Acquired Sexual Paraphilia in Patients with Multiple Sclerosis

OBSERVATION Acquired Sexual Paraphilia in Patients With Multiple Sclerosis

Elliot M. Frohman, MD, PhD; Teresa C. Frohman, BA; Ann M. Moreault, PhD

Background: Sexual dysfunction in patients with mul- hypothalamus and mesencephalon and extending into tiple sclerosis is typically characterized by diminished li- the right sides of the red nucleus, substantia nigra, and bido, erectile and ejaculatory dysfunction in men, and internal capsule. The altered sexual behavior was char- poor lubrication and anorgasmy in women. In contrast, acterized by an obsessive and insatiable desire to touch hypersexual behavior and paraphilias are distinctly un- women’s breasts. common in this population of patients, but have been associated with various focal brain lesions. Conclusions: Acquired sexual paraphilic behavior is uncommon in patients with multiple sclerosis but may Patient and Methods: We describe a man with clini- occur when inflammatory demyelination involves the cally definite multiple sclerosis who developed pro- hypothalamic and septal regions of the basal prosen- found and abrupt disinhibition and paraphilic behavior cephalon. Our experience with this man illustrates the during an exacerbation. great difficulty involved in treating such patients when the paraphilic behavior becomes persistent. Results: Neuroimaging revealed a marked increase in the number of enhancing lesions in the right sides of the Arch Neurol. 2002;59:1006-1010

ULTIPLE sclerosis (MS), peutically recalcitrant and eventually led a central nervous sys- to his incarceration. tem demyelinating disease, can be accom- REPORT OF A CASE panied by a broad di- versityM of neurological deficits and is the A 36-year-old right-handed man was first most common disabling neurological dis- diagnosed as having MS in 1993. At birth, order of young people. The most com- the patient had an occipital extra-axial he- mon disability involves a progressive loss matoma. In addition, he had an auditory of ambulation due to lower extremity perceptual problem in elementary school weakness and spasticity, often based on and was tutored from the age of 7 to 10 myelopathy. A host of cognitive and psy- years. He graduated from high school with chiatric manifestations have been well fair grades and dropped out of college af- documented in patients with MS. Demen- ter 11⁄2 semesters. The patient described tia,1-3 depression,4-6 bipolar affective dis- occasional marijuana use but denied al- ease,7 and fatigue-related cognitive dys- cohol abuse. Before the emergence of the function8 have all been associated with the reported aberrant sexual behavior, he had disorder. Although it has been reported no significant psychological history. that hypersexuality and paraphilic behav- The patient was well until June 1993, ior can occur with various focal brain le- when he developed an intermittent tremor sions in humans,9 these behavioral phe- of the right hand followed by right-sided nomena have been only rarely described paresis. One month later, he experienced From the Departments of in patients with MS.10,11 We describe a pa- an episode of oblique binocular diplopia. Neurology (Dr Frohman and tient with MS who developed hypersexu- A magnetic resonance imaging scan of Ms Frohman), Ophthalmology (Dr Frohman), and ality, disinhibition, and a sexual para- the brain demonstrated multifocal, high- Rehabilitation Science philia following a short-term exacerbation signal, T2-weighted white matter abnor- (Dr Moreault), The University of inflammatory demyelination involv- malities throughout the brain. These of Texas Southwestern Medical ing the preseptal region of the basal pros- occurred in the periventricular, hypotha- Center at Dallas. encephalon. These behaviors were thera- lamic, and brainstem regions (Figure 1).

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Figure 1. A, An axial proton density–weighted magnetic resonance imaging (MRI) scan demonstrates symmetric high-signal changes around the third ventricle (arrows) in the region of the hypothalamus. B, A coronal T2-weighted MRI scan demonstrates a large hyperintensity in the region of the hypothalamus, adjacent to the third ventricle, which is more prominent on the right (arrow). C, A postgadolinium T1-weighted MRI scan shows multifocal areas of enhancement in the right subinsular region, the basal ganglia, and the region of the hypothalamus.

