Aging and Sexual Function in Men

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1 Archives of Sexual Behavior, VoL 22, No. 6, 1993 Aging and Sexual Function in Men David L. Rowland, Ph.D., 1,5 Walter J. Greenleaf, Ph.D., 2 Leslie J. Dorfman, Ph.D., 3 and Julian M. Davidson, Ph.D. 4 Sexual function, and in particular erectile capacity, declines with age in men. The present study attempted to identify possible sensory~neural and autonomic factors related to this decline. Data on self-reported sexual activity and functioning, as well as erectile response to visual erotic stimulation, were gathered from 39 healthy, sexually functional men ranging in age from 21 to 82. In addition, four parameters of putative significance to sexual functioning were measured: penile electrical and vibrotactile thresholds, pudendal somatosensory evoked potentials, penile autonomic response to ischemia, and blood testosterone. Results indicated significant age-related decreases in self-reported frequency of sexual activity and in erectile response to erotica. Furthermore, penile sensitivity, response to penile ischemia, and somatosensory evoked potentials showed age-related changes. In contrast, self-reported erectile capacity, ratings of overall sex life, and levels of testosterone did not change over age groups. These findings suggest that decreasing erectile capacity in aging men may be related to decreasing sensory~neural and autonomic functioning, but they also indicate that factors other than the frequency of and potency for sexual response are important to the overall rating of sex life. KEY WORDS: aging; sexual function; sensory; neural; men; erection. INTRODUCTION Scientific investigation has supported the long-held notion that sexual function in men declines with age. A variety of studies indicate that as men 1Department of Psychology, Valparaiso University, Valparaiso, Indiana Department of Physiology, Stanford University, Stanford, California. 3Department of Neurology, Stanford University, Stanford, California. 4Department of Molecular and Cellular Physiology, Stanford University, Stanford, California. 5To whom correspondence should be addressed /93/ Plenum Publishing Corporation

2 546 Rowland, Greenleaf, Dorfman, and Davidson reach late middle and old age, the frequency of sexual activity becomes lower, libido is diminished, and an overall decline occurs in such parameters as sexual thoughts, sexual enjoyment, and erectile and orgasmic function (Kinsey et al., 1948; Martin, 1981; Davidson et al., 1983). Many factors apparently contribute to this decline, including such nonspecific agents as decreased health and mobility, increased incidence of disease, partner considerations, and increasing neurologic dysfunction (Potvin et al, 1980). Yet even when these factors are controlled, the pattern of diminishing sexual function with age is still evident (Davidson et al., 1983; Tsitouris et al., 1982). Although these studies provide strong evidence for a gerontological influence on sexual function, few studies have adequately delineated the particular phases of the sexual response cycle that are most likely affected in aging men, let alone the physiological mechanism of action. For example, it appears that sexual desire and satisfaction may be less affected by age than arousal (potency) and ejaculation. Several studies based upon prospective self-report techniques indicate little or no difference in sexual desire, sexual satisfaction, and enjoyment in men between the ages of 45 and 74 (Davidson et al., 1983; Schiavi et al., 1990; Schiavi, 1991). In contrast, laboratory measures of sexual arousal or potency, though scant, suggest that erectile response, both during erotic video stimulation and during nocturnal penile tumescence, is diminished in aging men compared with younger counterparts (Solnick and Birren, 1977; Karacan et al., 1975; Schiavi and Schreiner-Engel, 1988). Attempts have been made to identify factors specific to erectile function that may account for its age-related decline. A number of studies (Davidson et al., 1983; Tsitouris et al., 1982; Korenman et al., 1990; Zummoff et al., 1982) have found a small but reliable age-related decline in testosterone, a hormone of vital importance to sexual response in men. Other investigations, however, have not confirmed a major role for this hormone in the dysfunction of aging (Davidson etal., 1982; Krane et al., 1989). In some instances, the absence of a clear and direct relationship between testosterone and sexual function in aging men may reflect the inadequacy of measuring serum testosterone rather than bioavailable testosterone. Nevertheless, some evidence suggests that even bioavailability of testosterone may not be highly predictive of sexual function in older men (e.g., Davidson et al., 1983; Korenman et al., 1990). A more promising approach, therefore, may lie in the assessment of age-related changes in neural and/or vascular function. Several studies have documented increased penile thresholds to vibrotactile and electrical stimulation in aging men (Rowland et al., 1989; Edwards and Husted, 1976), suggesting decreased neurological function in the genital area as a result

