen quality and male reproductive health: the controversy about human sperm concentration decline.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvjtFakuw%3D%3D&md5=04f97a3f95ee32f3bd2e7c72f3768625CAS | 11478681PubMed |

Karvonen, M. J., and Malm, M. (1955). Colorimetric determination of fructose with indol. Scand. J. Clin. Lab. Invest. 7, 305–307.
Colorimetric determination of fructose with indol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG28XlvFKjsw%3D%3D&md5=c2fd13ffb29295ca21b84152c7bdd94eCAS | 13298615PubMed |

Kühnert, B., and Nieschlag, E. (2004). Reproductive functions of the ageing male. Hum. Reprod. Update 10, 327–339.
Reproductive functions of the ageing male.Crossref | GoogleScholarGoogle Scholar | 15192059PubMed |

Kumanov, P., Nandipati, K., Tomova, A., and Agarwal, A. (2006). Inhibin B is a better marker of spermatogenesis than other hormones in the evaluation of male factor infertility. Fertil. Steril. 86, 332–338.
Inhibin B is a better marker of spermatogenesis than other hormones in the evaluation of male factor infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsFejsbk%3D&md5=96ac76016cdd05c71f8e030048c934e5CAS | 16764873PubMed |

Lampiao, F., and du Plessis, S. S. (2008). TNF-alpha and IL-6 affect human sperm function by elevating nitric oxide production. Reprod. Biomed. Online 17, 628–631.
TNF-alpha and IL-6 affect human sperm function by elevating nitric oxide production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFektbvO&md5=bc56d16e3d53be8bcbb5445459ed06bcCAS | 18983746PubMed |

Li, Y., Putman-Lawson, C. A., Knapp-Hoch, H., Friel, P. J., Mitchell, D., Hively, R., and Griswold, M. D. (2005). Immunolocalization and regulation of cystatin 12 in mouse testis and epididymis. Biol. Reprod. 73, 872–880.
Immunolocalization and regulation of cystatin 12 in mouse testis and epididymis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGktb7N&md5=282b68723ace9a6e6cd7c9af22f24660CAS | 15972886PubMed |

MacDonald, A. A., Herbinson, G. P., Showell, M., and Farquhar, C. M. (2010). The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis. Hum. Reprod. Update 16, 293–311.
The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Kms74%3D&md5=24ee189546d91c7a2679f522ab80e2bfCAS | 19889752PubMed |

Mah, P. M., and Wittert, G. A. (2010). Obesity and testicular function. Mol. Cell. Endocrinol. 316, 180–186.
Obesity and testicular function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WgtbnF&md5=a5cd598966d2b2900a1a3cc210ba5a1eCAS | 19540307PubMed |

Mahmoud, A. M., Geslevich, J., Kint, J., Depuydt, C., Huysse, L., Zalata, A., and Comhaire, F. H. (1998). Seminal plasma alpha-glucosidase activity and male infertility. Hum. Reprod. 13, 591–595.
Seminal plasma alpha-glucosidase activity and male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFyqtL4%3D&md5=6b23e89c41e73af4519328547af1ee44CAS | 9572418PubMed |

Makler, A. (1980). The improved ten microliter chamber for rapid sperm count and motility evaluation. Fertil. Steril. 33, 337–338.
| 1:STN:280:DyaL3c7lslWltQ%3D%3D&md5=74aca8067ae95395c2c97ea37db5f3deCAS | 6892698PubMed |

Mann, T., and Lutwak-Mann, C. (1981). ‘Male Reproductive Functions and Semen. Themes and Trends in Physiology, Biochemestry and Investigative Andrology.’ (Springer-Verlag: Berlin.)

