ORIGINAL ARTICLE
Ahead of print publication  

Association of handgrip strength with semen characteristics: a study with repeated measurements among healthy Chinese men


1 Department of Epidemiology and Biostatistics, Ministry of Education Key Laboratory of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430000, China
2 Center for Reproductive Medicine, Department of Obstetrics and Gynaecology, Xiangyang No.1 People's Hospital, Hubei University of Medicine, Xiangyang 441100, China
3 Center for Reproductive Medicine, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430000, China
4 Hubei Province Human Sperm Bank, Wuhan 430000, China
5 Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA

Date of Submission05-Oct-2021
Date of Acceptance07-Feb-2022
Date of Web Publication05-Apr-2022

Correspondence Address:
An Pan,
Department of Epidemiology and Biostatistics, Ministry of Education Key Laboratory of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430000
China
Yi-Xin Wang,
Department of Epidemiology and Biostatistics, Ministry of Education Key Laboratory of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430000, China; Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA


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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/aja20221

PMID: 35381698

  Abstract 


Accumulating epidemiological evidence shows that handgrip strength provides predictive potential in physical, mental, and reproductive health status. However, the associations between handgrip strength and semen characteristics have not been explored. We recruited 1382 eligible men at the Hubei Province Human Sperm Bank (Wuhan, China) who had their handgrip strength measured at recruitment and provided 6458 repeated semen specimens within a 6-month period. Semen characteristics, including semen volume, sperm motility parameters (immotility, nonprogressive motility, and progressive motility), and sperm concentration, were assessed. Mixed-effect models and restricted cubic spline functions were applied to investigate the relationship of handgrip strength with repeated measurements of semen characteristics. After adjusting for confounding factors, the mixed-effect models revealed that handgrip strength was positively associated with semen volume, sperm concentration, progressive motility, total motility, and total count (all P for trend < 0.05). Compared to men in the lowest quartile, those in the highest quartile of handgrip strength had higher semen volume, sperm concentration, progressive motility, total motility, and total count, with measurements of 14.2% (95% confidence interval [CI]: 5.9%–23.2%), 19.5% (95% CI: 7.3%‒33.1%), 9.5% (95% CI: 3.4%‒15.9%), 8.8% (95% CI: 3.2%‒14.6%), and 36.4% (95% CI: 18.9%‒56.5%), respectively. These positive dose-response relationships were further confirmed in restricted cubic splines, where handgrip strength was modeled as a continuous variable. Handgrip strength, as an indicator of muscular function and strength, was positively associated with semen characteristics in a dose-dependent manner.

Keywords: epidemiology; handgrip strength; repeated measurements; semen characteristics


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How to cite this URL:
Sun B, Chen HG, Duan P, Tu ZZ, Chen YJ, Meng TQ, Xiong CL, Wang YX, Pan A. Association of handgrip strength with semen characteristics: a study with repeated measurements among healthy Chinese men. Asian J Androl [Epub ahead of print] [cited 2022 May 21]. Available from: https://www.ajandrology.com/preprintarticle.asp?id=342581


  Introduction Top


Handgrip strength is a feasible and validated marker of muscular function and strength, which makes it attractive for providing valuable information on overall health status for both men and women.[1] Recent studies have also suggested that handgrip strength is an attractive and objective marker of upper extremity strength, which makes it tempting to employ handgrip strength as a screening tool for monitoring and detecting changes in nutritional status, especially among younger adults.[2],[3] Accumulating epidemiological evidence shows that low handgrip strength is associated with greater all-cause mortality and cardiovascular outcomes,[4],[5] diabetes prevalence,[2] cognitive decline,[6] and functional disability,[7] suggesting that lower handgrip strength may have predictive potential for vulnerability to diseases.[8] Furthermore, Atkinson and colleagues revealed a positive association between handgrip strength and self-reported reproductive success.[9] A more recent study conducted among hunter-gatherers showed that male upper extremity strength significantly predicted reproductive success in terms of offspring production.[10] Meanwhile, handgrip strength was strongly related to higher serum testosterone concentrations among 7064 healthy adults from the National Health and Nutrition Examination Survey,[11] suggesting a potential influence on spermatogenesis,[12],[13],[14] given the strong association between testosterone concentrations and semen characteristics.[15],[16] However, the relationship between handgrip strength and semen characteristics remains unclear.