Axial proton density–weighted images showed symmetric high-signal changes throughout the hypothalamus and septal region bilaterally (Figure 1). Coronal T2- weighted imaging revealed a large hyperintensity in the hypothalamic region adjacent to the third ventricle. T1- weighted images with gadolinium showed evidence of scattered areas of punctate enhancement in the subinsular zones, the internal capsule, the region of the hypothalamus, and the deep white matter. High-signal intensity changes observed in the mesencephalon were adjacent to a low-signal appearance of the red nuclei, substantia nigra, and superior colliculi, taking on the appearance of the “face of the giant panda” sign (Figure 2). To our knowledge, this sign has not previously been reported in patients with MS, but has been associated with Wilson disease.11 The patient’s serum ce- ruloplasmin level was tested and was within normal limits. Somatosensory evoked potentials revealed abnormal conduction velocities from the median nerve to the somatosensory cortex. Visual evoked potentials demonstrated diminished amplitudes and prolongation of P100 latencies bilaterally, indicative of an occult optic neu- ropathy. Brainstem auditory evoked potentials and elec- troencephalographic recordings were within normal limits. An analysis of the cerebrospinal fluid showed an elevated protein of 78 and 2 oligoclonal bands. A diag- Figure 2. A T2-weighted magnetic resonance imaging scan demonstrates nosis of MS was made at that time. The patient was treated mesencephalic white matter hyperintensity with areas of hypointensity in the with intravenous methylprednisolone, which was fol- red nuclei, substantia nigra, and superior colliculi, which takes on the lowed by substantial improvement. He started disease- appearance of the “face of the giant panda” sign (arrow). modifying therapy with interferon beta-1b, 8ϫ106 U sub- cutaneously every other day, but had to discontinue this pia, upper extremity tremors, episodic dysarthria, and mod- medication after several months due to his loss of medi- erate ataxia with some stumbling. He also complained of cal insurance. urinary urgency, but had no bowel or sexual dysfunc- By September 1994, he began to experience severe tion. He was treated again with methylprednisolone, 1 g/d fatigue and the reemergence of diplopia. He was em- intravenously, for 5 days. During the next month, the in- ployed in the television industry as a production engi- terferon beta-1b therapy was restarted, and no further ex- neer until he went on disability in October 1994. At that acerbations were noted until May 1995. At that time, his time, he noted a persistence of oblique binocular diplo- family observed a steady progression in behavioral de-

