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An exploration of the association between male body mass index and semen quality

Published:September 07, 2011DOI:https://doi.org/10.1016/j.rbmo.2011.07.018

      Abstract

      Obesity is becoming a serious problem, especially in industrialized societies. This study was designed to explore the association between body mass index (BMI) and semen quality. Semen analysis and demographic data were collected from male partners of couples undergoing fertility investigations in a referral fertility centre. Men were classified into groups according to their BMI (A, <18.5; B, 18.5–24.99; C, 25–29.99; D, ⩾30 kg/m2). Data from 2035 men were analysed using logistic regression. There were 18, 839, 909 and 269 men in groups A, B, C and D, respectively. Taking group B as the reference, adjusted odds ratios (95% CI) for groups A, C and D for semen volume <2 ml were 1.57 (0.49–5.01), 1.06 (0.82–1.38) and 1.69 (1.20–2.38), respectively; for sperm morphology <15%, 1.44 (0.45–4.61), 1.07 (0.86–1.33) and 1.50 (1.06–2.09); for sperm concentration <20 million/ml, 0.46 (0.10–2.07), 1.03 (0.82–1.31) and 1.00 (0.72–1.41); and for motility <50%, 2.62 (0.73–9.45), 0.96 (0.78–1.18) and 0.75 (0.56–1.01). In conclusion, obese men are more likely to have lower semen volume and fewer morphologically normal spermatozoa than men with normal BMI.
      Obesity is becoming a serious problem, especially in industrialized societies. We designed this study to explore the association between body weight in proportion to height, in men, as expressed by the body mass index (BMI) and semen quality. Semen analysis and demographic data were collected from male partners of couples undergoing fertility investigations in a referral fertility centre. Men were classified into groups according to their BMI: A, <18.5, underweight; B, 18.5–24.99, normal weight; C, 25–29.99, overweight; and D, 330 kg/m2, obese. Data from 2,035 men were analysed. There were 18, 839, 909 and 269 men in groups A, B, C and D, respectively. Compared with men from group B, normal weight, and taking into account other factors besides BMI that may affect semen quality in the analysis, the adjusted odds ratios (95% CI) for groups A, C and D to have a semen volume <2 ml were 1.57 (0.49–5.01), 1.06 (0.82–1.38) and 1.69 (1.20–2.38), respectively, for sperm morphology <15%, 1.44 (0.45–4.61), 1.07 (0.86–1.33) and 1.50 (1.06–2.09), for sperm concentration <20 million /ml, 0.46 (0.10–2.07), 1.03 (0.82–1.31) and 1.00 (0.72–1.41) and for motility <50%, 2.62 (0.73–9.45), 0.96 (0.78–1.18) and 0.75 (0.56–1.01). In conclusion, obese men are more likely to have lower semen volume and fewer morphologically normal spermatozoa than men with normal BMI.

      Keywords

      Introduction

      Obesity is recognized as a serious problem in the developed world and is conventionally categorized on the basis of body mass index (BMI). Values between 18.5 and 24.99 kg/m2 are considered to be normal; individuals with BMI ⩾25 kg/m2 are considered to be overweight, while those with BMI ⩾30 kg/m2 are considered to be obese. Those with a BMI <18.5 kg/m2 are considered to be underweight (). There has been a marked increase in the proportion of men who are obese in England from 13% in 1993 to 24% in 2008 (

      The NHS Information Centre, Lifestyles Statistics, 2010. Statistics on obesity, physical activity and diet, England.

      ). In Scotland, the Scottish Health Survey in 2003 indicated that two-thirds of men (65%) were either overweight or obese (

      The Scottish Executive, 2005. The Scottish Health Survey, 2003.