3 Aging and Sexual Function in Men 547 of aging. A role for vasculopathy has been implicated as well; postmortem histological analysis has revealed morphological changes in the arterial bed of the penis of aging men, and some attempt has been made to relate such changes with sexual competence (Conti and Virag, 1989; Ruzbuarsky and Michal, 1977; Mottonen and Nieminen, 1988). Taken together, these data suggest that no single factor is likely to account for all or most of the agerelated decline in sexual activity. More likely, neural, vascular, and other, as yet unspecified, factors combine to produce the sexual deficit in aging men. It remains unclear as to when the onset of diminished erectile capacity is most likely to occur, and to what extent decreased erectile capacity might be interrelated with changes in endocrine levels, vasculopathy, and sensory/neural function. The following research represents a preliminary attempt to study age-related changes in self-reported and laboratorydetermined erectile capacity in a group of disease-free, sexually functional men spanning six decades in age. Erectile response was then related to sensory/neural integrity, autonomic nervous system functioning, and testosterone levels. METHOD Subjects Thirty-nine eugonadal, sexually functional and active men ranging in age from 21 to 82 were recruited through local advertisement and wordof-mouth. Volunteers were informed by phone about all procedures involved in participation and were requested to complete the Stanford Male Questionnaire which solicited information on personal and sexual history, level of sexual activity and satisfaction, and current sexual functioning. In addition, a complete medical history was obtained on each subject prior to acceptance in the study. Subjects identified as having a physical disorder or taking medication/drugs that might interfere with sexual function were screened from the study. Extensive clinical interview and questionnaire responses were used to determine level of sexual function, and to eliminate subjects having a major sexual disorder. For this study, a major disorder was defined as one that interfered with any aspect of sexual response more than half the time. Informed consent was obtained after the subject's preliminary visit to the laboratory and interview with a member of the experimental team.

4 548 Rowland, Greenleaf, Dorfman, and Davidson Measurements In addition to the self-report data on sexual function and activity obtained with the Stanford Male Questionnaire, the following laboratory measurements were made: Erectile Response Erectile response, measured in mm of penile circumference, to erotic stimulation and self-generated sexual fantasy was determined in two separate 45-min sessions using a mercury strain gauge. The dc output from the gauge was amplified with a Grass polygraph, with hard copy output recorded on standard polygraph chart paper, and analog and digitized output sent to an on-line data collection system. In this laboratory procedure, the subject sat in a private, comfortable room adjacent to the recording laboratory. The strain gauge was placed at the base of the penis by the subject, with placement visually verified by the male experimenter. During the session, the subject viewed two erotic films and attempted two sexual fantasies. All episodes were interspersed with neutral (nonerotic) film segments. Stimulus and neutral periods lasted 4-6 min, though neutral stimulus periods were extended if the erectile measure failed to return to baseline within that interval. The order of stimuli was: fantasy 1, erotic tape 1, erotic tape 2, and fantasy 2. Different erotic tapes were used in each of the 45-min psychophysiological testing sessions. Three erectile response values were calculated for each subject: maximum amplitude of erection (MAX), defined as the greatest amount of circumference increase during any stimulus period; latency to 80% of MAX (T-UP), defined as the latency in seconds between the onset of the erotic stimulus (either film or fantasy) and an increase to 80% of the value of MAX; and latency to 20% of baseline (T-DOWN), defined as the amount of time between the end of the erotic stimulus and the return to 20% of the prestimulus baseline. Vibrotactile and Electrical Thresholds Vibrotactile and electrical thresholds were determined on the ventral surface of the penis, with stimulation approximately 10 mm anterior to the coronal ridge. Electrical stimulation was delivered through silver/silver chloride electrodes in pulses of 200 msec. Vibrotactile stimulation of 120 Hz was applied to an area approximately 200 mm 2 for approximately 500 msec. A more detailed report of this procedure, as well as preliminary results,