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 cline, characterized by poor judgment, impulsivity, and duction subtests of the Wechsler Memory Scale–Re- inappropriate sexual contact with strangers. vised. He also demonstrated some errors on measures of The patient voluntarily admitted himself, at the re- motor programming. The evaluator concluded that the quest of his family, to an inpatient psychiatric facility for patient’s findings were most consistent with a diffuse 2 weeks in July 1995. Family members reported that the pattern of subcortical brain dysfunction. patient began to have drastic changes in behavior that A brief reevaluation several months later, on Au- included approaching and asking “sexually explicit” ques- gust 8, 1995, essentially replicated the previous find- tions of strangers and masturbating 10 to 12 times per ings, with average intellectual functioning and intact day. The most troubling behavior was his inappropriate performances on traditional measures of frontal lobe actions toward women, characterized by reaching out and functioning (Wisconsin Card Sorting Test and the Book- touching their breasts. He described this as an irresist- let Category Test); however, mild difficulties were noted ible urge and said that he felt “quenched” or relieved af- on measures of oral fluency and confrontation naming. ter the act, despite recognizing how inappropriate these This evaluator concluded that the findings were consis- actions were. He felt helpless to control these actions. The tent with a diffuse demyelinating disease, such as MS. patient’s sister described him as “like a predator” in seek- However, involvement of frontal and subcortical sys- ing out women to touch their breasts. He also began to tems was also suggested by the examples of behavioral smoke cigarettes and was rarely seen without a cigarette disinhibition from the clinical history and behavioral ob- in his mouth. servations during the examination, despite the patient’s The patient presented to our MS clinic on August intact performances on more traditional tests of frontal 2, 1995, after discharge from the psychiatric facility. He dysfunction. denied visual loss, vertigo, tinnitus, hearing loss, facial Additional testing, completed on November 17, 1995, pain, alteration in facial or body sensation, and Lher- repeated measures of motor programming and the Stroop mitte and Uhthoff phenomena. However, he did have color test and added measures of olfaction. Consistent dysarthric speech. There had been no problems with with previous testing, the patient’s performance on the arthralgia, myalgia, galactorrhea, dry eyes or dry mouth, Stroop color test was within normal limits, and he made oral or genital ulceration, and alopecia. There was some perseverative and sequencing errors on tests of bi- no history of hallucinations or significant psychiatric manual programming. In addition, on a confrontation test problems. of olfactory functioning, he was only able to spontane- The cerebrospinal fluid demonstrated no oligo- ously identify 1 of 5 odors; he identified 3 of 5 when pro- clonal bands, normal VDRL test results, negative acid- vided with a multiple choice format. It was concluded, fast bacilli test results, and negative bacterial, fungal, and based on the present and previous findings and on the viral cultures. The test result for a cryptococcal antigen patient’s behavioral history, that involvement of frontal was negative. The patient did not have human T- and subcortical systems was likely and that perhaps there lymphotropic virus 1 or Lyme disease. In the cerebro- was greater involvement of orbitofrontal systems. spinal fluid, the white blood cell count was 0.07/µL; pro- Pertinent neurological examination findings in- tein level, 6.4 g/dL; glucose level, 57 mg/dL (3.2 mmol/ cluded evidence of bilateral upper extremity cerebellar L); synthesis rate, 5.1 (upper limit of normal, 3.3); and outflow tremors. There were slow alternating move- IgG index, 0.63 (upper limit of normal, 0.58). Thyroid ments and finger sequences, with some irregularity in the function test results were normal. The testosterone level right hand vs the left. Rhythm tapping was slow, again was low at 163 ng/dL (5.7 nmol/L) (normal range, 300- more prominent in the right hand compared with the left. 1200 ng/dL [10.4-41.6 nmol/L]). A follow-up magnetic Heel-to-shin testing demonstrated mild bilateral ataxia. resonance imaging scan demonstrated severe lesions in There was no evidence of dysdiadochokinesia. Reflexes the region of the hypothalamus and the septal region, as were 2+ and symmetric. Sensory examination results were previously observed. intact to pinprick, temperature, vibratory sense, and pro- The patient participated in neuropsychological test- prioception. ing on 3 separate occasions in 1995. The first examina- During the following year, the patient had periods tion, on January 11, 1995, revealed the presence of mild of excellent behavioral control, punctuated by episodes cognitive impairments within the context of average in- of impulsivity, sexual disinhibition, and inappropriate so- tellectual functioning, as measured by the Wechsler Adult cial contact. Therapy with a combination of fluvox- Intelligence Scale–Revised. His performance on typical amine maleate and medroxyprogesterone acetate, 400 mg/ measures of frontal lobe functioning, such as the Wis- wk, was started to treat the aberrant sexual urges and consin Card Sorting Test, the Booklet Category Test, and fatigue. The patient, and his caregivers, noted improve- the Stroop color test, was intact. He also demonstrated ment in his behavioral control and his obsessive- intact performances on structured tests of verbal memory compulsive tendencies to touch women’s breasts. (Wechsler Memory Scale Revised–Logical Memory), at- After approximately 9 months, the patient devel- tention and concentration, and basic language skills. In oped refractory orthostatic hypotension. A medical contrast, on less structured measures of memory, such work-up failed to reveal any underlying causes. All medi- as the list-learning task of the California Verbal Learn- cations, except interferon beta-1b, were discontinued and ing Test, his performance was impaired due to perse- the orthostasis resolved. verative errors, intrusions, and false-positive errors. His Before his exacerbative episode in May 1995, this memory for visual material was mildly reduced on the man had no history of sexually abnormal behavior. He Rey Osterrieth Complex Figure and the Visual Repro- held a steady job, was involved in a steady relationship,