Martini, A. C., Molina, R. I., Vincenti, L. M., Santillán, M. E., Stutz, G., Ruiz, R. D., and Fiol de Cuneo, M. (2007). Neutral alpha-glucosidase activity in mouse: a marker of epididymal function? Reprod. Fertil. Dev. 19, 563–568.
Neutral alpha-glucosidase activity in mouse: a marker of epididymal function?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltFyitro%3D&md5=709003e0ad27bff315f9a879642077ceCAS | 17524301PubMed |

Martini, A. C., Tissera, A., Estofán, D., Molina, R. I., Mangeaud, A., Fiol de Cuneo, M., and Ruiz, R. D. (2010). Overweight and seminal quality: a study in 794 patients. Fertil. Steril. 94, 1739–1743.
Overweight and seminal quality: a study in 794 patients.Crossref | GoogleScholarGoogle Scholar | 20056217PubMed |

Martini, A. C., Molina, R. I., Tissera, A., Ruiz, R. D., and Fiol de Cuneo, M. (2013). The impact of obesity on male reproduction: its biological significance. Expert Rev. Endocrinol. Metab. 8, 139–148.
The impact of obesity on male reproduction: its biological significance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtF2ku7s%3D&md5=e75b2bf4075f6a460213686b36906a0eCAS |

Menkveld, R., Stander, F. S., Kotze, T. J., Kruger, T. F., and van Zyl, J. A. (1990). The evaluation of morphological characteristics of human spermatozoa according to stricter criteria. Hum. Reprod. 5, 586–592.
| 1:STN:280:DyaK3czmvV2jug%3D%3D&md5=9dc60b3f639429efae8a86374f153630CAS | 2394790PubMed |

Pauli, E. M., Legro, R. S., Demers, L. M., Kunselman, A. R., Dodson, W. C., and Lee, P. A. (2008). Diminished paternity and gonadal function with increasing obesity in men. Fertil. Steril. 90, 346–351.
Diminished paternity and gonadal function with increasing obesity in men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVGlsLvM&md5=f9c29a81e0e46d64a489d4adcc30dddeCAS | 18291378PubMed |

Qin, D. D., Yuan, W., Zhou, W. J., Cui, Y. Q., Wu, J. Q., and Gao, E. S. (2007). Do reproductive hormones explain the association between body mass index and semen quality? Asian J. Androl. 9, 827–834.
Do reproductive hormones explain the association between body mass index and semen quality?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVWrtLbL&md5=a3709fee55cf8d82a0f83b8f96a8197aCAS | 17968470PubMed |

Ramlau-Hansen, C. H., Hansen, M., Jensen, C. R., Olsen, J., Bonde, J. P., and Thulstrup, A. M. (2010). Semen quality and reproductive hormones according to birth weight and body mass index in childhood and adult life: two decades of follow-up. Fertil. Steril. 94, 610–618.
Semen quality and reproductive hormones according to birth weight and body mass index in childhood and adult life: two decades of follow-up.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFansb8%3D&md5=b8e5510057e310c1df6eaff99739e3a6CAS | 19328465PubMed |

Samavat, J., Natali, I., Degl’Innocenti, S., Filimberti, E., Cantini, G., Di Franco, A., Danza, G., Seghieri, G., Lucchese, M., Baldi, E., Forti, G., and Luconi, M. (2014). Acrosome reaction is impaired in spermatozoa of obese men: a preliminary study. Fertil. Steril. 102, 1274–1281.e2.
Acrosome reaction is impaired in spermatozoa of obese men: a preliminary study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVOku77J&md5=5a78bb16e792c309aa38da2d18233c3aCAS | 25226854PubMed |

Schneider, J. E. (2004). Energy balance and reproduction. Physiol. Behav. 81, 289–317.
Energy balance and reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1Srtrg%3D&md5=3c969c1a377224f7f9f17f82c3af5425CAS | 15159173PubMed |

Sermondade, N., Faure, C., Fezeu, L., Lévy, R., Czernichow, S., Obesity-Fertility Collaborative Group (2012). Obesity and increased risk for oligozoospermia and azoospermia. Arch. Intern. Med. 172, 440–442.
Obesity and increased risk for oligozoospermia and azoospermia.Crossref | GoogleScholarGoogle Scholar | 22412113PubMed |

Sermondade, N., Faure, C., Fezeu, L., Shayeb, A. G., Bonde, J. P., Jensen, T. K., Van Wely, M., Cao, J., Martini, A. C., Eskandar, M., Chavarro, J. E., Koloszar, S., Twigt, J. M., Ramlau-Hansen, C. H., Borges, E., Lotti, F., Steegers-Theunissen, R. P., Zorn, B., Polotsky, A. J., La Vignera, S., Eskenazi, B., Tremellen, K., Magnusdottir, E. V., Fejes, I., Hercberg, S., Lévy, R., and Czernichow, S. (2013). BMI in relation to sperm count: an updated systematic review and collaborative meta-analysis. Hum. Reprod. Update 19, 221–231.
BMI in relation to sperm count: an updated systematic review and collaborative meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s3it1Kltw%3D%3D&md5=35b8412d9afd762483739badb4398c6aCAS | 23242914PubMed |

