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COPROLALIA AND OTHER COPROPHENOMENA

  • Author Footnotes
    * From the Movement Disorders Clinic, Department of Neurology, University of Miami School of Medicine, Miami, Florida
    Carlos Singer
    Footnotes
    * From the Movement Disorders Clinic, Department of Neurology, University of Miami School of Medicine, Miami, Florida
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  • Author Footnotes
    * From the Movement Disorders Clinic, Department of Neurology, University of Miami School of Medicine, Miami, Florida
      In his original 1885 description of the syndrome, Gilles de la Tourette emphasized the triad of multiple tics, coprolalia, and echolalia.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      Although current diagnostic criteria do not include coprolalia as a necessary component of Tourette syndrome (TS),
      • Shapiro A.K.
      • Shapiro E.
      An update of Tourette syndrome.
      its presence is highly indicative, albeit not pathognomonic, of this condition.
      Coprolalia is the uncontrollable utterance of obscenities and profanities. Obscenities are defined as utterances describing sexual acts, body function or elimination acts, and organs of reproduction and sexual anatomy.
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      Profane utterances, on the other hand, convey a religious connotation.
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      In reality, the spectrum of these socially inappropriate utterances also includes references to animals (e.g., bitch, bull, pig)
      • Bruun R.D.
      • Budman C.L.
      The natural history of Tourette syndrome.
      and racial epithets.
      • Scott B.L.
      • Jankovic J.
      • Donovan D.T.
      Botulinum toxin injection into vocal cord in the treatment of malignant coprolalia associated with Tourette's syndrome.
      Coprolalia is the most common of the so-called coprophenomena, which also include copropraxia, or the uncontrollable performance of obscene gestures, mental coprolalia, or obsessive thinking of obscenities and profanities, and coprographia, or the compulsion to write down such expressions. Coprolalia and copropraxia are among the most socially disabling of the symptoms seen in TS.
      • Golden G.
      Tourette syndrome: The pediatric perspective.
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.
      This review focuses attention on a variety of aspects of coprophenomena, pointing out those areas clearly in need of further study.

      HISTORIC ASPECTS

      Tic disorders have been linked to prominent historic figures such as Napoleon, Moliere, Mozart, and Peter the Great.
      • Lees A.J.
      Some celebrated ticqueurs.
      Perhaps one of the best characterized was the case of Dr. Samuel Johnson.
      • Lees A.J.
      Some celebrated ticqueurs.
      Although he was affected by a variety of dramatic and complex motor tics, compulsions, and echolalia, he was apparently spared the burden of coprolalia. On the other hand, historic investigation of Mozart's private letters has highlighted the possible presence of coprophenomena (particularly coprographia) and has been used as argument that Mozart suffered from this disorder.
      • Simkin B.
      Mozart's scatological disorder.
      The earliest medical description of TS has been traced to 60 years before Gilles de la Tourette's seminal description, and it included coprolalia as one of its components. Jean-Marc Itard described the case of the Marquise de Dampierre who barked, repeated words, and uttered offensive words and obscene sayings.
      • Shapiro A.K.
      • Shapiro E.S.
      • Young J.G.
      • et al.
      History of Tourette and Tic disorders.
      The result was a reclusive existence until the patient's death at the age of 85 years.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      Subsequently, this patient was included with eight others in Gilles de la Tourette's original paper.
      • Erenberg G.
      • Cruse R.P.
      • Rothner A.D.
      Tourette syndrome: An analysis of 200 pediatric and adolescent cases.
      • Shapiro A.K.
      • Shapiro E.S.
      • Young J.G.
      • et al.
      History of Tourette and Tic disorders.
      Only five of Tourette's nine patients exhibited coprolalia. Tourette also observed that echolalia and coprolalia could appear years after the motor tics, and he considered the presence of coprolalia as pathognomonic of the syndrome.
      Initially, Tourette was impressed with his patients' preserved mental health and agreed with others, including Charcot and Trousseau, that the disease was hereditary. In 1899, he revised his views, advocating coprolalia as a sign of “psychic stigma.” Freud also contributed to the notion of the psychological origin of the disorder, interpreting coprolalia as the result of a self-fulfilling fear of being unable to repress the utterance of obscene words. Views such as these evolved into a variety of psychoanalytic interpretations of the origin of TS that prevailed through the first half of this century.
      • Shapiro A.K.
      • Shapiro E.S.
      • Young J.G.
      • et al.
      History of Tourette and Tic disorders.
      In the 1950s the pendulum began to swing back to an organic view of the etiology of TS, based on large epidemiologic studies and on successful use of dopamine-blocking agents for the symptomatic treatment of TS.
      • Shapiro A.K.
      • Shapiro E.S.
      • Young J.G.
      • et al.
      History of Tourette and Tic disorders.
      This historical evolution has parallelled the increasing recognition that several disorders of behavior frequently associated with TS, such as obsessive-compulsi ve disorders (OCD) and attention deficit hyperactivity disorders (ADHD) are biologically determined.

