The complex interaction between obesity, metabolic syndrome and reproductive axis: A narrative review

Michalakis, Konstantinos; Mintziori, Gesthimani; Kaprara, Athina; Tarlatzis, Basil C.; Goulis, Dimitrios G.

doi:10.1016/j.metabol.2012.08.012

Cited by 321Hypothalamic control of reproductive hormonesOvarian function and disordersAdipokines, Inflammation, and Metabolic Diseases

The complex interaction between obesity, metabolic syndrome and reproductive axis: A narrative review

Michalakis, Konstantinos, Mintziori, Gesthimani, Kaprara, Athina, Tarlatzis, Basil C., Goulis, Dimitrios G.·2013·Metabolism

DOI 10.1016/j.metabol.2012.08.012

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Abstract

The aim of this narrative review is to provide current evidence for the interaction between obesity, metabolic syndrome (MS) and reproductive axis. Gonadotropin-releasing hormone (GnRH) pulses and, consequently, normal function of reproductive (hypothalamus-pituitary-gonadal) axis depend on normal energy balance, which presupposes sufficient food intake, reasonable energy consumption and average thermoregulatory costs. In case of an energy imbalance, reproductive dysfunction may occur. In young women, excessive leanness is accompanied by puberty delay, whereas premature puberty might be a manifestation of obesity. In a similar way, obesity in men affects fertility. Excess adipose tissue results in increased conversion of testosterone to estradiol, which may lead to secondary hypogonadism through reproductive axis suppression. Moreover, oxidative stress at the level of the testicular micro-environment may result in decreased spermatogenesis and sperm damage. Products of the adipocyte, such as leptin, adiponectin and resistin, and gut peptides, such as ghrelin, are considered to be crucial in the interaction between energy balance and reproduction. Finally, an indirect evidence for the interplay between MS and reproductive axis is the fact that when treating components of one, parameters of the other can be improved as well. These therapeutic interventions include lifestyle modifications, pharmacological agents, such as sex hormone replacement therapy, and surgical procedures. Although many issues remain unclear, the elucidation of the complex interaction between MS and reproductive axis will have obvious clinical implications in the therapeutic approach of both entities.

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Several adipokines were proposed as negative mediators on the reproductive axis.
“Several adipokines were proposed as negative mediators on the reproductive axis (28).”
From Effects of liraglutide on obesity-associated functional hypogonadism in men (2019) · cites this paper as [28]

