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Adult urology| Volume 61, ISSUE 1, P184-189, January 2003

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Nocturnal penile tumescence and effects of complete spinal cord injury: possible physiologic mechanisms

  • Donald D Suh
    Affiliations
    Department of Urology, University of Washington School of Medicine, Seattle, Washington, USA
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  • Claire C Yang
    Correspondence
    Reprint requests: Claire C. Yang, M.D., Department of Urology, University of Washington School of Medicine, Spinal Cord Injury Unit, Veterans Affairs Puget Sound Health Care System, 112-UR, 1660 South Columbian Way, Seattle, WA 98108, USA
    Affiliations
    Department of Urology, University of Washington School of Medicine, Seattle, Washington, USA

    Spinal Cord Injury Unit, Veterans Affairs Puget Sound Health Care System, Seattle, Washington, USA
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  • Diane E Clowers
    Affiliations
    Spinal Cord Injury Unit, Veterans Affairs Puget Sound Health Care System, Seattle, Washington, USA
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      Abstract

      Objectives

      To determine the role of the spinal cord in the initiation and/or modulation of nocturnal erectile activity, we measured nocturnal penile tumescence (NPT) in men with complete spinal cord injuries at known locations.

      Methods

      Eighteen men between the ages of 27 and 57 years (mean 45) with known complete spinal cord lesions and no history of other medical problems adversely affecting erectile function completed International Index of Erectile Function questionnaires and underwent RigiScan testing for two consecutive nights. RigiScan tracings were evaluated for the presence and quality of NPT activity. Erectile episodes lasting longer than 10 minutes with base and tip rigidity greater than 70% were designated “good”; the remainder were designated “borderline,” “poor,” or “absent.”

      Results

      Of 9 men with cervical injuries and 9 with thoracic injuries, 8 and 3, respectively, had evidence of NPT. Of the 9 men with cervical injuries, 3 had one or more “good” nocturnal erections, and 1 of 9 men with thoracic injuries had one or more “good” nocturnal erections. The mean duration of the single longest erectile event was 26 minutes in men with cervical spinal injuries and 12 minutes in men with thoracic spinal injuries. Men with cervical and thoracic injuries had a mean overall International Index of Erectile Function score of 10 and 16 and a mean erectile domain score of 2 and 3, respectively.

      Conclusions

      Spinal regulation is critical for nocturnal erectile activity, and the isolated thoracic cord is less effective than the isolated cervical cord in maintaining NPT. Despite the presence of nocturnal erectile activity, volitional erectile function in spinal cord-injured men is significantly impaired.
      N octurnal penile tumescence (NPT) monitoring is an important tool for the study of erectile dysfunction. NPT monitoring reflects the integrity of the efferent arm of the erectile reflex, indirectly testing the neural, vascular, and hormonal influences on erectile function. Many clinicians have used NPT testing as the noninvasive reference standard for the differentiation of organic and psychogenic causes of erectile dysfunction.
      • Levine L.A.
      • Lenting E.L.
      Use of nocturnal penile tumescence and rigidity in the evaluation of male erectile dysfunction.
      ,
      • Kaneko S.
      • Bradley W.E.
      Evaluation of erectile dysfunction with continuous monitoring of penile rigidity.
      Because the motor (efferent) pathway is presumed to be the same for reflexogenic, psychogenic, and nocturnal erections, the presence of nocturnal erections is thought to reflect an intact ability for volitional (ie, psychogenic or reflexogenic) erections.
      • Levine L.A.
      • Lenting E.L.
      Use of nocturnal penile tumescence and rigidity in the evaluation of male erectile dysfunction.
      Despite the importance of NPT testing, little research has been done of the neurologic mechanisms of NPT.
      The spinal cord is an important organizational center for all genitourinary functions, including micturition and erection.
      • Bors E.
      • Comarr A.
      Neurological disturbances of sexual function with special reference to 529 patients with spinal cord injury.
      The precise role of the spinal cord in NPT remains unclear. The identification of the centers for initiation and modulation of NPT will improve our understanding of central nervous system control of erection and may hold the keys for the restoration of erectile function in men with neurologic etiologies of erectile dysfunction. Spinal cord-injured men serve as important models for the investigation of central nervous system centers necessary for NPT. Because the injured spinal cord is isolated from the upper central nervous system, it is possible to study relationships between NPT activity and spinal lesions at specific levels. By measuring NPT in men with complete spinal cord injuries at known locations, we can begin to determine the role of the spinal cord in initiation and/or modulation of nocturnal erectile activity.

