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Male Infertility and Risk of Nonmalignant Chronic Diseases: a Systematic Review of the Epidemiological Evidence

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Male Infertility and Risk of Nonmalignant Chronic Diseases: a Systematic Review of the Epidemiological Evidence 282 Male Infertility and Risk of Nonmalignant Chronic Diseases: A Systematic Review of the Epidemiological Evidence Clara Helene Glazer, MD1 Jens Peter Bonde, MD, DMSc, PhD1 Michael L. Eisenberg, MD2 Aleksander Giwercman, MD, DMSc, PhD3 Katia Keglberg Hærvig, MSc1 Susie Rimborg4 Ditte Vassard, MSc5 Anja Pinborg, MD, DMSc, PhD6 Lone Schmidt, MD, DMSc, PhD5 Elvira Vaclavik Bräuner, PhD1,7 1 Department of Occupational and Environmental Medicine, Address for correspondence Clara Helene Glazer, MD, Department of Bispebjerg University Hospital, Copenhagen NV, Denmark Occupational and Environmental Medicine, Bispebjerg University 2 Departments of Urology and Obstetrics/Gynecology, Stanford Hospital, Copenhagen NV, Denmark University School of Medicine, Stanford, California (e-mail: [email protected]). 3 Department of Translational Medicine, Molecular Reproductive Medicine, Lund University, Lund, Sweden 4 Faculty Library of Natural and Health Sciences, University of Copenhagen, Copenhagen K, Denmark 5 Department of Public Health, University of Copenhagen, Copenhagen, Denmark 6 Department of Obstetrics/Gynaecology, Copenhagen University Hospital, Hvidovre, Denmark 7 Mental Health Center Ballerup, Ballerup, Denmark Semin Reprod Med 2017;35:282–290 Abstract The association between male infertility and increased risk of certain cancers is well studied. Less is known about the long-term risk of nonmalignant diseases in men with decreased fertility. A systemic literature review was performed on the epidemiologic evidence of male infertility as a precursor for increased risk of diabetes, cardiovascular diseases, and all-cause mortality. PubMed and Embase were searched from January 1, 1980, to September 1, 2016, to identify epidemiological studies reporting associations between male infertility and the outcomes of interest. Animal studies, case reports, reviews, studies not providing an accurate reference group, and studies including Downloaded by: Stanford University. Copyrighted material. infertility due to vasectomy or malignancy were excluded. The literature search resulted in 2,485 references among which we identified seven articles fulfilling the eligibility criteria. Of these, four articles were prospective (three on risk of mortality, Keywords one on risk of chronic diseases) and three were cross-sectional relating male infertility ► male infertility to the Charlson Comorbidity Index. The current epidemiological evidence is compatible ► comorbidity with an association between male infertility and risk of chronic disease and mortality, ► mortality but the small number of prospective studies and insufficient adjustment of confoun- ► chronic diseases ders preclude strong statements about male infertility as precursor of these outcomes. Issue Theme Fertility Status and Overall Copyright © 2017 by Thieme Medical DOI https://doi.org/ Health; Guest Editor, Margareta D. Publishers, Inc., 333 Seventh Avenue, 10.1055/s-0037-1603568. Pisarska, MD New York, NY 10001, USA. ISSN 1526-8004. Tel: +1(212) 584-4662. Male Infertility and Risk of Nonmalignant Chronic Diseases Glazer et al. 283 In recent years, there has been an increasing interest in the not subjects of regular health screening programs; therefore, association between male infertility and future health, espe- the contact with the health care system as part of infertility cially the development of chronic diseases and mortality. workup may represent a golden opportunity to identify Furthermore, emerging evidence suggests that a man’s general subjects being at increased risk of long-term morbidity and reproductive health is closely intertwined.1 Although the and mortality and to offer them proper preventive measures. link between male infertility and testicular cancer is well During the past decade, the association between a man’s established, recent studies have shown that abnormal semen reproductive and general health has, therefore, received parameters may also be linked to nonmalignant diseases such increased attention in Europe and the United States. But as diabetes and ischemic heart disease.2,3 It has been hypothe- despite this, the association remains unclear and there is a sized that shared genetic pathways including hormones as need for a systematic assessment of this evidence. The well as environment and lifestyle factors possibly acting in objective of this review was to systematically identify and utero could play an important role.4,5 Furthermore, studies evaluate the existing epidemiological evidence linking male have suggested that semen quality may serve as a biological infertility to subsequent risk of morbidity and