      ). Obesity is known to be a risk factor for reproductive problems in women, including ovulatory dysfunction (
      • Balen A.H.
      • Anderson R.A.
      • Policy and Practice Committee of the, B.F.S.
      Impact of obesity on female reproductive health: British Fertility Society, Policy and Practice Guidelines.
      ). Relatively few studies have explored the association between obesity and male fertility.
      In a cross-sectional study on Danish young men,
      • Jensen T.K.
      • Andersson A.M.
      • Jorgensen N.
      • Andersen A.G.
      • Carlsen E.
      • Petersen J.H.
      • Skakkebaek N.E.
      Body mass index in relation to semen quality and reproductive hormones among 1, 558 Danish men.
      reported reduced semen quality to be associated with high or low BMI. Since this study, a few studies, the majority of them with small sample sizes, have examined this topic and came up with varying and occasionally conflicting results. While some of these studies reported a negative impact of raised BMI on semen quality (
      • Chavarro J.E.
      • Toth T.L.
      • Wright D.L.
      • Meeker J.D.
      • Hauser R.
      Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic.
      ,
      • Hammoud A.O.
      • Wilde N.
      • Gibson M.
      • Parks A.
      • Carrell D.T.
      • Meikle A.W.
      Male obesity and alteration in sperm parameters.
      ,
      • Hofny E.R.
      • Ali M.E.
      • Abdel-Hafez H.Z.
      • El-Dien Kamal E.
      • Mohamed E.E.
      • Abd El-Azeem H.G.
      • Mostafa T.
      Semen parameters and hormonal profile in obese fertile and infertile males.
      ,
      • Koloszar S.
      • Fejes I.
      • Zavaczki Z.
      • Daru J.
      • Szollosi J.
      • Pal A.
      Effect of body weight on sperm concentration in normozoospermic males.
      ,
      • Kort H.I.
      • Massey J.B.
      • Elsner C.W.
      • Mitchell-Leef D.
      • Shapiro D.B.
      • Witt M.A.
      • Roudebush W.E.
      Impact of body mass index values on sperm quantity and quality.
      ,
      • Magnusdottir E.V.
      • Thorsteinsson T.
      • Thorsteinsdottir S.
      • Heimisdottir M.
      • Olafsdottir K.
      Persistent organochlorines, sedentary occupation, obesity and human male subfertility.
      ,
      • Martini A.C.
      • Tissera A.
      • Estofan D.
      • Molina R.I.
      • Mangeaud A.
      • Fiol de Cuneo M.
      • Ruiz R.D.
      Overweight and seminal quality: a study of 794 patients.
      ,
      • Robeva R.
      • Sestrimska N.
      • Atanasova I.
      • Mekhandzhiev T.
      • Tomova A.
      • Kumanov F.
      [Sperm disorder in males with obesity and metabolic syndrome–pilot study].
      ,
      • Sekhavat L.
      • Reza M.
      The effect of male body mass index on sperm parameters.
      ,
      • Stewart T.M.
      • Liu D.Y.
      • Garrett C.
      • Jorgensen N.
      • Brown E.H.
      • Baker H.W.
      Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output.
      ), others showed no significant association (
      • Duits F.H.
      • Van Wely M.
      • Van Der Veen F.
      • Gianotten J.
      Healthy overweight male patners of subfertile couples should not worry about their semen quality.
      ,
      • Fejes I.
      • Koloszar S.
      • Szollosi J.
      • Zavaczki Z.
      • Pal A.
      Is semen quality affected by male body fat distribution?.
      ,
      • Li Y.
      • Lin H.
      • Ma M.
      • Li L.
      • Cai M.
      • Zhou N.
      • Han X.
      • Bao H.
      • Huang L.
      • Zhu C.
      • Li C.
      • Yang H.
      • Rao Z.
      • Xiang Y.
      • Cui Z.
      • Ao L.
      • Zhou Z.
      • Xiong H.
      • Cao J.
      Semen quality of 1346 healthy men, results from the Chongqing area of southwest China.
      ,
      • Nicopoulou S.C.
      • Alexiou M.
      • Michalakis K.
      • Ilias I.
      • Venaki E.
      • Koukkou E.
      • Mitios G.
      • Billa E.
      • Adamopoulos D.A.
      Body mass index vis-a-vis total sperm count in attendees of a single andrology clinic.
      ,
      • Paasch U.
      • Grunewald S.
      • Kratzch J.
      • Glander H.-J.
      Obesity and age affect male fertility potential.
      ,
      • Pauli E.M.
      • Legro R.S.
      • Demers L.M.
      • Kunselman A.R.
      • Dodson W.C.
      • Lee P.A.
      Diminished paternity and gonadal function with increasing obesity in men.
      ,
      • Ramalu-Hansen C.H.
      • Hansen M.
      • Jensen C.R.
      • Olsen J.
      • Bonde J.P.
      • Thulstrup A.M.
      Semen quality and reproductive hormones according to birthweight and body mass index in childhood and adult life: two decades of follow-up.
      ). Qin even reported that being overweight may improve semen quality (
      • Qin D.-D.
      • Yuan W.
      • Zhou W.-J.
      • Cui Y.-Q.
      • Wu J.-Q.
      • WuGao E.-S.
      Do reproductive hormones explain the association between body mass index and semen quality?.
      ). A recent systematic review reported no evidence of an association between increased BMI and semen parameters. Due to significant clinical heterogeneity in the sample populations and different outcome measures, this review was unable to aggregate data from many of the identified studies in terms of a meta-analysis (
      • Macdonald A.A.
      • Herbison G.P.
      • Showell M.
      • Farquhar C.M.
      The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis.
      ) and highlighted the need for more population based studies ‘with large sample sizes’.
      The aim of this study was to examine the effect of BMI on semen parameters (which is the main tool used to assess the male partner in couples presenting with subfertility), with appropriate adjustments for possible confounders. The Aberdeen Fertility Clinic receives about 500 new infertility referrals per year and clinical details of both partners are entered prospectively into the Fertility Clinic database. Semen analysis is performed routinely for all male partners and data on over 20,000 samples are entered concurrently on the Aberdeen Andrology Laboratory database. This provides an opportunity to link the body mass index of men to their semen analysis parameters.