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Visceral fat accumulation in relation to sex hormones in obese men and women undergoing weight loss therapy
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Lifestyle and nutritional determinants of bioavailable androgens and related hormones in British men
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PPAR-γ Activation Mediates Adipose Depot−Specific Effects on Gene Expression and Lipoprotein Lipase Activity
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Leptin Is Inversely Related to Age at Menarche in Human Females
Matkovic, V. (1997) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.10.3239 · Cited by 152 · see citing works
Comparative Analysis of the Effects of Ghrelin and Unacylated Ghrelin on Luteinizing Hormone Secretion in Male Rats
Martini, A. C., Fernández-Fernández, R., Tovar, S. A., Navarro, V. M., Vigo, E., Vazquez, M. J., Davies, J. S., Thompson, N. M., Aguilar, E., Pinilla, L., et al. (2006) · Endocrinology · doi:10.1210/en.2005-1422 · Cited by 151 · see citing works
Novel Expression and Direct Effects of Adiponectin in the Rat Testis
Caminos, J. E., Nogueiras, R., Gaytán, F., Pineda, R., González, C. R., Barreiro, M. L., Castano, J. P., Malagón, M. M., Pinilla, L., Toppari, J., et al. (2008) · Endocrinology · doi:10.1210/en.2007-1582 · Cited by 151 · see citing works
Erectile dysfunction and hormonal imbalance in morbidly obese male is reversed after gastric bypass surgery: a prospective randomized controlled trial
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Effects of ghrelin on Kisspeptin mRNA expression in the hypothalamic medial preoptic area and pulsatile luteinising hormone secretion in the female rat
Forbes, S. C., Li, X. F., Kinsey‐Jones, J. S., & O’Byrne, K. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.05.060 · Cited by 150 · see citing works
Obesity and reproduction
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Chemerin inhibits IGF-1-induced progesterone and estradiol secretion in human granulosa cells
Reverchon, M., Cornuau, M., Ramé, C., Guérif, F., Royère, D., & Dupont, J. (2012) · Human Reproduction · doi:10.1093/humrep/des089 · Cited by 149 · see citing works
Effects of Chronic Hyperghrelinemia on Puberty Onset and Pregnancy Outcome in the Rat
Fernández-Fernández, R., Navarro, V. M., Barreiro, M. L., Vigo, E., Tovar, S. A., Sirotkin, A. V., Casanueva, F. F., Aguilar, E., Diéguez, C., Pinilla, L., et al. (2005) · Endocrinology · doi:10.1210/en.2004-1622 · Cited by 147 · see citing works
Effect of dieting on plasma leptin, soluble leptin receptor, adiponectin and resistin levels in healthy volunteers
Wolfe, B. E., Jimerson, D. C., Orlova, C., & Mantzoros, C. S. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02101.x · Cited by 146 · see citing works
The long-term effect of recombinant methionyl human leptin therapy on hyperandrogenism and menstrual function in female and pituitary function in male and female hypoleptinemic lipodystrophic patients
Musso, C., Cochran, E., Javor, E., Young, J., DePaoli, A. M., & Gorden, P. (2005) · Metabolism · doi:10.1016/j.metabol.2004.08.021 · Cited by 146 · see citing works
The ‘beneficial’ adipokines in reproduction and fertility
Campos, D. B., Palin, M., Bordignon, V., & Murphy, B. D. (2007) · International Journal of Obesity · doi:10.1038/sj.ijo.0803719 · Cited by 144 · see citing works
Body size affects measures of ovarian reserve in late reproductive age women
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Leptin in reproduction.
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Integration of hormonal and nutrient signals that regulate leptin synthesis and secretion
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Hypothalamic Sites of Leptin Action Linking Metabolism and Reproduction
Donato, J., Cravo, R. M., Frazão, R., & Elias, C. F. (2010) · Neuroendocrinology · doi:10.1159/000322472 · Cited by 141 · see citing works
Letrozole once a week normalizes serum testosterone in obesity-related male hypogonadism
Loves, S., Ruinemans-Koerts, J., & de Boer, H. (2008) · European Journal of Endocrinology · doi:10.1530/eje-07-0663 · Cited by 141 · see citing works
Sexual dysfunction in obese and overweight women
Yaylalı, G. F., Tekekoğlu, S. D., & Akın, F. (2010) · International Journal of Impotence Research · doi:10.1038/ijir.2010.7 · Cited by 140 · see citing works
Fatness, Menarche, and Female Fertility
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Metformin Treatment May Increase Omentin-1 Levels in Women With Polycystic Ovary Syndrome
Tan, B. K., Adya, R., Syed, F., Chen, J., Lehnert, H., & Randeva, H. S. (2010) · Diabetes · doi:10.2337/db10-0124 · Cited by 138 · see citing works
Cross-Sectional Associations of Resistin, Coronary Heart Disease, and Insulin Resistance
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17 -Hydroxyprogesterone Responses to Leuprolide and Serum Androgens in Obese Women with and without Polycystic Ovary Syndrome after Dietary Weight Loss
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Obesity and Increased Risk for Oligozoospermia and Azoospermia
Sermondade, N. (2012) · Archives of Internal Medicine · doi:10.1001/archinternmed.2011.1382 · Cited by 136 · see citing works
Sex Hormone Changes in Morbidly Obese Patients after Vertical Banded Gastroplasty
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Higher serum testosterone concentration in older women is associated with insulin resistance, metabolic syndrome, and cardiovascular disease