mortality. marker for future male health.6 The latter representing results from large epidemiological studies in Europe and the United Methods States which have found an association between poor semen – quality and mortality.6 8 We reviewed the literature according to the MOOSE guide- Infertility is a disease of the reproductive system defined as lines for systematic reviews of observational studies29 with thefailure to achieve a clinical pregnancyafter at least 1 year of methodology adapted from Bonde et al.30 regular unprotected sexual intercourse.9 The lifetime preva- lence of infertility is between 16 and 25%, where male factor Protocol and Registration etiology is identified in 30 to 50% of the cases.10,11 Male A review protocol has been registered at PROSPERO.org with infertility is often associated with semen abnormalities and registration number CRD42016047463, prior initiation of a semen analysis is used as a measure of male fecundity.12 A the review process on September 9, 2016, with amendments conventional semen analysis includes sperm count, motility, regarding inclusion of cross-sectional studies on October 15, and morphology and is today routine care for diagnosis of male 2016. All authors approved the final version of this protocol. infertility. Determinants of sperm quality and other semen characteristics include age, onset of puberty, body mass, stress, Eligibility Criteria and lifestyle conditions such as smoking and alcohol, but wide We conducted a systematic search of peer-reviewed original intra-variability in semen quality is also observed in the same articles in English published between January 1, 1980, and – men.13 17 Decreasing trends in semen quality have been September 1, 2016, to identify articles providing data on the reported over the past decades, but the evidence is still association between male infertility and the risk of the two – debated.18 20 Despite intensifying research on male reproduc- out of three major nonmalignant chronic conditions accord- tive health, still much is unknown as no clear explanation of ing to WHO (diabetes and cardiovascular diseases) and the underlying causes of male infertility is identified in at least all-cause mortality. The complete search specification is 30 to 50% of cases.10 available from the corresponding author. According to the World Health Organization (WHO), the Eligibility criteria for inclusion in the systematic review Downloaded by: Stanford University. Copyrighted material. three main nonmalignant chronic diseases include diabetes, were as follows: cardiovascular disease, and respiratory disease.21 Cardiovas- cular diseases include a broad group of diseases affecting the 1. Exposure: A population (cohort or case–control study) of heart and blood vessels and are the leading cause of death infertile men where the fertility diagnosis precedes the globally.22 Diabetes is a group of metabolic diseases character- outcome of interest (cf. point 2). According to the amend- ized by high blood sugar levels, with increasing trends reported ments in PROSPERO protocol, we also included cross- globally. Infertile men may have lower levels of testosterone,23 sectional studies relating infertility to outcomes of inter- which has previously been linked to risk of cardiovascular est (cf. point 2), as they supported the mechanistic disease, diabetes, and mortality.24,25 Chronic respiratory dis- relationships we try to assess using the included prospec- eases include diseases of the airway and lungs but are excluded tive studies. from this review as the pathogenic pathways connecting to 2. Outcomes: reproduction are uncertain.26 a. Diabetes: Type 1 and type 2 diabetes according to the Since the introduction of in vitro fertilization (IVF) with International Classification of Diseases (ICD). These intracytoplasmic sperm injection (ICSI) in 1992,27 even men were defined as ICD8 249, 250, and ICD10 E10, E11, with severe fertility problems are able to become biological E13, E14, or by using self-reported questionnaires. fathers. Thus, in many cases, the investigation of the male b. Cardiovascular diseases: Hypertensive disease, is- partner includes only semen analysis without further chemic heart disease, pulmonary disease, and cerebro- investigation. This is a source of concern, as an underlying vascular diseases definedasICD8400–404, 410–414, medical pathology may be the cause of the infertility linking 420–429, and ICD10 I10–I15, I20–I26, I63–65, I70, or this to increased risk of disease or mortality in later life.28 It using self-reported questionnaires. should be kept in mind that, in contrast to women, men are c. All-cause mortality provided by death records. Seminars in Reproductive Medicine Vol. 35 No. 3/2017 284 Male Infertility and Risk of Nonmalignant Chronic Diseases Glazer et al. We included epidemiological studies where the exposure and testosterone deficiency leading to obesity
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