      Materials and methods

      Ethical approval for this study was obtained from the North of Scotland Research Ethics Service. Data were extracted on all male partners of couples attending for infertility investigations at the Aberdeen Fertility Clinic from 1990 to 2007. Variables extracted included age, height and weight, social deprivation (Scottish Index of Multiple Deprivation (SIMD) http://www.scotland.gov.uk/Topics/Statistics/SIMD), smoking status, alcohol intake, type of infertility (primary or secondary), coital frequency, and having a history of drug abuse, erectile dysfunction or ejaculatory failure.
      Electronic results of semen analyses were linked to the demographic and clinical data on all men (including date of sample, period of abstinence prior to producing the sample, semen volume, sperm concentration, percentage progressive motility and percentage normal morphology). The study excluded men with previous surgery for vasectomy or vasectomy reversal and men with azoospermia.

      Semen analysis

      Each man provided a semen sample by masturbation into a sterile plastic container. Analysis of the semen samples was carried out using both computer-assisted semen analysis (CASA) and manual methods appropriate to each sample. In samples where the sperm concentration was less than 2 million/ml, morphology was not assessed.
      A total of five biomedical scientists carried out all the analyses over the 18-year period of data collection. Quality control comprised of weekly assessment of inter-operator variability for concentration and motility measurements. Variations between operators and between manual and CASA measurements were audited regularly. Quarterly participation in the UK National External Quality Assessment Service (NEQAS) was also used for concentration and morphology (anonymous).

      Statistical analysis

      The 1998 Scottish Health Survey found that 4.5% of adult Scottish males were underweight, 33.3% had a normal weight, 42.6% were overweight and 19.6% were obese (

      Shaw, A., McMunn, A., Field, J., 2000. The Scottish Health Survey.

      ). For a study of 2000 men with BMI distributed in this fashion, and assuming 22% of the men with a normal weight had low sperm concentration (
      • Jensen T.K.
      • Andersson A.M.
      • Jorgensen N.
      • Andersen A.G.
      • Carlsen E.
      • Petersen J.H.
      • Skakkebaek N.E.
      Body mass index in relation to semen quality and reproductive hormones among 1, 558 Danish men.
      ), separate chi-squared tests would have over 80% power to detect an odds ratio of 2.25 compared with the underweight men, an odds ratio of 1.45 compared with the overweight men and an odds ratio of 1.55 compared with the obese men, with a two-sided 5% level of significance.
      Demographic characteristics were compared between men whose BMI data were available and men without this information. Independent t-tests and Mann–Whitney U-tests were used to compare normally and non-normally distributed data, respectively. Chi-squared tests were used for comparisons of categorical data. Men whose BMI data were not available were excluded from the study.
      The study population was divided into four groups depending on their BMI, underweight (<18.5 kg/m2), normal weight (18.5–24.99 kg/m2), overweight (25–29.99 kg/m2) and obese (⩾30 kg/m2). Demographic characteristics and semen parameters were compared across the four BMI groups using chi-squared tests for categorical data, ANOVA tests for normally distributed data and Kruskal–Wallis tests for non-normally distributed data.
      Semen parameters were then classified as abnormal using the 1999 World Health Organization (WHO) criteria as follows: volume <2 ml, concentration <20 million spermatozoa/ml, progressive motility <50% and normal morphology <15% (

      WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction, 1999, fourth ed., Cambridge University Press, <http://www.ukneqas.org.uk/>.

      ). The association between BMI and having abnormal semen parameters was examined using chi-squared tests and logistic regression to adjust for possible confounding factors.
      Missing values of demographic characteristics and semen parameters were excluded from all analyses. The Statistical Package for Social Sciences version 16.0.2 was used for analysis (SPSS, USA).

      Results

      Records on a total number of 5314 men were available. Data on either height or weight were missing for 3279 (62%) men and available for 2035 (38%) men, who formed the study population. Men with known BMI and with missing BMI data were comparable in many aspects, including their age, alcohol consumption and having a history of drug abuse, erectile dysfunction or ejaculatory dysfunction. Men with known BMI data were marginally less socially deprived and included more non-smokers (71% versus 66%).
      Of this study population (men with known BMI), 18 men (1%) were underweight, 839 (41%) had a normal weight, 909 (45%) were overweight and 269 (13%) were obese. The median (interquartile range, IQR) BMI for the entire study population was 25.7 (23.5–27.9) kg/m2.
      Data on age and deprivation category were available for all subjects; smoking data were missing in 22 (1%) cases, alcohol intake in 58 (3%) cases, days of abstinence in 48 (2%) cases, type of infertility in six (0.3%) cases, coital frequency in 769 (38%) cases, erectile dysfunction in 76 (4%) cases, ejaculatory failure in 75 (4%) cases and having a history of drug abuse in 106 (5%) cases. Semen volume data were available for all cases, sperm concentration was missing in 69 (3%) cases, motility was missing in 72 (4%) cases and morphology was not available in 162 (8%) cases.
      As shown in Table 1, age tended to increase with increasing BMI (P < 0.001). Smoking was more common in men with low and normal BMI than those with higher BMI (P = 0.005). Men in the two extreme groups of BMI (underweight and obese) were more socially deprived compared with the other two groups (P = 0.026). Underweight men were less likely to consume alcohol compared with the other three groups (P = 0.039). There were no statistically significant differences between BMI groups in terms of drug abuse, type of infertility (primary or secondary), erectile dysfunction, ejaculatory failure, coital frequency or period of abstinence.
      Table 1Demographic and social characteristics of men in the four body mass index groups.
      Body mass index (kg/m2)P-value
      <18.5 (n = 18)18.5–24.99 (n = 839)25–29.99 (n = 909)30 (n = 269)
      Age (years)30.6 ± 5.632.4 ± 6.033.4 ± 6.034.0 ± 5.8<0.001
      ANOVA.
      Smoking
       None12 (67)553 (67)669 (74)192 (72)0.005
      Chi-squared linear by linear association.
       Moderate6 (33)230 (28)200 (22)67 (25)
       Excessive0 (0)44 (5)32 (4)8 (3)
      Alcohol consumption
       None4 (24)103 (13)96 (11)27 (10)0.039
      Chi-squared linear by linear association.
       Moderate13 (76)690 (86)772 (87)231 (87)
       Excessive0 (0)14 (2)19 (2)8 (3)
      Deprivation category
      Postcodes within a designated geographical data zone were used to determine the Scottish Index of Multiple Deprivation (SIMD) ranking for the whole of Scotland as a relative measure of deprivation. SIMD ranking ranges from 1 to 6505 across the different data zones in Scotland and can be categorized as deciles ranging from 1 (most affluent) to 10 (most deprived).
      6 (3–9)3 (2–6)3 (2–6)4 (2–6)0.026
      Kruskal–Wallis test.
      Drug abuse0 (0)9 (1)6 (1)1 (< 1)NS
      Pearson chi-squared. NS=not statistically significant.
      Primary male infertility14 (78)545 (65)576 (64)170 (64)NS
      Pearson chi-squared. NS=not statistically significant.
      Erectile dysfunction0 (0)12 (2)12 (1)3 (1)NS
      Pearson chi-squared. NS=not statistically significant.
      Ejaculatory dysfunction0 (0)10 (1)13 (1)6 (2)NS
      Pearson chi-squared. NS=not statistically significant.
      Coital frequency/month10 (5–12)10 (8–12)10 (8–12)10 (8–12)NS
      Kruskal–Wallis test.
      Period of abstinence (days)5 (4–6)4 (4–6)4 (4–5)4 (4–5)NS
      Kruskal–Wallis test.
      Values are mean ± standard deviation, n (%) or mean (interquartile range).
      a ANOVA.
      b Chi-squared linear by linear association.
      c Postcodes within a designated geographical data zone were used to determine the Scottish Index of Multiple Deprivation (SIMD) ranking for the whole of Scotland as a relative measure of deprivation. SIMD ranking ranges from 1 to 6505 across the different data zones in Scotland and can be categorized as deciles ranging from 1 (most affluent) to 10 (most deprived).