To fill the data gap, we explored the associations between handgrip strength and repeated semen characteristics among 1382 healthy Chinese men screened as potential sperm donors. Our findings will provide more useful information on the utility of a handgrip dynamometer as a potentially useful predictor of human semen characteristics.


  Participants and Methods Top


Study design

A total of 1487 healthy men were recruited from potential sperm donors at the Hubei Province Human Sperm Bank (Wuhan, China) during the period from April 2017 to July 2018, as described previously.[17],[18] The protocol of this study was approved by the Ethics Committee of the Center for Reproductive Medicine, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China (approval No. 2017-01). After providing written informed consent, each participant underwent a physical examination, completed a baseline questionnaire, and provided a semen specimen at enrolment. The questionnaire collected various information regarding demographic characteristics (e.g., age, height, weight, education level, income level, and marital status), lifestyle factors (e.g., abstinence time, and drinking and smoking habits), medical history, and reproductive health conditions (e.g., testis injury, vasectomy, and varicocele).

Participants were required to fulfill the screening standards for inclusion in the current study: (1) had a high school degree or above; (2) were aged between 22 years and 45 years; (3) were in good health without genetic diseases or sexually transmitted diseases (e.g., thalassemia, karyotype abnormalities, hepatitis, human immunodeficiency virus, syphilis, gonorrhea, and chlamydia); and (4) had no occupational exposure. The donors were asked to provide sufficient quantities of semen samples to impregnate five women in 6 months if they met the following donation standard published by the Chinese Ministry of Health: (1) a fresh sperm concentration ≥60 × 106 ml−1, progressive sperm motility ≥60%, and percentage of normal morphology >30%; and (2) a frozen-thaw survival rate ≥60%, postthaw sperm motility ≥40%, and number of motile sperm per vial ≥12 × 106.[19] Men who failed to meet the screening standard were asked to provide additional amounts of semen samples for further screening at 1–15 days, 16–31 days , 32–63 days, and ≥64 days after recruitment. Semen characteristics were evaluated each time the participants provided specimens regardless of whether the semen characteristics met the donation criteria. We excluded 102 men because of genetic diseases or sexually transmitted diseases (e.g., thalassemia, chromosome abnormalities, and human hepatitis B virus infection) and three men due to missing data on handgrip strength, leaving 1382 eligible men for our current analysis.

Semen collection and analyses

After an abstinence time of more than 48 h, the volunteer collected semen specimens into a sterile polyethylene cup by masturbation. After liquefaction at 37°C, semen characteristics, including semen volume, sperm motility parameters (immotility, nonprogressive motility, and progressive motility), and sperm concentration, were assessed according to the World Health Organization laboratory manual,[20] as described previously.[17],[18] Briefly, a weighing method was used to determine semen volume assuming a sperm density of 1.0 g ml−1. After being thoroughly mixed, 10 μl of semen was placed into a sterile Makler chamber (Sefi Medical Instruments, Haifa, Israel) and estimated by an optical microscope (BX53, Olympus Corporation, Tokyo, Japan) to evaluate progressive sperm motility, total motility, and sperm concentration. Then, we calculated total motility (progressive motility + nonprogressive motility) and total sperm count per ejaculate for each sample (sperm concentration × semen volume). The semen sample was analyzed by trained technicians at the Andrology Laboratory of Hubei Province Human Sperm Bank, and the between- and within-day quality control were assessed to ensure variation of less than 10%.[21]

Handgrip strength

Handgrip strength was assessed by professional research staff using a Jamar Plus+ hand dynamometer (Sammons Preston, Warrenville, IL, USA). Before each measurement, the grip span of the device was adjusted to fit the participant's hand size. Handgrip strength was assessed while standing; the device was held with the elbow in full extension and the arm was positioned at the side of the body. Then, the participant was required to squeeze the dynamometer as hard as they could for 3 s. The test was measured twice more at intervals of >30 s, and the value was recorded with a precision of 0.1 kg. If the participant changed their position during the measurement, a new test was performed. Handgrip strength was measured twice for each hand, with intraclass correlation coefficients (ICCs) of 0.86 and 0.87 for left and right handgrip strength, respectively. Because the left and right handgrip measurements were significantly correlated (rspearman = 0.84, P < 0.0001), we used the average values of handgrip strength from both hands in all subsequent analyses.[4],[22] The handgrip measurements were expressed as absolute units (kg).[2],[4]

