Journal of Occupational & Environmental Medicine:
ORIGINAL ARTICLES: CME Article #1
Potential Association Between Male Infertility and Occupational Psychological Stress
Sheiner, Einat K. MD, MSc; Sheiner, Eyal MD; Carel, Refael MD; Potashnik, Gad MD; Shoham-Vardi, Ilana PhD
From the Department of Occupational Medicine, (Dr E. K. Sheiner, Dr Carel); Department of Obstetrics and Gynecology Fertility & In-Vitro Fertilization Unit (Dr E. Sheiner, Dr Potashnik); and Epidemiology and Health Services Evaluation (Dr Shoham-Vardi), Faculty of Health Sciences, Soroka University Medical Center, Ben-Gurion University of the Negev, Beer-Sheva, Israel.
Address correspondence to: Eyal Sheiner, MD, Department of Obstetrics and Gynecology Soroka University Medical Center P.O. Box 151 Beer Sheva 84101, Israel; e-mail: firstname.lastname@example.org.
The work was performed as part of the requirements for Einat K. Sheiner’s MSc degree in Occupational Medicine, in The Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel.
The corresponding author has no commercial interest related to this article.
Copyright © by American College of Occupational and Environmental Medicine
* Recall past findings associating sperm parameters with occupational exposure to chemicals or work-related psychological distress
* Understand in what occupational, health, and demographic respects workers with male factor infertility differ from those seen for female infertility.
* Note which if any aspects of occupational stress were associated with male infertility in this study.
* Identify any clinical implications of these findings.
The purpose of this work was to investigate the influence of working conditions, occupational exposures to potential reproductive toxic agents, and psychological stress on male fertility. The study population consisted of 202 consecutive male patients attending a fertility clinic. Of those, 106 patients had attended the clinic because of a male infertility problem (case group), 66 patients had attended the clinic because of a female infertility problem (control group), and 30 patients had a combined infertility problem (male and female). Male infertility was associated with working in industry and construction as compared with other occupations (78.6% vs 58.3%, P = 0.044). Industry and construction workers were of lower educational level than the other workers (mean: 12.1 vs 13.4 years, P = 0.021). These patients also tended to smoke more than the other workers (OR = 2.53, 95% CI = 1.08 to 5.98), more often worked in shifts (OR = 3.12, 95% CI = 1.19 to 8.13), reported physical exertion in work (OR = 3.35, 95% CI = 1.44 to 7.80), and were more exposed to noise and welding (OR = 3.84, 95% CI = 1.63 to 9.14, OR = 4.40, 95% CI = 1.11 to 1.76, respectively). Male infertility (case group) was found to be statistically related to higher marks in all four measures of burnout as compared with the controls. The largest difference was obtained in the measure of cognitive weariness (mean:2.9vs 2.1, P < 0.001). In a multiple logistic regression analysis, industry and construction jobs (adjusted OR = 2.2, 95% CI 1.2 to 2.7) and cognitive weariness (adjusted OR = 1.8, 95% CI = 1.03 to 4.6) were found to be independent risk factors for male infertility problems. Male infertility was independently associated with industry and construction jobs as well as job burnout.
The rise in industrialization, environmental pollution, the use of chemicals, and repeated exposure to hazardous compounds at work adversely affect reproductive health. 1,2 Indeed, during the last decades, there is evidence of decreasing quality of sperm as a result of these factors. 3,4
Several studies had attempted to determine possible associations between abnormal semen parameters and occupational exposures to organic solvents, metals, and pesticides. Significant associations were reported between impaired semen parameters and the following chemical exposures: metals (lead, mercury), 5–8 pesticides (dibromochlorooropane, 2,4-dichlorophenoxyacetic acid), 9–11 solvents (ethylene glycol ethers), 12,13 and estrogens. 14,15 The following physical exposures were shown to deteriorate sperm parameters: radiation (ionizing and microwaves) 16–18 and heat. 19–23 Several exposures cannot be isolated, as illustrated by the impaired spermatogenesis among professional drivers that might be affected by combination of heat exposure, direct toxicity of fuel or exhaust fumes, vibration, occupational or noise stress, and pelvic congestion. 22,23
Psychological distress has another important contribution to infertility. 24,25 Psychological factors in both women and men were found to be significant predictors of a couple’s fertility status. 26,27 Although most studies investigated the psychological component of infertility among women, several studies indicated that stress has a negative impact on sperm parameters as well. 28–31
Another important but less investigated aspect of infertility is the influence of working conditions and psychological stress during work on male fertility. Although several aspects of job strains were investigated in relation to preterm deliveries 32 and plasma testosterone fluctuations, 33 we could not find studies investigating direct relationship between job strains and sperm parameters.