      d Kruskal–Wallis test.
      e Pearson chi-squared. NS = not statistically significant.
      Analysis of the semen parameter data (Table 2) showed normal sperm morphology to be significantly higher in the normal-weight and underweight groups compared with the overweight and obese groups (P = 0.001), which remained significant after adjusting for age, abstinence period and social deprivation. Sperm concentration, total sperm count and progressive motility were not associated with BMI. The semen volume, and the total number of morphologically normal and progressively motile spermatozoa per ejaculate (obtained by combining all semen analysis parameters) also showed no association with BMI.
      Table 2Semen analysis results of men in the four body mass index groups.
      Body mass index (kg/m2)
      <18.5 (n = 18)18.5–24.99 (n = 839)25–29.99 (n =909)⩾30 (n =269)
      Semen volume (ml)3.2 ± 1.93.5 ± 1.83.5 ± 1.83.2 ± 1.7
      Sperm concentration (millions/ml)45.9 (31.9–98.5)47.9 (22.0–84.3)47.0 (21.0–82.0)50.8 (21.3–83.0)
      Total sperm count (millions)147.2 (70.8–266.3)144.0 (61.1–290.8)153.0 (58.8–273.4)162.7 (48.9–259.8)
      Motile sperm (%)40.8 (26.0–51.0)45.0 (29.4–59.0)45.4 (27.6–59.0)47.0 (27.0–61.0)
      Morphologically normal spermatozoa (%)
      Crude P=0.001; after adjustment for age, abstinence period, and social deprivation, P=0.023. Adjusted P-values were calculated using multinomial logistic regression.
      11.0 (4.0–34.5)9.0 (3.0–20.0)8.0 (3.0–20.0)6.0 (3.0–14.0)
      Motile concentration (millions/ml)17.3 (9.1–47.3)20.3 (5.9–44.6)20.2 (5.3–44.4)22.2 (4.4–45.6)
      Motile normal concentration (millions/ml)1.2 (0.3–7.4)1.4 (0.2–6.1)1.3 (0.2–6.0)1.0 (0.1–4.4)
      Total normal motile sperm (millions)3.4 (0.6–26.2)4.5 (0.6–20.1)3.9 (0.6–19.1)2.7 (0.3–12.9)
      Values are mean ± standard deviation or mean (interquartile range). Semen volume was analysed by ANOVA and all other parameters by Kruskal–Wallis test.
      a Crude P = 0.001; after adjustment for age, abstinence period, and social deprivation, P = 0.023. Adjusted P-values were calculated using multinomial logistic regression.
      When applying the WHO criteria of normality for semen parameters as the cut offs, there was a significant association between BMI and abnormal semen volume after adjusting for age, smoking habits, alcohol intake, deprivation and period of abstinence (Table 3). Obese men were more likely to have low volume (<2 ml) compared with men with a normal weight, with an adjusted odds ratio of 1.69 (95% CI 1.20–2.38). There was a statistically-significant association between BMI and having normal sperm morphology <15% (P = 0.006), which remained statistically significant after adjustment for potential confounders (adjusted P = 0.040); when compared with the normal-weight group, obese men had a lower proportion of morphologically normal spermatozoa. There was no evidence of any association between having low sperm concentration or sperm motility and BMI.
      Table 3Association between abnormal semen parameters and body mass index.
      Parameter and BMI group (kg/m2)n/N (%)CrudeAdjusted
      Logistic regression used to adjust for age, smoking, alcohol intake, abstinence period and social deprivation.
      Odds ratio (95% CI)
      Logistic regression.
      P-valueOdds ratio (95% CI)P-value
      Semen volume <2 ml
       <18.54/18 (22)1.41 (0.46–4.36)0.0251.57 (0.49–5.01)0.014
       18.5–24.99141/839 (17)ReferenceReference
       25–29.99155/909 (17)1.02 (0.79–1.31)1.06 (0.82–1.38)
       ⩾3066/269 (25)1.61 (1.16–2.24)1.69 (1.20–2.38)
      Sperm concentration <20 million/ml
       <18.52/17 (12)0.45 (0.10–1.98)NS0.46 (0.10–2.07)NS
       18.5–24.99184/802 (23)ReferenceReference
       25–29.99208/883 (24)1.04 (0.83–1.30)1.03 (0.82–1.31)
       ⩾3062/264 (23)1.03 (0.74–1.43)1.00 (0.72–1.41)
      Sperm motility <50%
       <18.513/17 (76)2.24 (0.73–6.94)NS2.62 (0.73–9.45)NS
       18.5–24.99478/808 (59)ReferenceReference
       25–29.99513/879 (58)0.97 (0.80–1.8)0.96 (0.78–1.18)
       ⩾30141/259 (54)0.83 (0.62–1.09)0.75 (0.56–1.01)
      Normal sperm morphology <15%
       <18.511/17 (65)1.04 (0.38–2.83)0.0061.44 (0.45–4.61)0.040
       18.5–24.99494/773 (64)ReferenceReference
       25–29.99566/838 (68)1.8 (0.96–1.44)1.07 (0.86–1.33)
       ⩾30186/245 (76)1.78 (1.28–2.47)1.50 (1.06–2.09)
      CI = confidence interval; NS = not statistically significant.
      a Logistic regression.
      b Logistic regression used to adjust for age, smoking, alcohol intake, abstinence period and social deprivation.