Patel, S. M., Ratcliffe, S. J., Reilly, M. P., Weinstein, R., Bhasin, S., Blackman, M. R., Cauley, J. A., Sutton-Tyrrell, K., Robbins, J., Fried, L. P., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-0740 · Cited by 132 · see citing works
Effects of leptin and adiponectin on pancreatic β-cell function
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IMPACT OF OBESITY ON FEMALE REPRODUCTIVE FUNCTION
Калинкина, О. Б., Калинкина, О. Б., Tezikov, Y. V., Владимирович, Т. Ю., Станиславович, Л. И., Станиславович, Л. И., Аравина, О. Р., & Аравина, О. Р. (2016) · Aspirantskiy Vestnik Povolzhiya · doi:10.17816/2072-2354.2016.0.5-6.55-61 · Cited by 131 · see citing works
Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output
Stewart, T. M., Liu, D. Y., Garrett, C., Jørgensen, N., Brown, E., & Baker, H. W. G. (2009) · Human Reproduction · doi:10.1093/humrep/dep075 · Cited by 129 · see citing works
Inhibitory Effect of Obesity on Gonadotropin, Estradiol, and Inhibin B Levels in Fertile Women
Pergola, G. D., Maldera, S., Tartagni, M., Pannacciulli, N., Loverro, G., & GIORGINO, R. (2006) · Obesity · doi:10.1038/oby.2006.228 · Cited by 129 · see citing works
Glucose and Insulin Components of the Metabolic Syndrome Are Associated with Hyperandrogenism in Postmenopausal Women: The Atherosclerosis Risk in Communities Study
Golden, S. H. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh250 · Cited by 121 · see citing works
Effects of weekly administration of pegylated recombinant human OB protein on appetite profile and energy metabolism in obese men
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Adipokine Pattern in Subjects with Impaired Fasting Glucose and Impaired Glucose Tolerance in Comparison to Normal Glucose Tolerance and Diabetes
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Is the plasma anti-Müllerian hormone (AMH) level associated with body weight and metabolic, and hormonal disturbances in women with and without polycystic ovary syndrome?
Skałba, P., Cygal, A., Madej, P., Dąbkowska-Huć, A., Sikora, J., Martirosian, G., Romanik, M. K., & Olszanecka‐Glinianowicz, M. (2011) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2011.06.006 · Cited by 118 · see citing works
Reversal of the hypogonadotropic hypogonadism of obese men by administration of the aromatase inhibitor testolactone
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Treatment of male infertility secondary to morbid obesity
Roth, M. Y., Amory, J. K., & Page, S. T. (2008) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0844 · Cited by 115 · see citing works
Human Resistin Gene, Obesity, and Type 2 Diabetes
Sentinelli, F., Romeo, S., Arca, M., Filippi, E., Leonetti, F., Banchieri, M., Mario, U. D., & Baroni, M. G. (2002) · Diabetes · doi:10.2337/diabetes.51.3.860 · Cited by 114 · see citing works
Novel expression of resistin in rat testis: functional role and regulation by nutritional status and hormonal factors
Nogueiras, R., Barreiro, M. L., Caminos, J. E., Gaytán, F., Suominen, J., Navarro, V. M., Casanueva, F. F., Aguilar, E., Toppari, J., Diéguez, C., et al. (2004) · Journal of Cell Science · doi:10.1242/jcs.01196 · Cited by 113 · see citing works
Contraceptive Treatment after Biliopancreatic Diversion Needs Consensus
Gerrits, E. G., Ceulemans, R., Hee, R. H. G. G. V., Hendrickx, L., & Totté, E. (2003) · Obesity Surgery · doi:10.1381/096089203765887697 · Cited by 113 · see citing works
Letrozole normalizes serum testosterone in severely obese men with hypogonadotropic hypogonadism
De Boer, H., Verschoor, L., Ruinemans‐Koerts, J., & Jansen, M. (2005) · Diabetes, Obesity and Metabolism · doi:10.1111/j.1463-1326.2004.00397.x · Cited by 108 · see citing works
Regulation of adipokine secretion by n -3 fatty acids
Moreno-Aliaga, M. J., Lorente‐Cebrián, S., & Martínez, J. A. (2010) · Proceedings of The Nutrition Society · doi:10.1017/s0029665110001801 · Cited by 105 · see citing works
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?
Winters, S. J., Wang, C., Abdelrahaman, E., Hadeed, V., Dyky, M. A., & Brufsky, A. (2006) · Journal of Andrology · doi:10.2164/jandrol.05193 · Cited by 105 · see citing works
Plasma metastin levels are negatively correlated with insulin resistance and free androgens in women with polycystic ovary syndrome
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Gastric Inhibitory Polypeptide Release after Oral Glucose: Relationship to Glucose Intolerance, Diabetes Mellitus, and Obesity
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Balancing ovulation and anovulation: integration of the reproductive and energy balance axes by neuropeptides
Evans, J. J., & Anderson, G. M. (2012) · Human Reproduction Update · doi:10.1093/humupd/dms004 · Cited by 101 · see citing works
The androgenic sex hormone profile is an essential feature of metabolic syndrome in premenopausal women: a controlled community-based study
Korhonen, S., Hippeläinen, M., Vanhala, M. J., Heinonen, S. T., & NISKANEN, L. K. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00347-9 · Cited by 101 · see citing works
Low sex hormone-binding globulin is associated with the metabolic syndrome in postmenopausal women
Weinberg, M. E., Manson, J. E., Buring, J. E., Cook, N. R., Seely, E. W., Ridker, P. M., & Rexrode, K. M. (2006) · Metabolism · doi:10.1016/j.metabol.2006.06.017 · Cited by 101 · see citing works