The study objective was to investigate the influence of working conditions, occupational exposures to potential reproductive toxic agents (chemical and physical), and psychological stress on male fertility. An analysis was performed by comparing men who attended a fertility clinic for a male fertility problem with men who were treated in the clinic as a result of their spouse’s fertility problems.
Materials and Methods
Setting and Patients
The study included all male patients who had attended the fertility clinic at the Soroka University Medical Center, a regional teaching hospital, between October 1999 to August 2000. The patients were asked to fill out a questionnaire after having received an explanation about the purpose of the study. The attending physician filled out another questionnaire, including detailed medical history and laboratory test results. The ethical review committee of the hospital approved the study.
The inclusion criteria were working patients who could speak Hebrew and gave their informed consent. Only two patients refused participation. An additional four patients were excluded because of an inability to determine the cause (male or female) of the infertility problem.
The physicians classified infertility into male versus female problems on the basis of laboratory and clinical parameters. All study members were managed in one setting according to standardized protocols by the same personnel.
Semen specimens were collected by ejaculation into a sterile plastic cup in a temperature-controlled environment of a clinical setting. Men were asked to adhere to a 3-day period of sexual abstinence. Specimens were analyzed within 60 to 90 minutes after samples were obtained. All procedures and interpretations used were in accordance with established World Health Organization (WHO) criteria, 34 besides morphology, which was established according to the Kruger parameters. 35 The normal WHO values included concentration of at least 20 million/mL and motility of 50% or more with forward progression. Using the Kruger strict criteria, males with greater than 14% normal forms were considered normal. Undiluted semen (10 μL) was placed in a Makler chamber and evaluated manually by light microscope observation. Sperm concentration, quantity, and quality of motility were assessed. Quality of motility was evaluated subjectively on a scale from 0 to 3. The eosin/nigrosin stain was accomplished distinguishing live from dead cells. 34 The Panicolaou stain was performed for the examination of morphologic features. 34 Analyses were based on at least two samples given by each participant.
The following parameters were assessed by the attending physician: type of infertility (primary or secondary), etiology (male, female, combined, or unexplained), number of treatment cycles, medical history, sperm parameters, laboratory studies including hormonal levels (ie, testosterone, prolactin, luteinizing hormone, follicle-stimulating hormone). The following sociodemographic parameters were evaluated: age, ethnicity, country of birth, level of education, economic status, and number of children. The patients were asked about smoking, alcohol, drugs, physical and sexual activities, and duration of infertility. Assessment of working conditions included the following: number of hours, shifts, occupational exposures to potential reproductive toxic agents (chemical and physical), and psychological stress. Occupational classification was standardized according to the Israel Central Bureau of Statistics. 36
The following three aspects of occupational stress were measured: burnout, job strain (including job demands and decision latitude), and job satisfaction.
Shirom 37 defined burnout as a combination of emotional exhaustion, physical fatigue, and cognitive weariness. The burnout measure comprised three scales: burnout, tension, and listlessness, according to Melamed et al 38 Reliability was evaluated by Cronbach’s alpha coefficients 0.84, 0.90, and 0.73, respectively. Another scale, investigating cognitive weariness was added, according to Kushnir and Melamed, 39 with reliability coefficients—Cronbach’s alpha of 0.70. The burnout questionnaire included eight parameters investigating physical fatigue and emotional exhaustion on a scale of 1 (never) to 7 (almost always), with determinants such as “I feel physically exhausted” or “I feel tired.” The tension and listlessness questionnaires had four parameters, using the same scale. Examples for parameters inquiring tension were as follows: “I feel restless,” “I feel intense inner tension.” Items measuring listlessness were as follows: “I feel sleepy,” “I feel alert” (reversed score), etc. Cognitive weariness was assessed using six parameters, using the same scale. Sample items included the following: “My head is not clear,” “I feel I am disorganized lately.” The total score was averaged by dividing by the number of items.