      Discussion

      Principal findings

      These results suggest a significant association between male body mass index and abnormally low semen volume and normal sperm morphology. Obese men were more likely to have low semen volume and abnormally low sperm morphology compared with normal-weight men. The study found no evidence of an association between sperm concentration or motility and BMI.

      Strengths and weaknesses

      As far as is known, this is the largest single study investigating the association between BMI and semen parameters. The study population comprised of men from different age groups and included a large number of overweight and obese men, reflecting the current BMI trends in industrialized societies, and the study could adjust for many potential confounders. This is an important strength, given the known difficulties associated with adjusting for confounders in meta-analyses of observational data from a number of smaller studies. This study was able to report results in underweight men as well, in contrast to the majority of the published studies.
      As a study based on electronic records, it has a number of limitations with regards to the availability of some data. The study was obliged to exclude a large proportion of men due to missing BMI data. Comparison of men with and without BMI details showed that they were similar in many respects and the study adjusted for the factors found to be different between the two groups. As the study population attended a fertility centre, these results may not reflect semen quality in the general population and should be interpreted with caution.
      Since 1980, the WHO has published five editions of the guide to semen analysis, each one sets slightly different cut-off points of what to call as ‘normal’ when assessing the different semen analysis parameters. Clearly the concept of normality is a relative one. Setting cut-off points is required for clinical guidance to clinicians. However, as far as fertility is concerned, these are not cut-off points to separate fertile from infertile men. The main reason why cut offs have changed with time is the change of the semen quality in men observed over the last few decades as they are drawn from centiles of the parameter in the general population, Another reason in relation to the morphology parameter is adopting more strict criteria for sperm morphological assessment. This is why the cut offs have changed with time and may continue to change in the future. This study chose to use the cut-off points published in the fourth edition of this guide, as this edition covered most of this study’s sample population. However, the conclusions remain the same if the cut-off points in the 1992 or the 2010 editions of this manual are adopted.
      Interpretation of the results of sperm morphology is difficult due to inter-observer variability. All of the biomedical scientists involved in the semen analyses were participating in the UK NEQAS quality-assessment service, to ensure the validity of the results as assessed by an external body.