5 Aging and Sexual Function in Men 549 are described in Rowland et al. (1989). Threshold values included in the data analysis represent milliamperes for electrical stimulation and microns of stimulus movement for vibrotactile stimulation. Somatosensory Evoked Potentials Somatosensory evoked potentials (SEP) were recorded from locations CZ, PZ, and PZ prime (int system), referenced to linked mastoids. All recordings were collected using the same DISA evoked potential recorder and signal averager. Session wave form values were obtained by averaging the results of two separate SEP tracings, each in itself representing the average of between 500 and 2000 evoked responses. Stimulation occurred at two sites: penis (pudendal nerve) and ankle (tibial nerve). The stimulus voltage for both central and peripheral stimulation was set for 25% above sensory perceptual threshold--this level is usually described as unpleasant but not painful. The stimulus was a square wave pulse of msec duration, delivered at a rate of 3 to 5 per sec. Latencies of onset positivity (P0) and peak positivities (P1, P2) were calculated for each subject and used in the data analysis. Autonomic Function Test Autonomic function test (AFT): the local autonomic reactive hyperemia response to 4 rain of occlusive ischemia was obtained from both finger and penis. This technique has been used clinically to distinguish and index the degree of local autonomic' neuropathy in diabetics (Sumner, 1977), and less frequently, to assess autonomic neuropathy in men with sexual dysfunction (Abelson, 1975). For penile recordings, a pneumatic cuff was wrapped around the base of the flaccid penis, and a photoplethysmographic sensor was placed anterior to the cuff against the dorsal surface of the penis. Following a 4-min baseline, ischemia was produced by inflating the cuff to a pressure slightly above the mean arterial pressure. After 4 rain of ischemia, the pressure was released, and the pulse signal monitored for an additional 2 mix. Results were scored as the percentage of change in pulse amplitude between resting and postischemic periods. Serum Testosterone Overall serum testosterone was determined from 20-ml aliquots obtained by venipuncture between 0900 and Blood was immediately

6 550 Rowland, Greenleaf, Dorfman, and Davidson frozen and later assayed for total testosterone by radioimmunoassay according to the method of Frankel et al. (1975). General Procedure After preliminary screening and informed consent, a blood sample was collected from the subject and a schedule for further testing established. Somatosensory evoked potentials and autonomic function tests were carried out during the first two laboratory visits. Electrical and vibrotactile thresholds were determined immediately prior to the two psychophysiological sessions with erotic videotapes. Laboratory tests were generally scheduled at least 1 week apart. For thresholds and penile response to erotic stimulation, the average of the two sessions was used in the data analysis (test-retest reliability for comparable studies in our lab has been.82 and.71, respectively). Data Analysis Data from this study were viewed in two ways. To facilitate cross-sectional comparisons of the data, the subjects were divided into either three or four age categories, each of about 10 to 20 years. In those instances where numbers of subjects were fewer, age groups were collapsed and these new groups are described within each analysis. Due to the scarcity of data regarding age-related changes on sexual function, no theoretical basis was used to establish age intervals. However, where possible we did try to establish late middle (55-69) and old age (70+) groups, consistent with the idea that self-reported declines in sexual response occur at these ages (e.g., Davidson et al., 1983). For each variable, a one-way ANOVA was performed, followed by Newman-Keuls multiple comparison tests. A second approach was also used, in which age was correlated with each dependent variable measure using the Pearson r. In some instances, dependent variables were correlated among each other. Two-tailed probabilities are reported for all analyses unless otherwise stated. RESULTS Description of Self-Reported Sexual Functioning Most items of self-reported sexual function showed no significant variation across age groups (Table I). However, total sexual activity per month