Shayeb, A. G., Harrild, K., Mathers, E., and Bhattacharya, S. (2011). An exploration of the association between male body mass index and semen quality. Reprod. Biomed. Online 23, 717–723.
An exploration of the association between male body mass index and semen quality.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38%2FksFylsw%3D%3D&md5=3a4dd9894f449e29252f157bddc5d4f9CAS | 22019618PubMed |

Spira, A., and Multigner, L. (1998). The effects of industrial and agricultural pollution on human spermatogenesis. Hum. Reprod. 13, 2041–2042.
The effects of industrial and agricultural pollution on human spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmt1Wjs7Y%3D&md5=232427934b1f249b1b6620830b778a72CAS | 9756262PubMed |

Stewart, T. M., Liu, D. Y., Garrett, C., Jorgensen, N., Brown, E. H., and Baker, H. W. (2009). Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output. Hum. Reprod. 24, 1561–1568.
Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslGrsr4%3D&md5=938b68d2aaf287e06d296907f455f205CAS | 19351657PubMed |

Swan, S. H., Elkin, E. P., and Fenster, L. (2000). The question of declining sperm density revisited: an analysis of 101 studies published 1934–1996. Environ. Health Perspect. 108, 961–966.
The question of declining sperm density revisited: an analysis of 101 studies published 1934–1996.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FlvV2ntg%3D%3D&md5=60019b5ef489a0175124789effc8beb6CAS | 11049816PubMed |

Teerds, K. J., de Rooij, D. G., and Keijer, J. (2011). Functional relationship between obesity and male reproduction: from humans to animal models. Hum. Reprod. Update 17, 667–683.
Functional relationship between obesity and male reproduction: from humans to animal models.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MjmslamsA%3D%3D&md5=66de1a8ada80c599c663174050fc134fCAS | 21546379PubMed |

Tena-Sempere, M. (2013). Interaction between energy homeostasis and reproduction: central effects of leptin and ghrelin on the reproductive axis. Horm. Metab. Res. 45, 919–927.
Interaction between energy homeostasis and reproduction: central effects of leptin and ghrelin on the reproductive axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVOrsL8%3D&md5=c1732e789d7e704b6ef61a934fe121aeCAS | 24155252PubMed |

Thomsen, L., Humaidan, P., Bungum, L., and Bungum, M. (2014). The impact of male overweight on semen quality and outcome of assisted reproduction. Asian J. Androl. 16, 749–754.
The impact of male overweight on semen quality and outcome of assisted reproduction.Crossref | GoogleScholarGoogle Scholar | 24759576PubMed |

Wade, G. N. (1999). Energy balance, effects on reproduction. In ‘The physiology of reproduction’. (Eds E. Knobil and J. D. Neill). pp. 1091–1100. (Raven Press: New York.)

Winters, S. J., Wang, C., Abdelrahaman, E., Hadeed, V., Dyky, M. A., and Brufsky, A. (2006). Inhibin-B levels in healthy young adult men and prepuberal boys: is obesity the cause for the contemporary decline in sperm count because of fewer Sertoli cells? J. Androl. 27, 560–564.
Inhibin-B levels in healthy young adult men and prepuberal boys: is obesity the cause for the contemporary decline in sperm count because of fewer Sertoli cells?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVaqsr4%3D&md5=4f98ce06b19556fbb8c1a9bbdbb3a107CAS | 16582411PubMed |

World Health Organization (WHO). (2010a). ‘Estimated Overweight and Obesity Prevalence, Males, Aged 15+.’ Available at: https://apps.who.int/infobase/Index.aspx [verified 2 February 2015].

World Health Organization (WHO). (2010b). ‘WHO Laboratory Manual for the Examination and Processing of Human Semen.’ 5th edn. (WHO Press: Geneva, Switzerland.)

Yanagimachi, R. (1994). Mammalian fertilization. In ‘The Physiology of Reproduction’. (Eds E. Knobil and J.D. Neill). pp. 189–317. (Raven Press, New York, USA).