      Results in relation to other studies

      • Jensen T.K.
      • Andersson A.M.
      • Jorgensen N.
      • Andersen A.G.
      • Carlsen E.
      • Petersen J.H.
      • Skakkebaek N.E.
      Body mass index in relation to semen quality and reproductive hormones among 1, 558 Danish men.
      have reported a significant association between sperm concentration and BMI, but no association with the rest of the semen parameters. Their study included young men and the overweight and obese individuals were under-represented when compared with the general population.
      • Martini A.C.
      • Tissera A.
      • Estofan D.
      • Molina R.I.
      • Mangeaud A.
      • Fiol de Cuneo M.
      • Ruiz R.D.
      Overweight and seminal quality: a study of 794 patients.
      has reported sperm motility to be the only parameter associated with obesity. Both sperm concentration and motility were found to be associated with BMI in a study of 390 patients (
      • Hammoud A.O.
      • Wilde N.
      • Gibson M.
      • Parks A.
      • Carrell D.T.
      • Meikle A.W.
      Male obesity and alteration in sperm parameters.
      ).
      • Stewart T.M.
      • Liu D.Y.
      • Garrett C.
      • Jorgensen N.
      • Brown E.H.
      • Baker H.W.
      Associations between andrological measures, hormones and semen quality in fertile Australian men: inverse relationship between obesity and sperm output.
      linked obesity to reduced total sperm number in the ejaculate in a study on 225 men and
      • Chavarro J.E.
      • Toth T.L.
      • Wright D.L.
      • Meeker J.D.
      • Hauser R.
      Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic.
      reported a lower semen volume in obese men.
      • Aggerholm A.S.
      • Thulstrup A.M.
      • Toft G.
      • Ramlau-Hansen C.H.
      • Bonde J.P.
      Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile?.
      combined five separate studies and failed to show any statistically significant differences in semen parameters between the different BMI groups, but morphology was not included in this study.
      • Duits F.H.
      • Van Wely M.
      • Van Der Veen F.
      • Gianotten J.
      Healthy overweight male patners of subfertile couples should not worry about their semen quality.
      ,
      • Li Y.
      • Lin H.
      • Ma M.
      • Li L.
      • Cai M.
      • Zhou N.
      • Han X.
      • Bao H.
      • Huang L.
      • Zhu C.
      • Li C.
      • Yang H.
      • Rao Z.
      • Xiang Y.
      • Cui Z.
      • Ao L.
      • Zhou Z.
      • Xiong H.
      • Cao J.
      Semen quality of 1346 healthy men, results from the Chongqing area of southwest China.
      ,
      • Paasch U.
      • Grunewald S.
      • Kratzch J.
      • Glander H.-J.
      Obesity and age affect male fertility potential.
      and
      • Ramalu-Hansen C.H.
      • Hansen M.
      • Jensen C.R.
      • Olsen J.
      • Bonde J.P.
      • Thulstrup A.M.
      Semen quality and reproductive hormones according to birthweight and body mass index in childhood and adult life: two decades of follow-up.
      all separately could not demonstrate any association between BMI and any of the semen analysis parameters. On the other hand,
      • Qin D.-D.
      • Yuan W.
      • Zhou W.-J.
      • Cui Y.-Q.
      • Wu J.-Q.
      • WuGao E.-S.
      Do reproductive hormones explain the association between body mass index and semen quality?.
      suggested that being overweight may be protective against low sperm concentration and total sperm count; however, only 1.7% (17 men) in this study had BMI >30 kg/m2.
      A recent systematic review combined data from five studies and meta-analysis was performed for the sperm concentration and the total sperm-count parameters. It found no evidence of a relationship between BMI and these two parameters (
      • Macdonald A.A.
      • Herbison G.P.
      • Showell M.
      • Farquhar C.M.
      The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis.
      ). The current study included men of all age groups and had a large proportion of overweight and obese men, which is more representative of the general population current trends. It had a larger sample size than any of the other individual studies, but did not confirm the association between BMI and sperm concentration. However, here is demonstrated an association between BMI with semen volume and morphology; the latter has rarely been reported in any of the previous studies.