      PREVALENCE

      Reported prevalence figures for coprolalia have ranged from single-digit percentage numbers to over two thirds in different series.
      • Bruun R.D.
      • Budman C.L.
      The natural history of Tourette syndrome.
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.
      • Jankovic J.
      • Rohaidy H.
      Motor, behavioral and pharmacologic findings in Tourette's syndrome.
      • Kurlan R.
      • Behr J.
      • Medved L.
      • et al.
      Familial Tourette's syndrome: Report of a large pedigree and potential for linkage analysis.
      • Micheli F.
      • Gatto M.
      • Gershanik O.
      • et al.
      Gilles de la Tourette syndrome: Clinical features of 75 cases from Argentina.
      • Nee L.E.
      • Polinsky R.J.
      • Ebert M.H.
      Tourette syndrome: Clinical and family studies.
      • Nomura Y.
      • Segawa M.
      Tourette syndrome in Oriental children: Clinical and pathophysiological considerations.
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      • Robertson M.M.
      • Trimble M.R.
      • Lees A.J.
      The psychopathology of the Gilles de la Tourette syndrome.
      • Shapiro A.K.
      • Shapiro E.S.
      • Young J.G.
      • et al.
      History of Tourette and Tic disorders.
      Cultural factors and selection bias may help to explain these disparities. Copropraxia is less common than coprolalia
      • Jankovic J.
      • Rohaidy H.
      Motor, behavioral and pharmacologic findings in Tourette's syndrome.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      • Robertson M.M.
      • Trimble M.R.
      • Lees A.J.
      The psychopathology of the Gilles de la Tourette syndrome.
      and is rarely present in the absence of the latter.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      • Robertson M.M.
      • Trimble M.R.
      • Lees A.J.
      The psychopathology of the Gilles de la Tourette syndrome.
      Jankovic
      • Jankovic J.
      • Rohaidy H.
      Motor, behavioral and pharmacologic findings in Tourette's syndrome.
      called attention to a high male-to-female ratio in his series, with numbers of 4.4 for coprolalia and 20:1 for copropraxia.
      Studies from Japan have reported a prevalence of coprolalia of only 4%.
      • Nomura Y.
      • Segawa M.
      Tourette syndrome in Oriental children: Clinical and pathophysiological considerations.
      This has led to the suggestion that cultural factors may act as modifiers for the manifestation of this symptom.
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      It should be noted, however, that an additional 14% of patients exhibited so-called quasi-coprolalia, which this author interprets as involuntary utterances modified so as to hide their sexual connotation.
      Variability also has been found when comparing results from kindred studies.
      • Kurlan R.
      • Behr J.
      • Medved L.
      • et al.
      Familial Tourette's syndrome: Report of a large pedigree and potential for linkage analysis.
      • McMahon W.M.
      • Leppert M.
      • Filoux F.
      • et al.
      Tourette symptoms in 161 related family members.
      Kurlan reported on a large Mennonite kindred affected with chronic motor tics and vocal tics in a probable autosomal dominant pattern. Twenty-nine subjects were identified as suffering from TS or chronic motor tics. Five of them (17%) had coprolalia.
      • Kurlan R.
      • Behr J.
      • Medved L.
      • et al.
      Familial Tourette's syndrome: Report of a large pedigree and potential for linkage analysis.
      In contrast, McMahon found only 2 of 47 (4%) affected members in a large Nevada kindred.