7 Aging and Sexual Function in Men S$1 (an inclusive measure of sexual activity with self and/or with partner) differed significantly among age groups (p = 0.001). The two highest age groups differed from the lower age groups on this item (p < 0.05), but did not differ significantly from each other. The correlation between total sexual activity and age was -.36 (p < 0.05). There was also a significant correlation between total sexual activity and the "opportunity for sex," (r =.39; p = 0.024), and a lower, nonsignificant correlation between age and the opportunity for sex (r = -.31). Erectile Parameters During Erotic Videotape and Fantasy Maximum Amplitude Although there were higher maximum amplitudes (indicating greater tumescence) in younger subjects (Fig. 1), differences among the four groups only approached significance (p = 0.07). Correlational analysis indicated a moderate negative correlation between age and maximum amplitude (!" = -.48; p < 0.01). Latency to maximum tumescence (T-UP) differed significantly among age groups (p < 0.001). Individual comparisons indicated that the two high- Table I. Self-Reported Sexual Function in Four Age Groups of Men Age group n Age Testosterone (ng/100 ml) ,8 a Sexual activity (times/month) b Quality of sex life (1 = poor, 7 = excellent) Lack of interest in sex c Difficulty getting erection c Difficulty keeping erection c ,0 Premature ejaculation c 5.6 5, Retarded ejaculation c 6.2 6, Loss of interest in partner c 5.4 4, Dissatisfied with partner c 4.7 5, ,2 Not enough opportunity for sex c b Fear of sexual performance c afor this variable, n = 4; this group was not included in ANOVA. bp < 0.05 for overall ANOVA. CFor this item, 1 = always, 4 = about half the time, 7 = never.

8 552 Rowland, Greenleaf, Dorfman, and Davidson Maximum Amplitude of Erection (MAX) A X =E Age Group Time to Maxium Amplitude (T-UP) B. 200 m Age Group Fig. 1. Age comparisons of (A) maximum change in penile circumference from baseline in mm (MAX) and (B) latency to 80% of maximum (T-UP). est age groups took significantly longer to achieve erections than the two lower age groups. In addition, the two lowest age groups differed significantly on this parameter. Latency to detumescence (T-DOWN), while longer for older subjects, did not differ significantly among groups. The correlation between T-UP and age was +.68 (/7 < 0.001); between T- DOWN and age, +.41 (p < 0.01).

9 Aging and Sexual Function in Men 553 Somatosensory Evoked Potentials Evoked potentials were recorded on a subgroup of 28 subjects. For age group comparisons, subjects were divided into three categories: years (n = 10), (n = 9), and (n = 9). Within-subject comparison for the corresponding latency measurements for the two stimulation sites (pudendal vs. tibial) indicated no significant differences in the latency between onset positivity (P0) and peak positivities (P1, P2) despite a difference of up to 85 cm in the length of the conductive pathway. Comparisons among age groups indicated significant changes with age for all three measures for pudendal evoked potentials (p < 0.05), with post hoc analysis indicating that the oldest group showed longer latencies than the two other age groups (p < 0.05). For tibial evoked potentials, peak positivities (P1, P2) showed significant variation across age (p < 0.05), with the youngest group showing significantly lower latencies than the two older groups (Table II). Correlational analysis controlling for height of the individual subjects indicated high correlations between age and all evoked potential parameters (see Table III). Autonomic Function Test Due to the difficulty of achieving a steady baseline for the resting penile pulse amplitude, measurements for finger and penile local autonomic function were obtained from only 16 subjects. Subjects were divided into two groups: years (n = 8) and (n = 8). For within-subject comparisons between finger and penis, percentage change in pulse amplitude following ischemia was lower for the finger than the penis (p < 0.05); and a greater difference between the two locations Table II. Somatosensory Evoked Potentials (Latency in msec) Over Three Age Groups P0 P1 P2 Age group n x SEM x SEM x SEM Pudendal , , Tibial

10 554 Rowland, Greenleaf, Dorfman, and Davidson Table III. Correlations Between Age and Somatosensory Evoked Potentials P0 P1 P2 Pudendal r p Tibial r p <0.001 <0.001 was observed in the younger age group than the above-50 group (p < 0.05) (Fig. 2). Moreover, comparison of the two age groups yielded significant variation for penis (p < 0.05) but not for finger values, with lower percentage change in the older group. Because the ages were bimodally distributed, no correlational analysis was undertaken. Testosterone The mean serum testosterone values did not differ significantly for the four age groups (see Table I), nor was there a significant correlation between age and testosterone. 4OO o~ i ~ 100 [] RNG~q [] PENIS AGE~P Fig. 2. Differences between finger and penile response to ischemia over age groups.