Statistical analyses

Descriptive analyses were conducted for participants' demographics, lifestyle factors, and semen characteristics according to handgrip strength (kg). The Kruskal–Wallis test or Chi-square tests were applied to assess the differences in demographic characteristics across the quartiles of handgrip strength. Semen volume, sperm concentration, progressive motility, total motility, and total count were transformed by natural logarithmic transformation to normalize the distribution. Then, linear mixed-effects models with a subject-specific random intercept, which provide researchers with powerful and flexible analytical tools for repeated-measures data,[23],[24] were applied to evaluate the relationships of handgrip strength (expressed in quartiles and per standard deviation [s.d.] difference) with repeated measures of semen characteristics. Tests for trends across the quartiles of handgrip strength were evaluated by using a median value within each quartile as a continuous value. Restricted cubic spline functions based on linear mixed-effects models were used to characterize the dose-response relationship between continuous handgrip strength and semen characteristics and visually check the linearity of these associations.[25] Potential confounders were selected a priori and were then retained in the multivariable models if the P value was less than 0.2 in the bivariate analyses in terms of their association with exposure or at least one outcome measure; covariates with a P > 0.15 for all tested semen characteristics were further removed from the final models.[26] Finally, the full models were adjusted for abstinence period (day), body mass index (BMI, kg m−2), age (year), smoking status (never, former, or current), alcohol consumption (never, occasional, former, or current), tea consumption (yes or no), marital status (married, unmarried, or divorced), monthly income (<4000 Chinese Yuan, 4000–8000 Chinese Yuan, or >8000 Chinese Yuan), education level (less than undergraduate, or undergraduate or above), and sampling season (winter, spring, summer, or autumn). For data with missing values (<0.5% for all covariates), missing indicator variables were used in the data analyses.

Stratified analyses were conducted to assess whether the relationships were modified by BMI (underweight [<18.5 kg m−2], normal weight [18.5–23.9 kg m−2], and overweight/obesity [≥24.0 kg m−2])[27] and age (<28 years vs ≥28 years). A cross-product term was added to the final model to evaluate multiplicative interactions.[28] Additionally, several sensitivity analyses were conducted to test the robustness of our results. First, we used handgrip strength relative to body weight (kg kg−1, per s.d. difference) to assess the influence of body size. Second, we used the within-subject average measurements to reflect individual semen characteristics. Third, we assessed the cross-sectional associations between handgrip strength and semen characteristics that were both measured at baseline enrolment. Fourth, we filled out the missing data with median values. Fifth, we separately assessed the associations for the average values of left and right handgrip strength. Finally, to evaluate the potential influence of physical activity and body fat, we additionally adjusted for these two variables by restricting our analysis to 535 men who had complete information on physical activity (evaluated by the long-form International Physical Activity Questionnaire[29]) and body fat percentage (assessed by a bioelectrical impedance analyzer; TBF-400, Tanita, Tokyo, Japan). SAS version 9.4 (SAS Institute, Cary, NC, USA) and R version 3.5.1 (https://www.rproject.org/) were used for all data analyses. P < 0.05 was considered statistically significant.


  Results Top


The demographic characteristics of the study population stratified by quartiles of handgrip strength are presented in [Table 1]. The mean (s.d.) abstinence time, age, and BMI were 6.2 (3.4) days, 28.0 (5.2) years, and 22.8 (3.3) kg m−2, respectively. The majority of the participants were unmarried (66.9%), had less than a bachelor's degree (64.4%), and had a self-reported household income level of ≥4000 Chinese Yuan per month (71.0%). Among the participants, 742 (53.7%) were nonsmokers and 352 (25.5%) did not drink alcohol over the past 3 months. Compared to men in the lowest quartile of handgrip strength, men in the highest quartiles had a greater BMI (23.7 ± 3.2 kg m−2 vs 22.3 ± 3.3 kg m−2) and shorter abstinence time (6.0 ± 3.3 days vs 6.4 ± 3.6 days) and were also more likely to get married (37.6% vs 23.1%). The median (interquartile range [IQR]) within-subject average measurements of semen volume, sperm concentration, progressive motility, total motility, and total count were 2.9 (1.5) ml, 48.3 × 106 (31.9 × 106) ml−1, 57.5% (13.2%), 60.8% (13.2%), and 138.6 × 106 (109.3 × 106), respectively.
Table 1: Demographic characteristics and semen characteristics of participants by quartiles of handgrip strength