      Material and methods

      Eighteen men with known complete spinal cord lesions (American Spinal Injury Association A, ASIA A) between the ages of 27 and 57 years (mean 45) were enrolled in this study. The Human Subjects Review Committee of our institution approved the study protocol. Subjects were inpatients in the Spinal Cord Injury Unit for annual comprehensive physical and social needs assessments or for treatment of decubitus ulcers. The level and completeness of the spinal cord injury were determined by neurologic evaluations and imaging. Patients with medical problems other than spinal cord injury that could adversely affect erectile function, such as cardiovascular disease or diabetes, were excluded from the study. All subjects denied any history of erectile dysfunction before the spinal cord injury. Only men with spinal injuries for 2 years or longer were enrolled.
      Each subject filled out an International Index of Erectile Function (IIEF) questionnaire.
      • Rosen R.C.
      • Riley A.
      • Wagner G.
      • et al.
      The International Index of Erectile Function (IIEF) a multidimensional scale for assessment of erectile dysfunction.
      Each patient underwent RigiScan (Timm Medical Technologies, Eden Prairie, Minn) monitoring for two consecutive nights. The RigiScan is a portable strain-gauge device that measures the girth, rigidity, and frequency of erections using two looped cables placed around the proximal and distal penile shaft.
      Kaneko and Bradley
      • Kaneko S.
      • Bradley W.E.
      Evaluation of erectile dysfunction with continuous monitoring of penile rigidity.
      and Kessler
      • Kessler W.O.
      Nocturnal penile tumescence.
      described nocturnal erections in healthy males with a duration greater than 10 minutes and base and tip rigidity greater than 70% as adequate for penetration and maintenance during intercourse. For the purposes of our study, we considered nocturnal erections meeting these criteria as “good,” realizing that volitional erectile function in spinal cord-injured men might be significantly impaired despite the presence of “good” NPT. The quality of NPT was considered “borderline” if the erections were of significant rigidity and duration but did not meet all the mentioned criteria and “poor” if the erections were of minimal rigidity and duration. Subjects were asked to abstain from self-stimulation or sexual activity during the overnight RigiScan sessions. Foley and condom catheters were left in place during RigiScan monitoring.

      Results

      Nine men with cervical injuries (mean age 42 years) and 9 men with thoracic injuries (mean age 47 years) participated in this study (Table I). Thirteen men were inpatients for annual evaluations and 5 for wound care of decubitus ulcers. For bladder management, 2 subjects performed clean intermittent catheterization, and 9 had an indwelling urethral Foley catheter, 3 a suprapubic catheter, and 4 an external condom catheter (after sphincterotomy). Testosterone levels within 1 year of the study were available in 14 of the 18 subjects and were within the normal range in 13 of the 14 men.
      TABLE IAge, injury level, and results of NPT testing for individual subjects
      Age (yr)Injury LevelNPT ActivityNPT QualityLongest EventDuration (min)
      49C4YesGood20
      34C4YesGood59
      46C4YesGood30
      33C5No
      47C5YesBorderline11
      51C6YesBorderline23
      31C7YesBorderline14
      40C7YesPoor<5
      43C7YesPoor<5
      45T1YesPoor<5
      54T3No
      51T4No
      27T5YesGood17
      44T8No
      51T9YesBorderline8
      39T9No
      57T12No
      55T12No
      Key: NPT = nocturnal penile tumescence.

      Subjective reports of erectile function

      All 9 men with cervical spinal injuries reported reflexogenic erections, none reported psychogenic erections, and 7 of 9 reported nocturnal erections. No men with cervical injuries reported ejaculation or orgasm after the spinal cord injury. Six of 9 men with thoracic spinal injuries reported reflexogenic erections, 0 of 9 psychogenic erections, and 5 of 9 nocturnal erections. Only 1 man with a thoracic injury (T12) reported episodes of ejaculation/orgasm after spinal cord injury.