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What we talk about when we talk about fat
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Body weight loss reverts obesity-associated hypogonadotropic hypogonadism: a systematic review and meta-analysis
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The relationship between male BMI and waist circumference on semen quality: data from the LIFE study
Eisenberg, M. L., Kim, S., Chen, Z., Sundaram, R., Schisterman, E. F., & Louis, G. M. B. (2013) · Human Reproduction · doi:10.1093/humrep/det428 · Cited by 342 · see citing works
Gut microbiome may contribute to insulin resistance and systemic inflammation in obese rodents: a meta-analysis
Jiao, N., Baker, S. S., Nugent, C. A., Tsompana, M., Cai, L., Wang, Y., Buck, M. J., Genco, R. J., Baker, R. D., Zhu, R., et al. (2018) · Physiological Genomics · doi:10.1152/physiolgenomics.00114.2017 · Cited by 276 · see citing works
Obesity, a serious etiologic factor for male subfertility in modern society
Liu, Y., & Ding, Z. (2017) · Reproduction · doi:10.1530/rep-17-0161 · Cited by 237 · see citing works
Sex-specific adipose tissue imprinting of regulatory T cells
Vasanthakumar, A., Chisanga, D., Blume, J., Gloury, R., Britt, K. L., Henstridge, D. C., Zhan, Y., Torres, S. V., Liene, S., Collins, N., et al. (2020) · Nature · doi:10.1038/s41586-020-2040-3 · Cited by 234 · see citing works
The Deep Correlation between Energy Metabolism and Reproduction: A View on the Effects of Nutrition for Women Fertility
Fontana, R., & Torre, S. D. (2016) · Nutrients · doi:10.3390/nu8020087 · Cited by 218 · see citing works
Leptin treatment: Facts and expectations
Paz-Filho, G., Mastronardi, C. A., & Licinio, J. (2014) · Metabolism · doi:10.1016/j.metabol.2014.07.014 · Cited by 220 · see citing works
Cytokines in ovarian folliculogenesis, oocyte maturation and luteinisation
Field, S. L., Dasgupta, T., Cummings, M., & Orsi, N. M. (2013) · Molecular Reproduction and Development · doi:10.1002/mrd.22285 · Cited by 214 · see citing works
An update on physical health and economic consequences of overweight and obesity
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White adipocyte dysfunction and obesity-associated pathologies in humans
Hagberg, C. E., & Spalding, K. L. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00680-1 · Cited by 217 · see citing works
Evolution of pharmacological obesity treatments: focus on adverse side‐effect profiles
Krentz, A. J., Fujioka, K., & Hompesch, M. (2016) · Diabetes Obesity and Metabolism · doi:10.1111/dom.12657 · Cited by 168 · see citing works
The effect of underweight on female and male reproduction
Boutari, C., Pappas, P. D., Mintziori, G., Nigdelis, M. P., Athanasiadis, L., Goulis, D. G., & Mantzoros, C. S. (2020) · Metabolism · doi:10.1016/j.metabol.2020.154229 · Cited by 165 · see citing works
Self-citation
Reduced breastfeeding rates among obese mothers: a review of contributing factors, clinical considerations and future directions
Babendure, J. B., Reifsnider, E., Mendias, E., Moramarco, M. W., & Davila, Y. R. (2015) · International Breastfeeding Journal · doi:10.1186/s13006-015-0046-5 · Cited by 157 · see citing works
Role of leptin in female reproduction
Pérez‐Pérez, A., Sánchez-Jiménez, F., Maymó, J. L., Dueñas, J. L., Varone, C. L., & Sánchez‐Margalet, V. (2014) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2014-0387 · Cited by 154 · see citing works
Leptin and the brain: Influences on brain development, cognitive functioning and psychiatric disorders
Farr, O. M., Tsoukas, M. A., & Mantzoros, C. S. (2014) · Metabolism · doi:10.1016/j.metabol.2014.07.004 · Cited by 146 · see citing works