      Meaning of the results and implications for clinicians

      Conventional semen analysis is a rough tool in terms of assessing male fertility. As such, the current results may not be able to provide clear answers regarding the potential relationship between BMI and male fertility.
      These results regarding the association between BMI and sperm morphology have rarely been reported in previous studies. Despite the difficulty in standardizing morphology reporting, this parameter has been reported to have the greatest discriminatory power in distinguishing between fertile and infertile men (
      • Guzick D.S.
      • Overstreet J.W.
      • Factor-Litvak P.
      • Brazil C.K.
      • Nakajima S.T.
      • Coutifaris C.
      • Carson S.A.
      • Cisneros P.
      • Steinkampf M.P.
      • Hill J.A.
      • Xu D.
      • Vogel D.L.
      • National Co-operative Reproductive Medicine, N.
      Sperm morphology, motility, and concentration in fertile and infertile men.
      ).
      Reasons for the association between BMI and semen quality remain speculative. Possible explanations include altered concentrations of circulating sex steroids in obese men (increased concentrations of oestrogens and decreased concentrations of total testosterone and FSH) (
      • Fejes I.
      • Koloszar S.
      • Zavaczki Z.
      • Daru J.
      • Szollosi J.
      • Pal A.
      Effect of body weight on testosterone/estradiol ratio in oligozoospermic patients.
      ,
      • Glass A.R.
      • Swerdloff R.S.
      • Bray G.A.
      • Dahms W.T.
      • Atkinson R.L.
      Low serum testosterone and sex-hormone-binding-globulin in massively obese men.
      ,
      • Glass A.R.
      • Swerdloff R.S.
      • Bray G.A.
      • Dahms W.T.
      • Atkinson R.L.
      Low serum testosterone and sex-hormone-binding-globulin in massively obese men.
      ,
      • Schneider G.
      • Kirschner M.A.
      • Berkowitz R.
      • Ertel N.H.
      Increased estrogen production in obese men.
      ,
      • Zumoff B.
      • Strain G.W.
      • Miller L.K.
      • Rosner W.
      • Senie R.
      • Seres D.S.
      • Rosenfeld R.S.
      Plasma free and non-sex-hormone-binding-globulin-bound testosterone are decreased in obese men in proportion to their degree of obesity.
      ), (
      • Jensen T.K.
      • Andersson A.M.
      • Jorgensen N.
      • Andersen A.G.
      • Carlsen E.
      • Petersen J.H.
      • Skakkebaek N.E.
      Body mass index in relation to semen quality and reproductive hormones among 1, 558 Danish men.
      ,
      • Pauli E.M.
      • Legro R.S.
      • Demers L.M.
      • Kunselman A.R.
      • Dodson W.C.
      • Lee P.A.
      Diminished paternity and gonadal function with increasing obesity in men.
      ,
      • Strain G.W.
      • Zumoff B.
      • Kream J.
      Mild hypogonadotropic hypogonadism in obese men.
      ). Increased scrotal temperature as a result of increased suprapubic, thigh or scrotal fat (
      • El-Sibai O.
      • Fouad M.
      Feminizing hormone in scrotal lipomatosis.
      ,
      • Koskelo R.
      • Zaproudina N.
      • Vuorikari K.
      High scrotal temperatures and chairs in the pathophysiology of poor semen quality.
      ,
      • Shafik A.
      • Olfat S.
      Scrotal lipomatosis.
      ) is a second possible mechanism of decreasing semen quality in these subjects.

      Future research

      Further research should include large studies to assess the relationship between male BMI in the general population and male fertility (achieving a pregnancy or a live birth). There is also a need for evaluative work on the effect of optimizing BMI on semen quality and fertility.

      Conclusion

      Obese men are more likely to have abnormally low semen volume and fewer morphologically normal spermatozoa. Whether these associations are reflected in reduced male fertility remains unproven.

      Acknowledgements

      The authors are grateful for the assistance of Valerie Angus, of the Data Management Team at the University of Aberdeen, in generating the original datasets from the Aberdeen Fertility Centre and the Andrology Laboratory Databases.

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