      • McMahon W.M.
      • Leppert M.
      • Filoux F.
      • et al.
      Tourette symptoms in 161 related family members.
      If one analyzes prevalence figures according to the level of specialization of the reporting clinic, tertiary referral centers exhibit a higher prevalence of coprophenomena
      • Golden G.
      Tourette syndrome: The pediatric perspective.
      • Jankovic J.
      • Rohaidy H.
      Motor, behavioral and pharmacologic findings in Tourette's syndrome.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      • Micheli F.
      • Gatto M.
      • Gershanik O.
      • et al.
      Gilles de la Tourette syndrome: Clinical features of 75 cases from Argentina.
      • Nee L.E.
      • Polinsky R.J.
      • Ebert M.H.
      Tourette syndrome: Clinical and family studies.
      • Robertson M.M.
      • Trimble M.R.
      • Lees A.J.
      The psychopathology of the Gilles de la Tourette syndrome.
      • Shapiro A.K.
      • Shapiro E.
      An update of Tourette syndrome.
      when compared with primary pediatric practices.
      • Erenberg G.
      • Cruse R.P.
      • Rothner A.D.
      Tourette syndrome: An analysis of 200 pediatric and adolescent cases.
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.
      This difference may not be surprising, because relatively mild cases, presumably less socially disabling and therefore free from coprolalia, may never be referred to a tertiary referral center.
      Figures for coprolalia reported from university centers within the last 20 years range from 27% to 39%
      • Jankovic J.
      • Rohaidy H.
      Motor, behavioral and pharmacologic findings in Tourette's syndrome.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      and for copropraxia from 7%
      • Golden G.
      Tourette syndrome: The pediatric perspective.
      to 21%.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      In contrast, analysis of two primary pediatric practices reveals a prevalence of coprolalia of only 8%.
      • Erenberg G.
      • Cruse R.P.
      • Rothner A.D.
      Tourette syndrome: An analysis of 200 pediatric and adolescent cases.
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.
      The discrepancy in prevalence figures between primary and tertiary care centers points to coprolalia as a measure of severity of TS, a view shared by some authors.
      • Erenberg G.
      • Cruse R.P.
      • Rothner A.D.
      Tourette syndrome: An analysis of 200 pediatric and adolescent cases.
      • Shapiro A.K.
      • Shapiro E.
      An update of Tourette syndrome.
      Shapiro and Shapiro felt that over the years the frequency of coprolalia had diminished in their series as the identification of many patients with less severe symptomatology had increased. Nevertheless, although severity of TS (as manifested by severity of tics or severity of associated behavioral disorders) may correlate with the presence of coprolalia. There are many instances of patients with relatively mild motor tics and severe coprolalia.
      Very little data can be obtained regarding prevalence of other coprophenomena. Golden reported that 3 of his 15 patients (20%) had mental coprolalia
      • Golden G.
      Tourette syndrome: The pediatric perspective.
      whereas Jankovic et al
      • Jankovic J.
      • Rohaidy H.
      Motor, behavioral and pharmacologic findings in Tourette's syndrome.
      and Micheli et al
      • Micheli F.
      • Gatto M.
      • Gershanik O.
      • et al.
      Gilles de la Tourette syndrome: Clinical features of 75 cases from Argentina.
      found it in 4% to 5% of their cases. We have found no prevalence data for coprographia.