Infertility as a proxy of general male health: results of a cross-sectional survey
Ventimiglia, E., Capogrosso, P., Boeri, L., Serino, A., Colicchia, M., Ippolito, S., Scano, R., Papaleo, E., Damiano, R., Montorsi, F., et al. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.04.020 · Cited by 136 · see citing works
Steroid biosynthesis in adipose tissue
Li, J., Papadopoulos, V., & Vihma, V. (2015) · Steroids · doi:10.1016/j.steroids.2015.03.016 · Cited by 130 · see citing works
Obesity and male hypogonadism: Tales of a vicious cycle
Carrageta, D. F., Oliveira, P. F., Alves, M. G., & Monteiro, M. P. (2019) · Obesity Reviews · doi:10.1111/obr.12863 · Cited by 130 · see citing works
Low testosterone is associated with disability in men with multiple sclerosis
Bove, R. M., Musallam, A., Healy, B. C., Raghavan, K., Glanz, B., Bakshi, R., Weiner, H. L., Jager, P. L. D., Miller, K. K., & Chitnis, T. (2014) · Multiple Sclerosis Journal · doi:10.1177/1352458514527864 · Cited by 128 · see citing works
The impact of adipose tissue-derived factors on the hypothalamic-pituitary-gonadal (HPG) axis
Tsatsanis, C., Dermitzaki, E., Avgoustinaki, P. D., Malliaraki, N. E., Mytaras, V., & Margioris, A. N. (2015) · HORMONES · doi:10.14310/horm.2002.1649 · Cited by 122 · see citing works
Metabolic and Endocrine Consequences of Bariatric Surgery
Cornejo-Pareja, I. M., Clemente‐Postigo, M., & Tinahones, F. J. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00626 · Cited by 126 · see citing works
Male infertility: lifestyle factors and holistic, complementary, and alternative therapies
Mills, J., & Yao, D. (2016) · Asian Journal of Andrology · doi:10.4103/1008-682x.175779 · Cited by 117 · see citing works
Female infertility: which role for obesity?
on behalf of the Obesity Programs of nutrition, E., Gambineri, A., Laudisio, D., Marocco, C., Radellini, S., Colao, A., & Savastano, S. (2019) · International Journal of Obesity Supplements · doi:10.1038/s41367-019-0009-1 · Cited by 114 · see citing works
Prevalence of male secondary hypogonadism in moderate to severe obesity and its relationship with insulin resistance and excess body weight
Calderón, B., Gómez‐Martín, J. M., Vega‐Piñero, B., Martín‐Hidalgo, A., Galindo, J., Luque‐Ramírez, M., Escobar‐Morreale, H. F., & Botella‐Carretero, J. I. (2016) · Andrology · doi:10.1111/andr.12135 · Cited by 105 · see citing works
Sedentary behavior, physical inactivity and body composition in relation to idiopathic infertility among men and women
Foucaut, A.-M., Faure, C., Julia, C., Czernichow, S., Lévy, R., Dupont, C., & the ALIFERT collaborative group (2019) · PLoS ONE · doi:10.1371/journal.pone.0210770 · Cited by 112 · see citing works
Prevalence of endocrine disorders in obese patients: systematic review and meta-analysis
van Hulsteijn, L. T., Pasquali, R., Casanueva, F., Haluzik, M., Ledoux, S., Monteiro, M. P., Salvador, J., Santini, F., Toplak, H., & Dekkers, O. M. (2020) · European Journal of Endocrinology · doi:10.1530/eje-19-0666 · Cited by 103 · see citing works
Men's knowledge of their own fertility: a population-based survey examining the awareness of factors that are associated with male infertility
Daumler, D., Chan, P. T. K., Lo, K. C., TAKEFMAN, J. E., & Zelkowitz, P. (2016) · Human Reproduction · doi:10.1093/humrep/dew265 · Cited by 103 · see citing works
Effects of liraglutide on obesity-associated functional hypogonadism in men
Jensterle, M., Podbregar, A., Goricar, K., Gregoric, N., & Janez, A. (2019) · Endocrine Connections · doi:10.1530/ec-18-0514 · Cited by 101 · see citing works