The job strain model of Karasek et al and Schnall et al 40–42 was developed specifically to assess occupational stress. The two components of the model are job demands and decisional latitude, the former being a measure of the workload. The latter investigates job control or autonomy and includes personal schedule freedom and intellectual discretion. The model is conceptualized as four cells, corresponding to high and low demands, and high and low decisions latitude. We chose the original questionnaire, as was introduced in the Swedish study 40 reporting an association between job strain and the risk of a heart attack. The model was previously examined with regard to fertility, demonstrating significant correlation between high strain and preterm deliveries 32 and testosterone fluctuations. 33
Job satisfaction was evaluated by a simple question “How satisfied are you from your job?” The answers were on a scale from 1 (unsatisfied) to 5 (very satisfied).
To test the statistical significance of the results, the chi-square test or Fisher exact test were used as appropriate when qualitative data were compared. For continuous variables, the t test was used. Multivariable analysis was performed to find independent factors associated with male infertility. Odds ratios (OR) and their 95% confidence interval (CI) were computed. P < 0.05 was considered statistically significant. Reliability coefficients using Cronbach’s alpha were assessed in the burnout and job strains questionnaires. The nonparametric Mann-Whitney test was used to investigate differences in psychological tests. Correlation between the different stress parameters investigated was performed using the parametric Pearson and a-parametric Spearman correlation analyses. Statistical analysis was performed with the SPSS package (SPSS, Chicago, IL).
During the study period, 202 consecutive couples had started cycle of treatment in our clinics. Of those, 106 patients had attended the clinics because of a male infertility problem (case group), 66 patients had attended the clinics because of a female infertility (control group), and 30 patients had a combined infertility problem (male and female). Because the study was based on a comparison of occupational and stress exposures between patients who had fertility problem with those who attended the clinic because their wife had a fertility problem and because of the small number of patients with combined cause for infertility, we did not include these 30 patients in the analysis.
Table 1 shows the sociodemographic and health characteristics of the two group of men. No significant differences were noted between the groups besides higher rate of primary infertility among patients with male infertility as compared with the controls (61.3% vs 40.9%;P = 0.009).
Table 2 presents semen and hormonal characteristics, in addition to medical conditions associated with infertility. As expected from the design of the study, abnormalities in both, sperm performance, hormonal levels, and medical conditions associated with infertility (mainly varicocele and cryptorchidism) of patients from the case group were significantly higher as compared with the controls.
Table 3 compares occupational characteristics according to the cause of infertility (male vs female). Men with male reasons for infertility were more likely to work in industry and construction than men in the control group. No other significant differences were found between the groups. Several exposures to potential reproductive toxic agents are presented on Table 4. Patients admitted because of male infertility problems did not report higher levels of exposures than the controls.
When comparing the group of industrial and construction workers with other occupations, there was a not significant trend toward reduced sperm quality among this group. Industry and construction workers were found to have significantly lower educational level (12.1 year vs 13.4;P = 0.021) and reported higher frequency of smoking (OR = 2.5, 95% CI = 1.1 to 6.0), shift work (OR = 3.1, 95% CI = 1.2 to 8.3) and physical efforts at work (OR = 3.4, 95% CI = 1.4 to 7.8) as compared with other workers. In addition, these patients reported significantly higher exposures to noise and welding (OR = 3.8, 95% CI = 1.6 to 9.1; OR = 4.4 95% CI = 1.1 to 1.8, respectively), and there was a nonsignificant trend toward vibration exposure during work (OR = 3.9 95% CI = 0.9 to 17.3). Table 5 demonstrates burnout, job strain, and job satisfaction of the two groups. All burnout parameters were significantly higher among the cases as with the controls using the Mann-Whitney test. High reliability was found, as demonstrated by Cronbach’s alfa of 0.85 to 0.91 for the four-burnout parameters. No significant differences were noted between the groups with regard to the job strain or job satisfaction scores.