      ONSET

      Coprolalia is rarely present at the onset of the disease. Coprolalia is seen as the presenting symptom of TS in only 1 to 1.4% of their series.
      • Bruun R.D.
      • Budman C.L.
      The natural history of Tourette syndrome.
      • Shapiro A.K.
      • Shapiro E.
      An update of Tourette syndrome.
      Most commonly coprolalia follows the onset of motor or phonic tics by a few years, on the average 4 to 7 years later.
      • Bruun R.D.
      • Budman C.L.
      The natural history of Tourette syndrome.
      Two sequential British studies from the same referral center group
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      • Micheli F.
      • Gatto M.
      • Gershanik O.
      • et al.
      Gilles de la Tourette syndrome: Clinical features of 75 cases from Argentina.
      revealed a mean age of onset of coprolalia between 14.5 and 15.1 years, with the youngest age that of 6 years,
      • Robertson M.M.
      • Trimble M.R.
      • Lees A.J.
      The psychopathology of the Gilles de la Tourette syndrome.
      whereas the mean age of onset of tics was 7 years (range 7-16 years) and that of vocalizations 11 years (range 4-33 years). Goldenberg, reporting on a primary care practice sample found a substantially younger mean age at onset of coprolalia of 9.1 years (range 6-16 years).
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.
      The onset of TS symptoms had occurred at a mean age of 6.9 years (range 2-14 years).

      NATURAL HISTORY

      The natural history of TS is variable, with most patients reporting symptomatic improvement as they enter adulthood.
      • Bruun R.D.
      Course and prognosis of Tourette's syndrome.
      • Bruun R.D.
      • Budman C.L.
      The natural history of Tourette syndrome.
      • Erenberg G.
      • Cruse R.P.
      • Rothner A.D.
      The natural history of Tourette syndrome: A follow-up study.
      • Goetz C.G.
      • Tanner C.M.
      • Stebbins G.T.
      • et al.
      Adult tics in Gilles de la Tourette's syndrome: Description and risk factors.
      Associated problems (e.g., OCD, ADHD, and a variety of other behavioral problems) however, may persist.
      • Bruun R.D.
      • Budman C.L.
      The natural history of Tourette syndrome.
      There is very little data on the effect of aging on TS, although most studies provide evidence that symptoms gradually improve after the first decades of life.
      • Bruun R.D.
      • Budman C.L.
      The natural history of Tourette syndrome.
      Goetz, in a study of 58 adults with TS diagnosed during childhood,
      • Goetz C.G.
      • Tanner C.M.
      • Stebbins G.T.
      • et al.
      Adult tics in Gilles de la Tourette's syndrome: Description and risk factors.
      found coprolalia present in 4%, compared with 22% at the time of worst function, which would occur mostly in adolescence (mean 13 years). This finding would suggest a gradual increase in coprolalia until the age of peak production, followed by a period of decline throughout adulthood, parallelling the decline in vocalizations in general that occurs after adolescence.
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.

      ASSOCIATIONS

      There appears to be a significant link between some of the features of TS (e.g., coprolalia, copropraxia, echophenomena) and the expression of aggression, hostility, and obsessionality.
      • Robertson M.M.
      • Trimble M.R.
      • Lees A.J.
      The psychopathology of the Gilles de la Tourette syndrome.
      • Trimble M.
      Psychopathology and movement disorders: A new perspective on the Gilles de la Tourette syndrome.
      Robertson et al
      • Robertson M.M.
      • Trimble M.R.
      • Lees A.J.
      The psychopathology of the Gilles de la Tourette syndrome.
      found several features to be significantly related to coprophenomena. In the case of coprolalia these included cumulative number of vocalizations, copropraxia, feeling forced to touch, echolalia, echopraxia, self-injury, and abnormal gait. In the case of copropraxia, the features were cumulative number of vocalizations, aggressive behavior, abnormal gait, and feeling forced to touch.
      Moreover, the total scores and one of the subscores of an obsessionality scale (the Leyton Obsessional Inventory total score and the Leyton Obsessional Inventory symptom subscore) were significantly related to coprolalia. Coprolalia also was associated with a number of subscales of the Hostility and Direction of Hostility Questionnaire (HDHQ).