The Insulin/IGF System in Mammalian Sexual Development and Reproduction
Neirijnck, Y., Papaioannou, M. D., & Nef, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20184440 · Cited by 99 · see citing works
Adipokines: A gear shift in puberty
Nieuwenhuis, D., Pujol‐Gualdo, N., Arnoldussen, I. A. C., & Kiliaan, A. J. (2020) · Obesity Reviews · doi:10.1111/obr.13005 · Cited by 99 · see citing works
Puberty dysregulation and increased risk of disease in adult life: Possible modes of action
Mantovani, A., & Fučić, A. (2013) · Reproductive Toxicology · doi:10.1016/j.reprotox.2013.06.002 · Cited by 94 · see citing works
The effect of excess body fat on female and male reproduction
Mintziori, G., Nigdelis, M. P., Mathew, H., Mousiolis, A. C., Goulis, D. G., & Mantzoros, C. S. (2020) · Metabolism · doi:10.1016/j.metabol.2020.154193 · Cited by 94 · see citing works
Self-citation
Relationships Between Body Mass Index, Fat Mass, Muscle Mass, and Musculoskeletal Pain in Community Residents
Yoo, J. J., Cho, N. H., Lim, S. H., & Kim, H. A. (2014) · Arthritis & Rheumatology · doi:10.1002/art.38861 · Cited by 89 · see citing works
Resistin, interleukin-6, tumor necrosis factor-alpha, and human semen parameters in the presence of leukocytospermia, smoking habit, and varicocele
Moretti, E., Collodel, G., Mazzi, L., Campagna, M., Iacoponi, F., & Figura, N. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.04.017 · Cited by 89 · see citing works
Physical activity before IVF and ICSI cycles in infertile obese women: an observational cohort study
Palomba, S., Falbo, A., Valli, B., Morini, D., Villani, M. T., Nicoli, A., & La Sala, G. B. (2014) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2014.03.006 · Cited by 87 · see citing works
Beyond the X Factor: Relevance of Sex Hormones in NAFLD Pathophysiology
Torre, S. D. (2021) · Cells · doi:10.3390/cells10092502 · Cited by 89 · see citing works
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The Impact of the Endocrine and Immunological Function of Adipose Tissue on Reproduction in Women with Obesity
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Authors: Michalakis, K., Mintziori, G., Kaprara, A., Tarlatzis, B. C., & Goulis, D. G.
Affiliations: Aristotle University of Thessaloniki (GR)
Corresponding author: Goulis, Dimitrios G.
ORCID: Michalakis, Konstantinos
Mintziori, Gesthimani
Kaprara, Athina
Tarlatzis, Basil C.
Goulis, Dimitrios G.
Venue: Metabolism
Publisher: Elsevier BV
Published: 2013-04
Volume: 62
Issue: 4
Pages: 457-478
ISSN: 0026-0495 (ISSN-L)
DOI: 10.1016/j.metabol.2012.08.012
OpenAlex: W2115987699
Cited by: 321
References: 272
Citations by year: 2026: 10 · 2025: 15 · 2024: 19 · 2023: 16 · 2022: 18 · 2021: 21 · 2020: 29 · 2019: 30 · 2018: 23 · 2017: 26 · 2016: 27 · 2015: 35 · 2014: 38 · 2013: 14
FWCI: 3.76
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Metabolism (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
Keywords: obesity, metabolic syndrome, reproductive axis, hypothalamic-pituitary-gonadal axis, energy balance, puberty, precocious puberty, male infertility, secondary hypogonadism, oxidative stress, spermatogenesis, leptin, adiponectin, resistin, ghrelin, sex hormone replacement therapy, bariatric surgery, lifestyle modification
MeSH terms: Adult, Female, Fertility, Gastrointestinal Hormones, Humans, Infertility, Life Style, Male, Obesity, Pregnancy, Reproduction, Gonadal Steroid Hormones, Metabolic Syndrome, Bariatric Surgery

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The complex interaction between obesity, metabolic syndrome and reproductive axis: A narrative review

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