      RigiScan findings

      Eight of 9 men with cervical injuries and 3 of 9 men with thoracic injuries had evidence of nocturnal erectile activity on RigiScan monitoring (Table I). Of the 8 men with cervical injuries who demonstrated erectile activity, 3 met the criteria for a “good” erection (greater than 70% rigidity at both tip and base and lasting for greater than 10 minutes), 3 had “borderline” quality erections, and 2 had “poor” quality erections. Of the 3 men with thoracic injuries who demonstrated erectile activity, 1 had an erection that met the criteria for a “good” erection, 1 had “borderline” quality erections, and 1 had “poor” quality erections. To assess the ability to sustain nocturnal erections, the duration of the longest erectile episode was measured. The average duration of this erection was 26 minutes in men with cervical injuries and 12 minutes in men with thoracic injuries (Table I).

      IIEF questionnaire scores

      Of a possible score of 75, the mean overall IIEF score was 10 in men with a cervical injury and 16 in men with a thoracic injury. Of a possible score of 30, the mean erectile domain score was 2 in men with a cervical injury and 3 in men with a thoracic injury. Four of 18 subjects reported the use of erectile aids: none were currently using sildenafil, 3 were using intracavernosal prostaglandin injections, and 1 was using a vacuum pump erection device. Eleven of 18 men had had no sexual activity within 1 year of the study.

      Comment

      Nocturnal erections are a phenomena that have received little attention since the 1980s, when the relationship between the quality of nocturnal erections and volitional erections was first noted.
      • Kaneko S.
      • Bradley W.E.
      Evaluation of erectile dysfunction with continuous monitoring of penile rigidity.
      ,
      • Karacan I.
      Diagnosis of erectile impotence in diabetes mellitus an objective and specific method.
      The decline in interest was partly related to concerns stemming from reports of inhibition of NPT by psychogenic factors and abnormal NPT in men claiming normal sexual function, which led to the belief that the physiology of nocturnal erections was not pertinent to volitional erectile function.
      • Levine L.A.
      • Lenting E.L.
      Use of nocturnal penile tumescence and rigidity in the evaluation of male erectile dysfunction.
      ,
      • Wasserman M.D.
      • Pollak C.P.
      • Spielman A.J.
      • et al.
      Theoretical and technical problems in the measurement of nocturnal penile tumescence for the differential diagnosis of impotence.
      ,
      • Morales A.
      • Condra M.
      • Reid K.
      The role of nocturnal penile tumescence monitoring in the diagnosis of impotence a review.
      Despite these concerns, the neural mechanisms for nocturnal erection and volitional erection must be similar, because the final common pathway, or efferent outflow by way of the sacral nuclei and cavernous nerves, is the same. Thus, studying NPT can be useful in understanding the neurophysiology of not only nocturnal erections, but also volitional erections. Spinal cord-injured men provide a clinical experimental situation in which the spinal cord is isolated from the upper central nervous system (brain and midbrain), and, as a result, the effects of an isolated cord on NPT can be measured.
      Our primary finding was the diminished quality of nocturnal erection in men with thoracic spinal injuries compared with men with cervical spinal injuries. Lamid
      • Lamid S.
      Nocturnal penile tumescence studies in spinal cord injured males.
      found that men with high spinal injuries (tetraplegics) were more likely to have NPT on RigiScan and had greater increases in penile circumference and a longer duration of nocturnal erections than did paraplegics, but did not specify the injury level or completeness of the injury. However, although the subjects in our study with cervical injury had some “good” nocturnal erections, when compared with neurally intact, healthy men, the number, quality, and duration of the nocturnal erections were significantly reduced.
      • Levine L.A.
      • Lenting E.L.
      Use of nocturnal penile tumescence and rigidity in the evaluation of male erectile dysfunction.
      ,
      • Karacan I.
      • Hursch C.J.
      • Williams R.L.
      • et al.
      Some characteristics of nocturnal penile tumescence in young adults.
      We believe that the results of our study reflect the importance of the spinal tracts and nuclei in the regulation of nocturnal erections.