      PHENOMENOLOGY

      Patients affected with coprolalia or copropraxia experience an urge to utter obscenities
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      or perform obscene gestures
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      respectively, in a fashion similar to the urge TS patients experience preceding their phonatory or motor tics. This has generated the view by some that these coprophenomena actually represent complex phonatory or motor tics. The utterances occur without any provoking cause, although stressful situations can make them occur more frequently.
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      Four-letter words focused on anatomy, and sexual and bodily function were the most common both in the British
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      and in the American studies (Table 1)
      Table 1COMMON COPROLALIC UTTERANCES IN SIX COUNTRIES
      USAUK
      Lees AJ 1984.
      Denmark
      Reuger L et al 1986.
      Spain
      Goldenberg et al 1994.6
      Hong Kong
      Goldenberg et al 1994.6
      Japan
      Goldenberg et al 1994.6
      Fuck, (-er, -off)
      Goldenberg et al 1994.6
      Jankovic and Rohaidy 1987.14
      Shapiro AK et al 1978.23
      Nuwer 1982.13
      FuckKaeft (shut up)Puta (whore)Tiu (fuck)Kusobaba (shit grandma)
      Shit
      Goldenberg et al 1994.6
      Jankovic and Rohaidy 1987.14
      Shapiro AK et al 1978.23
      Nuwer 1982.13
      CuntSvin (swine)Mierda (feces)Shui (useless person)Chikusho (son of a bitch)
      Bitch
      Goldenberg et al 1994.6
      Jankovic and Rohaidy 1987.14
      Shapiro AK et al 1978.23
      Nuwer 1982.13
      BastardFisse (vulva)Coño (vulva)Tiu ma (mother fucker)Omanko (female genitalia and breasts)
      Ass(hole)
      Goldenberg et al 1994.6
      Jankovic and Rohaidy 1987.14
      Nuwer 1982.13
      PissKusse (vulva)Joder (fornicate)Tiu so (aunt fucker)
      Bastard
      Goldenberg et al 1994.6
      Jankovic and Rohaidy 1987.14
      SodPik (penis)Maricon (homosexual)
      Pussy
      Jankovic and Rohaidy 1987.14
      CockRov (ass)Cojones (testicles)
      Prick, dick, cock (sucker)
      Shapiro AK et al 1978.23
      Nuwer 1982.13
      ShitPis (ass)Hijo de puta (son of a whore)
      Cunt
      Shapiro AK et al 1978.23
      Gylle (animal feces)Hostia (holy bread)
      Fart
      Nuwer 1982.13
      Sgu (by God)
      Nigger
      Shapiro AK et al 1978.23
      Lort (shit)
      * Goldenberg et al 1994.
      • Caine E.D.
      • Polinsky R.J.
      • Ludlow C.L.
      • et al.
      Heterogeneity and variability in Tourette syndrome.
      Jankovic and Rohaidy 1987.
      • Hassler R.
      • Dieckmann G.
      Traitment stéreotaxique des tics et cris inarticules ou coprolaliques considerés comme phénomêne d'obsession motrice au cours de la maladie de Gilles de la Tourette.
      Shapiro AK et al 1978.
      • Leckman J.F.
      • Hardin M.T.
      • Riddle M.A.
      • et al.
      § Nuwer 1982.
      • Goetz C.G.
      • Tanner C.M.
      • Stebbins G.T.
      • et al.
      Adult tics in Gilles de la Tourette's syndrome: Description and risk factors.
      Lees AJ 1984.
      Reuger L et al 1986.
      . These words usually appear during pauses between sentences and are uttered in a loud sharp tone that contrasts with the intonation of the ongoing conversation,
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      or they may be slurred and only partially pronounced.
      • Jankovic J.
      • Rohaidy H.
      Motor, behavioral and pharmacologic findings in Tourette's syndrome.
      Patients may try unsuccessfully to disguise them with euphemisms and neologisms.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      This preferential involvement of body- or sex-focused utterances seen in TS contrast with nonaffected people, who will tend to use such utterances in equal proportion with religious profanities.
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.
      Copropraxic gestures will vary from culture to culture. In the UK series the palm-backed V sign (something with no meaning in the US) was the commonest. Additional acts included the forearm jerk with the fist clenched, the clenched fist with an extended finger, and rhythmic hand movements and pelvic thrusting simulating a masturbatory act. Nonobscene gestures such as thumbs-up and victory sign also may be seen. Counterpart American studies have not provided descriptive information on copropraxic phenomena.
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.
      • Jankovic J.
      • Rohaidy H.
      Motor, behavioral and pharmacologic findings in Tourette's syndrome.