11 Aging and Sexual Function in Men 555 Correlations Among Measures Pearson correlations were performed for dependent measures where there was a physiological mechanism that would conceptually support an interrelationship. Maximum penile tumescence to erotic film was negatively correlated with penile threshold to electrical stimulation (r = -.45, p < 0.05), and latency to erection (T-UP) was correlated with penile vibrotactile thresholds (r = +0.69, p < 0.05). Thus greater tumescence and shorter latencies were associated with lower penile thresholds. Latency to erectile detumescence (T-DOWN) was also related to self-reported total sexual activity (r = -.37, p < 0.05). Finally, penile electrical sensory threshold correlated with pudendal evoked potential latencies when height was controlled (r = +.50, p < 0.05), indicating that men with longer SEP latencies had higher thresholds to electrical stimulation. Because each of these dependent measures also covaried with age, the nature of these relationships must be considered exploratory. DISCUSSION In this preliminary study, five objectives were put to bear in assessing mechanisms presumably related to sexual functioning in healthy, sexually active men: erectile response, penile electrical and vibrotactile thresholds, penile somatosensory evoked potentials, penile autonomic function assessed through response to ischemia, and blood measurement for testosterone. Despite the fact that all subjects, including those in the higher age groups, were selected on the basis of being both sexually functional and active, on four of these measures, age-related declines were apparent. Specifically, erectile capacity was lower and latency to erection longer for men 50 years of age or older. Penile vibrotactile and electrical sensitivities were lower (Rowland et al., 1989), pudendal evoked potentials showed longer latencies, and penile response to ischemia was diminished in the older group. Only testosterone showed no age-related change, a finding inconsistent with previous research (Davidson et al., 1983; Korenman et al., 1990) but not surprising in view of the small, highly functional sample used in this study. Such interrelationships among age, self-reported sexual activity, and decreased functioning of sensory, afferent neural, and autonomic function provide further evidence that changes in neural and vascular integrity may play a role in the decreased erectile capacity and self-reported sexual activity evident in older men. Despite these age-related declines, sexual interest among older men remained high, a finding consistent with previous reports (Davidson et al.,

12 556 Rowland, Greenleaf, Dorfman, and Davldson 1983) and possibly related to high levels of testosterone in this group. And, because subjects in this study were selected for their high level of sexual functioning, self-reported erectile capacity among older men was comparable to that of younger men, even though laboratory-measured erectile response was significantly lower in older men. Thus, while the age-related decline in self-reported total sexual activity may be partially related to lower sensory, neural, and autonomic function, part (though probably not all) of this decline may have also been related to the reported lack of opportunity for sex. Furthermore, despite lower sexual activity and erectile capacity in older men, this group rated the quality of their sex life as being comparable to that of the younger groups. The implication is that factors other than frequency and potency of response have a strong impact on the overall enjoyment of sex life. Of significance is the finding that age-related changes in physiological function were not restricted to the genitals. For measures of sensory, afferent neural, and autonomic function, the response at a nongenital site was affected as well. Thus, finger sensitivity was decreased, latency to tibial evoked potential response was longer, and finger response to ischemia was diminished in older men. Such patterns suggest that the decrements seen in the genital area are merely reflective of the larger process of aging occurring throughout the body. On the other hand, the fact that age-produced decrements in autonomic function and sensory thresholds were augmented in the genital region may indicate a particular vulnerability of this region to the effects of aging. An ongoing challenge in assessing sexual function in aging subjects is that of distinguishing between those effects that result from the aging process and those caused by sickness and disease related to old age, or by prolonged use of pathophysiological agents (e.g., tobacco, alcohol). Such processes often share common elements. As seen from this study, sexual function in aging men may be studied using a variety of objective measures. Because the present study included only sexually functional and active men, generalization of these findings to aging men with sexual dysfunction may be limited. However, we propose to examine with greater detail the relative importance that each of these measures brings to bear on the understanding of sexual response and dysfunction. Objective methodology of this type, together with larger samples that include greater variation in the range of sexual functioning and more powerful statistical techniques such as multiple regression analysis, may provide a useful supplement to the more common, though often less reliable, assessment methods of self-reported sexual function or of erectile capacity measured in the laboratory.