      Possible spinal mechanisms of NPT

      How does the spinal cord facilitate nocturnal erections, and what importance does this have in the physiology of volitional erections? The initiation of nocturnal erections does not appear to require intact pathways from the brain to the spinal cord, because NPT occurs in men with complete spinal cord injuries.
      • Lamid S.
      Nocturnal penile tumescence studies in spinal cord injured males.
      ,
      • Halstead L.
      • Dimitrijevic M.
      • Karacan I.
      • et al.
      Impotence in spinal cord injury neurophysiological assessment of diminished tumescence and its relation to supraspinal influences.
      Possible mechanisms include the release of central chemical or hormonal mediators during rapid eye movement (REM) sleep that activate or release inhibition of the sacral generator nuclei for erections. Direct application of peptide neurotransmitters within the spinal cord has been shown to produce erections in rats.
      • Mizusawa H.
      • Hedlund P.
      • Andersson K.E.
      Alpha-melanocyte stimulating hormone and oxytocin induced penile erections and intracavernous pressure increases in the rat.
      ,
      • Giuliano F.
      • Allard J.
      • Rampin O.
      • et al.
      Pro-erectile effect of systemic apomorphine existence of a spinal site of action.
      Another possibility includes the presence of intact, nonsomatic, bulbospinal tracts in spinal cord-injured men that allow for the transmission of impulses from the brain to the sacral spinal cord.
      • Halstead L.
      • Dimitrijevic M.
      • Karacan I.
      • et al.
      Impotence in spinal cord injury neurophysiological assessment of diminished tumescence and its relation to supraspinal influences.
      In our study, men with cervical injuries had nocturnal erections of greater frequency, rigidity, and duration than did men with thoracic injuries. If the maintenance of nocturnal erections depended on supraspinal (not spinal) mechanisms, men with cervical and thoracic injuries would have nocturnal erections of similar duration. We hypothesize that in the isolated cord, organizational neurons are present in the cervical region that modulate the neural activity in the thoracic and sacral regions to facilitate the maintenance of the erectile reflex. Spinal cord pathways act to increase the “gain” or amplification of the erectile reflex, resulting in prolongation of the erectile event, much in the same way the spinal cord acts to amplify the micturition reflex.

      Bradley WE: Physiology of the urinary bladder, in Walsh PC, Gittes RF, Perlmutter AD, et al (Eds): Campbell’s Urology, 5th ed. Philadelphia, WB Saunders, 1986, vol 1, pp 129–185

      It is possible that with a greater amount of intact spinal cord between the sacral cord/lower motor neurons and the level of injury, there is greater potential for spinal modulation of erectile activity. This explanation can also be extrapolated to volitional (non-nocturnal) erectile physiology, whereby reflex erections with genital stimulation are present in a greater percentage of men with cervical spinal injuries than in those with lower level injuries (both upper and lower motor neuron injuries).
      • Bors E.
      • Comarr A.
      Neurological disturbances of sexual function with special reference to 529 patients with spinal cord injury.
      ,

      Tsuji I, Nakajima F, Morimoto J, et al: The sexual function in patients with spinal cord injury. Urol Int 12: 270–280, 1961