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A total of 6458 semen specimens (mean frequency: 4.7) were collected from 1382 men. The association between handgrip strength and repeated semen characteristics is presented in [Table 2]. The crude and fully adjusted mixed-effects models both revealed increasing semen volume, sperm concentration, sperm motility (progressive and total), and total count across the quartiles of handgrip strength (all P for trend < 0.05). In the fully adjusted models, men in the highest versus men in the lowest quartile of handgrip strength had higher semen volume, sperm concentration, progressive sperm motility, total motility, and total count, with measurements of 14.2% (95% confidence interval [CI]: 5.9%–23.2%), 19.5% (95% CI: 7.3%–33.1%), 9.5% (95% CI: 3.4%–15.9%), 8.8% (95% CI: 3.2%–14.6%), and 36.4% (95% CI: 18.9%–56.5%), respectively. The associations remained when handgrip strength was modeled as a continuous variable.
Table 2: Associations between handgrip strength (kg) and repeated semen characteristics (n=6458) based on linear mixed-effects models

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[Figure 1] shows the associations between continuous handgrip strength and semen characteristics based on the restricted cubic spline functions. Consistent with the trend observed in mixed-effect models, handgrip strength was positively associated with semen volume, sperm concentration, progressive motility, total motility, and total count in a monotonical manner. Similar results were observed when we used handgrip strength relative to body weight (kg kg−1) in the mixed-effect models [Supplementary Table 1 [Additional file 1]] and cubic spline analysis [Supplementary Figure 1 [Additional file 2]].
Figure 1: Dose-response relationships of handgrip strength (kg) with repeated semen characteristics based on restricted cubic spline models (n=6458). The reference values (i.e., the gray vertical dotted lines) were set to 10% of handgrip strength. All models were adjusted for age, body mass index, abstinence period, marital status, smoking, drinking, tea consumption, monthly income, education level, and sampling season.

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No evidence of an interaction between handgrip strength and age was determined. However, the associations between handgrip strength and sperm concentration, progressive motility, and total motility were stronger among men who were overweight or obese (BMI ≥24.0 kg m−2; P-interaction = 0.02, 0.001, and 0.001, respectively; [Table 3]. The sensitivity analyses showed that the positive dose-response relationships of handgrip strength with semen volume, sperm concentration, and total count persisted when we replaced the missing data with median values, when we used the within-individual average semen characteristics or baseline measurements [Supplementary Table 2 [Additional file 3]], and when we separately assessed the associations for the average values of left and right handgrip strength [Supplementary Table 3 [Additional file 4]]. These associations were also essentially unchanged when we additionally adjusted for physical activity and body fat percentage after excluding men who did not have complete data for these two variables [Supplementary Table 4 [Additional file 5]], although men in the highest versus those in the lowest quartile of handgrip strength had a greater body fat percentage (16.6% ± 4.9% vs 13.7% ± 5.7%) and higher BMI (24.3 ± 2.8 kg m−2 vs 22.4 ± 3.3 kg m−2; [Supplementary Table 5 [Additional file 6]]).
Table 3: Associations between handgrip strength (kg) and repeated semen characteristics stratified by age and body mass index

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  Discussion Top


Across 1382 potential sperm donors, we found that higher handgrip strength was positively associated with semen volume, sperm concentration, motility, and total count. There was no evidence of an interaction between handgrip strength and age. However, the associations of handgrip strength and progressive sperm motility, total motility, and sperm concentration were stronger among men who were overweight or obese.

To the best of our knowledge, studies focusing on the associations of handgrip strength with semen characteristics are rare. In support of our findings, previous studies have reported that handgrip strength is related to masculine features and serum testosterone concentrations, as well as self-reported reproductive success in men.[9],[14],[30] Testosterone is responsible for spermatogenesis and provides feedback for the hypothalamic-pituitary-gonadal axis;[15] therefore, a positive association between testosterone and sperm motility has also been revealed.[16] In a recent study conducted among 7064 healthy adults from the National Health and Nutrition Examination Survey, Chiu and colleagues found a positive association between grip strength and serum testosterone concentrations[11] that had been strongly associated with total sperm count and concentration.[31] In addition, many studies have indicated that handgrip strength can serve as an indicator of nutritional status.[32],[33] Since muscle morphology and function are affected by undernutrition earlier, alterations in muscle physiology may result in lower handgrip strength.[3] Some sex hormones, such as luteinizing hormone (LH) and follicle-stimulating hormone (FSH), are sensitive to malnutrition, which may impact the onset of spermatogenesis, the development of sexual characteristics, and muscle development.[34]