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 and did not smoke cigarettes. However, during the 10 edge, there has not been a documented case in the lit- months following this exacerbation, he manifested a sexual erature that describes aberrant sexual behavior attrib- paraphilia, incessant masturbation, chain-smoking, im- uted to ventriculoperitoneal shunts without septal injury. pulsivity, and extremely poor judgment. He accosted sev- Septal lesions and sexual stimulation have been de- eral women in group homes that he was placed in and scribed in several animal species. Animal studies pro- female nurses at the hospital. He disabled the alarm in vide most of the knowledge that we have about the re- the group home so that he was able to go out unnoticed, lationship between regional brain function (predominantly and was subsequently located 40 hours later. During this the septal zone) and sexual response. Copulatory behav- time, he propositioned a 12-year-old girl in a movie the- ior can be induced in primates16 and rats17 by stimulat- ater, and then he sexually assaulted a second minor and ing the septal region. another woman. Charges were brought against him, and Disinhibition syndromes involving hypersexuality he was eventually incarcerated. have also been reported in humans who experienced damage to the orbitofrontal cortex. Starkstein and Kremer18 COMMENT reviewed several studies that highlight the importance of the integrity of the orbitofrontal cortex and its asso- Although paraphilias are uncommon, hypersexuality and ciated circuitry, which projects to the septum, hypo- paraphilic behavior are associated with several focal brain thalamus, and mesencephalon to maintain inhibitory con- lesions, especially those that involve loss of integrity of trol over such behaviors and eating, sexuality, and the frontal lobes and diencephalic structures.12 Idio- aggression. Despite the similarity in description be- pathic paraphilias almost always begin in childhood, ado- tween our patient’s disinhibition and that of individuals lescence, or early adulthood, but rarely occur with new with orbitofrontal damage, our patient performed nor- onset after the age of 30 years. Acquired paraphilias, in mally on several traditional neuropsychological mea- contrast, seem to be associated with focal brain injury, sures of frontal lobe functioning. This finding was not particularly in the frontal lobe, hypothalamic area, and surprising given the fact that many of these measures septal nuclei.13 are relatively insensitive to damage in the orbitofrontal Temporal lobe structures have an important role in region; in fact, the Wisconsin Card Sorting Test is sen- sexual behavior. In patients with the Klu¨ ver-Bucy syn- sitive to dorsolateral prefrontal damage rather than or- drome, a disorder caused by bilateral temporal lobe bitofrontal damage.19 dysfunction, sexual overtures, masturbation, and at- Humans who develop damage to the prefrontal tempted sexual contact are characteristic.14 Paraphilias cortex frequently exhibit defects in decision making have been associated with several other neurological dis- despite intact intellectual skills.20 Similar to our patient, eases, such as epilepsy, postencephalitic parkinsonism, these individuals seem to make behavioral choices that hypoxic brain injury, and hypothalamic tumors.9 Huws are harmful, despite the knowledge that negative conse- et al10 described a young man with MS who developed quences may occur. To explore the possible neural ba- hypersexuality and fetishism, which eventually led to his sis for this defect, an experimental paradigm called the imprisonment. A magnetic resonance imaging scan gambling task was developed by Bechara and col- showed periventricular and frontal damage. In another leagues.21 In this task, the subject is placed in a position report, hypersexuality and paraphilia were reported in a of making choices that could result in either immediate woman with MS, whose aberrant behavior included ex- short-term gains with long-term negative consequences hibitionism, incest, scopophilia, and zoophilia. She even- or a net gain over time with a lower level of reward. The tually was arrested on multiple accounts of sexual mis- task was designed so that the solution to avoiding long- conduct. She ultimately died while in jail, and an autopsy term negative consequences was easily acquired after sev- demonstrated severe demyelination in the frontal, tha- eral trials; thus, most healthy subjects showed no im- lamic, and mesencephalic regions.13 pairment in performing the task. However, studies22-25 Previous literature has suggested that the septal re- using this paradigm revealed that subjects with ventro- gion of humans is important in mediating the human medial prefrontal damage were impaired on the gam- sexual response. Two patients who underwent ventricu- bling task, ie, they consistently made poor choices and loperitoneal shunt revision for normal-pressure hydro- took risks despite their knowledge that it would even- cephalus demonstrated abnormal sexual behavior after tually lead to a negative outcome. In contrast, individu- the shunts were placed. Both patients made sexually ex- als with dorsolateral prefrontal damage consistently per- plicit comments toward women, tried to fondle the fe- formed in the normal range on this task. Thus, it seems male nurses, and masturbated in public. A computed to- that this paradigm shows some promise in distinguish- mographic scan later showed that, in one case, the tip of ing between different types of prefrontal damage, and may the catheter was lodged in the septum in the medial as- explain why some individuals perform in the normal range pect of the floor of the lateral ventricles at the junction on some frontal lobe measures despite the evidence of of the frontal horns. In the second case, a computed to- clearly disinhibited behavior. Additional research using mographic scan revealed that the catheter tip had been this experimental task is warranted to develop norma- inserted into the midline anterior hypothalamic-septal tive data on more subjects and to further explore its util- structures.15 Neither of these men displayed atypical sexual ity in the diagnosis and treatment of individuals with pre- behavior before shunt revision. Miller et al9 also report frontal damage. of a malpositioned shunt inserted into the septal region The complexity of the human sexual response and that resulted in intense sexual disinhibition. To our knowl- the neural basis for such response is poorly understood.