13 Aging and Sexual Function in Men 557 REFERENCES Abelson, D. (1975). Diagnostic value of the penile pulse and blood pressure: A Doppler study of impotence in diabetics. J. Urol. 113: Conti, G., and Virag, R. (1989). Human penis erection and organic impotence: Normal histology and histopathology. UroL Int. 44: Davidson, J. M., Chen, J., Crapo, L., Gray, G., Greenleaf, W., and Catania, J. (1983). Hormonal changes and sexual function in aging men. J. Clin. Endocrinol. Metab. 57: Davidson, J. M., Kwan, M., and Greenleaf, W. J. (1982). Hormonal replacement and sexuality in men. Clin. Endocrinol. Metab. 11: Edwards, A. E., and Husted, J. R. (1976). Penile sensitivity, age, and sexual behavior. Z Clin. PsychoL 32: Frankel, A. I., Mock, E. J., Wright, W. N., and Kamel, F. (1975). Characterization and validation of a radioimmunoassay for plasma testosterone in the male rat. Steroids 25: 73-89, Karacan, I., Williams, R. L., Thornby, J. I., and Salis, P. (1975). Sleep-related tumescence as a function of age. Am. J. Psychiat. 132: Kinsey, A. C., Pomeroy, W. B., and Martin, C. E. (1948). Sexual Behavior in the Human Male, W. B. Saunders, Philadelphia. Korenman, S. G., Morley, J. E., Mooradian, A. D., Davis, S. S., Kaiser, F. E., Silver, A. J., Viosca, S. P., and Garza, D. (1990). Secondary hypogonadism in older men: Its relation to impotence. J. Clin. EndocrinoL Metab. 71: Krane, R. J., Goldstein, I., and Saenz de Tejada, I. (1989). Impotence. N. Eng. Z Med. 321: Martin, C. E. (1981). Factors affecting sexual function in year old males. Arch. Sex. Behav. 10: Mottonen, M., and Nieminen, K. (1988). Relation of atherosclerotic obstruction of the arterial supply of the corpus cavernosum to erectile dysfunction. Proceedings of the 3rd Biennial World Meeting on Impotence, Abstract 12, Boston. Potvin, A. R., Syndulko, K., Tourtellotte, W., Lemmon, J., and Potvin, L (1980). Human neurologic function and the aging process. J. Am. Getiat. Soc. 28: 1-9. Rowland, D. L., Greenleaf, W., Mas, M., Myers, L., and Davidson, J. M. (1989). Penile and finger sensory thresholds in young, aging, and diabetic men. Arch. Sex. Behav. 18: Ruzbuarsky, V., and Michal, V. (1977). Morphological changes in the arterial bed of the penis with aging: Relationship to the pathenogenesis of impotence. Invest. Urol. 15: 194. Schiavi, R. C. (1991). Sexuality and aging in men. In Bancroft, J., Davis, C. M., and Weinstein, D. (eds.), Annual Review of Sex Research, Vol. 1, The Society for the Scientific Study of Sex, Lake Mills, IA, pp Schiavi, R. C., and Schreiner-Engel, P. (1988). Nocturnal penile tumescence in healthy aging men. Y. Gerontol. 43: M Schiavi, R. C., Schreiner-Engel, P., Mandel, I., Sehanzer, H., and Cohen, E. (1990). Health aging and male sexual function. Am. J. Psyehiat. 147: Solnick, R. L., and Birren, J. E. (1977). Age and male erectile responsiveness. Arch. Sex Behav. 6: 1-8. Sumner, D. S. (1977). Digital plethysmography. In Rutherford, R. B. (ed.), Vascular Surgery, W. B. Saunders, Philadelphia. Tsitouras, P. D., Martin, C. E., and Harman, S. M. (1982). Relationship of serum testosterone to sexual activity in healthy elderly men. J. Geronto! 37: Zumoff, B., Strain, G., Kream, J., O'Connor, J., Rosenfeld, R., Levin, J., and Fukoshima, D. (1982). Age variation in the 24-hour mean plasma concentrations of androgens, estrogens, and gonadotropins in normal adult men. Z Clin. EndoclinoL Metab. 54:

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