Significant associations between all four parameters of burnout were found using the nonparametric Spearman correlation (Table 6). To investigate independent contributions of the factors found to have significant correlation in the univariate analysis, a multivariable analysis model was constructed. The model included industry and construction workers and cognitive weariness. The latter was proved to be the most important, significant parameter of burnout, using a back-step multivariable analysis. Cognitive weariness was entered into the model as units of standard deviations from the mean. Both factors, industry and construction (adjusted OR = 2.2, 95% CI = 1.2 to 2.7;P = 0.043), and cognitive weariness (adjusted OR = 1.8, 95% CI = 1.03 to 4.6;P = 0.004) were found to be significantly associated with male infertility.
The present study demonstrates a significant association between male infertility and industry and construction jobs and high burnout. The design of the study, including only couples with infertility, enabled to control for recall bias. 43–45 This trend was explained by a tendency of individuals who have experienced adverse reproductive outcomes to over report, or report an exposure more accurately than those without reproductive dysfunction, who tend to underreport exposures. 43–45
The study was performed in the fertility clinic of a regional, tertiary medical center, including consecutive couples, with male and female infertility problems. Only two patients refused to participate; thus, patients who were included and provided semen samples truly represent the population with infertility in this area. 43 This fact is important because of reduced risk for selection bias. 45,46 Moreover, the semen samples were given as part of the routine treatment protocols and not for the study. Age, which was found to be another strong determinant of participation, 43 was similarly distributed in the two groups, like all other sociodemographic characteristics.
No significant differences were found between the groups regarding occupational exposures to physical or chemical agents. Although an important limitation is the study’s size, there is also a possibility of problematic exposure definition. Inclusion of all individuals who had ever exposed to an agent, rather than only those who recently had contact with the agent, may dilute the truly exposed population, and thus mask the contribution of a certain agent on the disease. 45
Men from the case group were more likely to be employed in industry and construction than men who attended because of female (ie, their spouse’s) infertility. These blue-collar workers introduce the healthy worker effect, indicating selection of healthy people to this job. This fact strengthened the contribution of these occupational exposures to infertility. In an attempt to characterize this group, we found these patients to be exposed to significant higher levels of smoking, shift work, physical efforts, noise, and welding. In addition, there was a not significant increased risk of exposures to vibration, metals, solvent, and heat. The latter were proved to be associated with reduced sperm quality. 5–8,12,13,19–23 A meta-analysis convincingly demonstrated that smoking is associated with reduced sperm concentration, with an average reduction between 13% to 17%. 47 However, inconsistency exists with regard to the influence of welding and noise on the male reproductive system, mainly because of difficulties in isolating these effects from heat, vibration, metals, etc. 48,49 Undoubtedly, industrial and construction workers are exposed to some environmental hazards, several of which can result in reduced semen quality.
A significant association was found between male infertility and job burnout. It is unclear whether this observation is a “chicken and egg problem,” that is, which comes first. The stress could be caused by the anxiety of not having children rather than work stress affecting the sperm quality. Although it may be difficult to really dichotomize the two clearly, stress at work was assessed mainly using the burnout questionnaire, detecting work-related stress. This questionnaire had a high reliability coefficients and previous experience with Israeli workers. 38 High level of burnout, as was assessed by this questionnaire, was recently found to be positively associated with several physiologic parameters as leukocyte adhesiveness and aggregation and salivary cortisol levels. 50,51 In the present study, for the first time, male infertility was found to be related to higher levels in all four measurements of burnout. Cognitive weariness was found as the strongest factor associated with infertility. Indeed, previous studies have indicated that psychological stress has a negative impact on semen quality. 26–31 Nevertheless, the majority of these studies did not differentiate between the sources of the stress (work, family problems, economical difficulties, health problems etc.). The importance of the present study is the attempt to examine the contribution of stress and burnout at work on infertility.
In conclusion, the study found male infertility to be associated with industry and construction jobs and in workers who suffer of work burnout. However, no significant association was found between male infertility and potential physical or chemical exposures, mainly because of the small study size. Occupational parameters should be an important part of history taking among patients attending infertility clinics. Moreover, possible psychological factors like work burnout should be evaluated on admission. The usefulness of interventions attempting to reduce the stress component in infertile patients should be evaluated in further prospective studies.
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