      Other factors affecting NPT

      Supraspinal factors are believed to play an important role in NPT. There is a close temporal association between NPT episodes and electroencephalogram patterns of increased neural activity during REM sleep.
      • Karacan I.
      • Hursch C.J.
      • Williams R.L.
      • et al.
      Some characteristics of nocturnal penile tumescence in young adults.
      ,
      • Fisher C.
      • Gross J.
      • Zuch J.
      Cycle of penile erection synchronous with dreaming (REM) sleep.
      Karacan et al.
      • Karacan I.
      • Dervent A.
      • Salis P.
      Spinal cord injuries and NPT.
      reported that spinal cord-injured men did not exhibit the normal REM-NPT relationship after observing a random distribution of NPT episodes in several spinal cord-injured men. Schmidt et al.
      • Schmidt M.H.
      • Sakai K.
      • Valatx J.L.
      • et al.
      The effects of spinal or mesencephalic transections on sleep-related erections and ex-copula penile reflexes in the rat.
      reported an elimination of REM sleep-related erections after midthoracic spinal cord transections in rats. Although men with cervical and thoracic spinal cord injuries demonstrated NPT in our study, the erectile episodes did not follow the regular patterns typical of REM-associated NPT (three to five episodes per night, each spaced approximately 90 minutes apart; FIGURE 1, FIGURE 2).
      • Fisher C.
      • Gross J.
      • Zuch J.
      Cycle of penile erection synchronous with dreaming (REM) sleep.
      It is possible that the disruption of neural pathways between the brain and spinal cord in spinal cord injury results in a dissociation between REM sleep cycles and NPT.
      Figure thumbnail GR1
      FIGURE 1Nighttime RigiScan monitoring sessions in men with cervical injuries. Screen width = 10 hours. Horizontal line within rigidity tracing indicates 70% rigidity level. (a) Graph of 34-year-old C4 tetraplegic man with “good” erection. Arrow indicates a significant nocturnal erectile episode with 70% or greater rigidity at both tip and base lasting longer than 10 minutes. (b) Graph of 51-year-old C7 tetraplegic man with “borderline” quality erections. Multiple erectile episodes evident. Although they did not meet the 70% rigidity criteria, they approached the criteria for “good” erections and were sustained for up to 40 minutes (arrow).
      Figure thumbnail GR2
      FIGURE 2Nighttime RigiScan monitoring sessions in men with thoracic injuries. Screen width = 10 hours. Horizontal line within rigidity tracing indicates 70% rigidity level. (a) Graph of 54-year-old T3 paraplegic man. Arrows indicate brief duration events that were likely reflex erections related to stimulation during turning every 4 hours. (b) Graph of 51-year-old T9 paraplegic man with “poor” quality erections. Multiple erectile episodes were evident but of short duration and poor rigidity.

      NPT and volitional erectile function

      As evidenced by low IIEF questionnaire scores,
      • Cappelleri J.C.
      • Rosen R.C.
      • Smith M.D.
      • et al.
      Diagnostic evaluation of the erectile function domain of the International Index of Erectile Function.
      spinal cord injury has a profoundly negative impact on erectile function and sexual satisfaction. Many men with multiple sclerosis, another disease affecting the spinal cord, also report severe erectile dysfunction despite the presence of “normal” nocturnal erectile activity.
      • Yang C.C.
      • Bowen J.D.
      • Kraft G.H.
      • et al.
      Physiologic studies of male sexual dysfunction in multiple sclerosis.
      These men, like those with traumatic spinal cord injury, have been labeled as having psychogenic impotence based on the criteria from the original NPT studies,
      • Tay H.P.
      • Juma S.
      • Joseph A.C.
      Psychogenic impotence in spinal cord injury patients.
      although their difficulties with volitional erections were clearly related to spinal cord lesions. The disconnect between the erectile dysfunction reported by men with spinal lesions and the presence of adequate erectile function with NPT can be explained by the loss of somatosensory function after spinal cord injury.
      • Yang C.C.
      • Bowen J.D.
      • Kraft G.H.
      • et al.
      Physiologic studies of male sexual dysfunction in multiple sclerosis.
      Afferent somatosensory impulses by way of intact pudendal nerves are necessary for the initiation and maintenance of volitional erections.
      • Uchio E.M.
      • Yang C.C.
      • Kromm B.G.
      • et al.
      Cortical evoked responses from the perineal nerve.
      These pathways are disrupted by complete spinal cord injuries, leading to impairment of volitional erections. The initiation of nocturnal erections, however, appears to be related to supraspinal factors (discussed above) and does not depend on somatosensory afferents.

      Limitations

      No men with complete lumbosacral spinal cord injuries were present during the enrollment period of our study. As a result, we cannot comment on the possible contributions of thoracolumbar (T11–L2) pathways to NPT. Because the spinal cord ends at the L1-L2 vertebral level in adults, men with lumbosacral injuries frequently have cauda equina or conus injuries and, as a result, would not provide insight into the role of the spinal cord in NPT. Neither the presence of a urethral catheter nor a past sphincterotomy appeared to eradicate the erectile response. Three of 4 men with a history of sphincterotomy demonstrated nocturnal erectile activity on RigiScan. Finally, our cohort was too small to perform a linear regression analysis to demonstrate that progressive levels of spinal injury result in progressive loss of nocturnal erectile function, but we saw a definite trend in that direction.

      Conclusions

      Spinal regulation is critical for nocturnal erectile activity, and the isolated thoracic cord is less effective than the isolated cervical cord in maintaining NPT. Despite the presence of nocturnal erectile activity, volitional erectile function in spinal cord-injured men is significantly impaired.

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