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 Arousal in humans is highly linked to structures with ex- REFERENCES tensive frontal and limbic connections. Several changes in sexual behavior have been reported as a result of dam- 1. Beatty PA, Gange JJ. Neuropsychological aspects of multiple sclerosis. J Nerv age to the frontal cortex, hypothalamus, and amygda- Ment Dis. 1977;164:42-50. loid nuclei.13 All of these regions have major anatomic 2. Peyser JM, Edwards KR, Poser CM, Filskov SB. Cognitive function in patients with multiple sclerosis. Arch Neurol. 1980;37:577-579. connections to the septal region and, taken together, de- 3. Ron MA, Feinstein A. Multiple sclerosis and the mind. J Neurol Neurosurg Psy- 15 fine a circuit of structures mediating sexual behavior. chiatry. 1992;55:1-3. Sexual behavior may be increased or decreased depend- 4. Joffe RT, Lipert GP, Gray TA, Sawa G, Horvath Z. 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Deciding advantageously before This study was supported by the National Multiple Scle- knowing the advantageous strategy. Science. 1997;275:1293-1295. rosis Society, New York, NY (Dr Frohman), and the Yel- 24. Bechara A, Damasio H, Tranel D, Damasio AR. Dissociation of working memory low Rose Foundation (Dr Frohman) and the Hawn Foun- from decision making within the human prefrontal cortex. J Neurosci. 1998;18: dation (Dr Frohman), Dallas, Tex. 428-437. Corresponding author and reprints: Elliot M. Frohman, 25. Bechara A, Damasio H, Damasio AR, Lee GP. Different contributions of the human amygdala and ventromedial cortex to decision making. J Neurosci. 1999; MD, PhD, Department of Neurology, The University of Texas 19:5473-5481. Southwestern Medical Center at Dallas, 5323 Harry Hines 26. Rosler A, Witzum E. Treatment of men with paraphilia with a long-acting ana- Blvd, Dallas, TX 75235 (e-mail: [email protected]). logue of gonadotropin-releasing hormone. 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