In our stratified analyses, the associations of handgrip strength with several semen characteristics were stronger among men who were overweight or obese. Compared with leaner men (BMI <24.0 kg m−2), we noted a wider interquartile range of handgrip strength among overweight or obese men (10.4 kg vs 8.7 kg), and more people were in the third and fourth quartiles of handgrip strength (60.6% vs 45.0%). Therefore, the different distribution of handgrip strength across BMI categories may partly explain the different associations in men with different BMI. Therefore, we further employed handgrip strength relative to body weight to reduce the influence of body size. While the positive trends persisted robustly, we did not observe any evidence of an interaction between handgrip strength relative to body weight and BMI. Additionally, some previous studies found that BMI was positively associated with muscle strength, and people with higher BMI tended to have a greater performance on handgrip strength tests.[35],[36],[37] Moreover, overweight or obesity has been associated with increased fat mass[38] and reduced physical activity, which might, in turn, affect semen characteristics.[39] Previous epidemiological studies have reported a positive association of physical activity with semen characteristics,[40],[41],[42] as well as an inverse relationship of body composition with sperm concentration and volume.[43],[44] Consistent with previous studies, our data showed that greater handgrip strength was associated with higher BMI and a higher percentage of body fat, but there was no difference in physical activity across the quartiles of handgrip strength. After further adjusting for body fat percentage and physical activity in our mixed-effects models, the positive dose-response relationships of handgrip strength with progressive sperm motility, semen volume, and total count remained robust. Moreover, we found no evidence of an interaction between handgrip strength and age, which may be partly explained by the fact that our recruited individuals were mostly young adults (72.5% were less than 30 years old).

The strengths of this study included the large number of subjects, repeat-measured semen characteristics at multiple time points, and a relatively homogeneous population (healthy men aged 22–45 years) that reduced potential residual confounders. In addition, we enrolled healthy men from a sperm bank who were more representative than previous study participants enrolled from fertility centers and clinics. The present study also had some limitations. First, handgrip strength was measured at a single time point at recruitment. However, we measured the handgrip strength for both hands twice, and the average value of the two hands was used for analysis, which could reduce the potential measurement error. In addition, we deemed that handgrip strength may not be greatly changed in a short time period (6-month follow-up in the current study) if the individual maintained his lifestyle, particularly physical activity and training. Second, sex hormones (e.g., testosterone, LH, and FSH) were not measured in the current study, although previous studies revealed that testosterone was associated with not only semen characteristics,[31],[45] but also handgrip strength.[11],[46] However, the potential mechanisms between handgrip strength and semen characteristics need to be demonstrated in further studies. Third, our recruited participants were typically healthy and young (all aged between 22 years and 45 years), and our study results should be extrapolated with caution to other age groups or those with physical diseases. Fourth, given that our study had a cross-sectional design, it did not confirm any causal relationship of handgrip strength with semen characteristics. However, handgrip strength is strongly elated to limb strength and provides an objective index of overall muscle strength,[47] which can benefit from healthy lifestyle habits[48] (e.g., regular physical exercise and a healthy diet). Previous studies have demonstrated that people who have less sedentary time and are more physically active have a higher handgrip strength.[49],[50] Finally, residual confounding cannot be fully ruled out.


  Conclusions Top


In conclusion, our repeated measurements study found that greater handgrip strength was associated with higher semen volume, sperm motility, sperm concentration, and total count in a dose-dependent manner. Our findings suggest that handgrip strength, as an objective, noninvasive marker of muscle strength, may therefore provide more useful information on the utility of a handgrip dynamometer as a potentially useful predictor of human semen characteristics. Further studies are needed to confirm our novel findings and explore the precise mechanisms.


  Author Contributions Top


All authors fulfill the criteria for authorship. TQM, CLX, YXW, and AP participated in the study design and conception. BS, HGC, PD, ZZT, and YJC were responsible for data collection and data management. BS drafted the manuscript and YXW and AP reviewed and revised the manuscript. All authors read and approved the final manuscript.


  Competing Interests Top


All authors declared no competing interests.


  Acknowledgments Top


This study was supported by the National Natural Science Foundation of China (No. 81903281), the National Postdoctoral Program for Innovative Talents (No. BX201700087), and the Health Commission of Hubei Province Scientific Research Project (No. WJ2019H270).

Supplementary Information is linked to the online version of the paper on the Asian Journal of Andrology website.

 
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