      PATHOPHYSIOLOGY

      The current view of TS as an organic disorder involving central dopaminergic mechanisms and disruption of normal striatal and limbic functions
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      has followed years of psychological interpretations of this disorder, during which coprolalia was actually used as an argument in support of the psychogenicity of TS.
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      Once it became apparent that coprolalia can be present within the context of well-defined organic disorders, such reasoning had to give way to alternative views. For instance, coprolalia may be seen in general paresis,
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      in “senility,”
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      as a sequelae of encephalitis lethargica,
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      in vasculogenic hemiballismus, and in brain tumors, and is sometimes reversible with medical
      • Marti-Masso J.F.
      • Obeso J.A.
      Coprolalia associated with hemiballismus: response to tetrabenazine.
      or surgical
      • Hassler R.
      • Dieckmann G.
      Traitment stéreotaxique des tics et cris inarticules ou coprolaliques considerés comme phénomêne d'obsession motrice au cours de la maladie de Gilles de la Tourette.
      treatment.
      Based on the premise that the basal ganglia are functionally composed of multiple parallel corticostriatothala mocortical (CSTC) circuits that concurrently subserve a wide variety of sensorimotor, cognitive, and limbic processes,
      • Leckman J.F.
      • Pauls D.L.
      • Peterson B.
      • et al.
      Pathogenesis of Tourette syndrome: Clues from the clinical phenotype and natural history.
      Leckman advanced the hypothesis that TS (and etiologically related forms of OCD) may be associated with a failure to inhibit subsets of CSTC minicircuits.
      • Leckman J.F.
      • Hardin M.T.
      • Riddle M.A.
      • et al.
      • Leckman J.F.
      • Pauls D.L.
      • Peterson B.
      • et al.
      Pathogenesis of Tourette syndrome: Clues from the clinical phenotype and natural history.
      Such circuits may be influenced by neurochemical systems originating in the brain stem and mediated by dopamine, serotonin, and norepinephrine.
      • Caine E.D.
      • Polinsky R.J.
      • Ludlow C.L.
      • et al.
      Heterogeneity and variability in Tourette syndrome.
      The observation that occasionally patients with severe aphasia following a stroke still may utter obscenities
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      even as word substitutions
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      could be interpreted as a manifestation of such a short-circuited pathway.
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      Obsessions with aggressive and sexual themes—such as can be seen in TS—could be associated with failure to inhibit portions of the limbic minicircuits
      • Leckman J.F.
      • Pauls D.L.
      • Peterson B.
      • et al.
      Pathogenesis of Tourette syndrome: Clues from the clinical phenotype and natural history.
      and perhaps coprolalia could be viewed similarly. In support of the idea that coprolalia may represent a manifestation of OCD, there is at least one report in which coprolalia occurred in a subject without coexistent TS (although he did experience transient motor tics) and was preceded by obsessive thoughts (mental coprolalia) that the patient unsuccessfully attempted to suppress.
      • Pitman R.K.
      • Jenike M.A.
      Coprolalia in obsessive-compulsi ve disorder: A missing link.
      In his comprehensive review on the subject, Nuwer
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      advanced several considerations in support of the notion of the organic origin of coprolalia. He pointed out that coprolalic utterances frequently would display unusual pitch and volume, sometimes with imprecise pronunciation of individual phonemes, and clearly differed from instances in which the same phonemes were used by nonaffected persons in ordinary speech, that is, by lacking the expected emotional intonation.
      In the coprolalia of TS—in contradistinction to nonaffected personsfour-letter obscenities (defined here as swear words relating to copulation, defecation, or micturition) predominate over religious profanities (e.g., God, hell, and damn). One could speculate that separate neuroanatomic pathways for both categories may exist and the one with the more taboo-loaded utterances (four-letter obscenities) is more likely to be dysfunctional in TS. This “dysfunctional center” or “short-circuited pathway” would then release the undesired utterances, superimposing them on the conversational flow of desired speech.
      An alternative explanation to the presence of a specific neroanatomic pathway subserving obscenities is presented by Bennet's finding, as quoted by Nuwer, that these obscenities—a nd not the profanities— are frequently produced in English and German by computer programs that generate letters or “spoken phonemes” using a so-called Markov process.
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      Such a process involves random strings of letters or phoneme generation based on grades of probability for each letter or spoken phoneme as applied to the particular language. Coprolalia in TS therefore could be viewed as resulting from a short circuit in brain functioning that produces high-probability strings of phonemes out of proportion to other words.
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      Kurlan has postulated that brain regions involved in TS (basal ganglia and limbic system) are counterparts in humans of those regions functioning in primitive (mammalians, birds, fish) reproductive behavior, the development and organization of which are under sex control.
      • Kurlan R.
      The pathogenesis of Tourette's syndrome: A possible role for hormonal and excitatory neurotransmitter influences in brain development.
      Motor tics, phonatory tics, and coprolalic utterances could represent fragments of primitive motor and vocal programs involved in reproductive activity that are inappropriately expressed as a result of a dysfunction in such regions.
      This hypothesis would be in agreement with Nuwer
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      in his work on high-probability phonemes or with Burd on his work on nocturnal coprolalia
      • Burd L.
      • Kerbeshian J.
      Nocturnal coprolalia and phonic tics letter.
      in that they all see coprolalia as part of the motor and phonatory tic continuum. An alternative view would be represented by Pitman's report, in which coprolalia is seen as part of the spectrum of the OCD.
      • Pitman R.K.
      • Jenike M.A.
      Coprolalia in obsessive-compulsi ve disorder: A missing link.

      DIFFERENTIAL DIAGNOSIS

      TS may be not only familial but also seen in mentally retarded subjects with diffuse brain damage, patients with hyperekplexia, neuroacanthocytosi s, and drug-induced dyskinesias. Outside of these instances of secondary TS (also known as secondary tourettism), coprolalia has been observed in a few well documented cases of Sydenham's chorea
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      and hemiballismus
      • Marti-Masso J.F.
      • Obeso J.A.
      Coprolalia associated with hemiballismus: response to tetrabenazine.
      but the distinction of motor tics from choreiform or ballistic movements should not be difficult.
      Startle syndromes such as latah, myryachit, and the “jumping Frenchmen of Maine” are “characterized by the association of startle myoclonus with echolalia, coprolalia, or automatic obedience”
      • Lees A.J.
      • Robertson M.
      • Trimble M.R.
      • et al.
      A clinical study of Gilles de la Tourette syndrome in the United Kingdom.
      or an exaggerated startle, often exclaiming normally inhibited sexually denotative words, with occasional automatic obedience or imitation of actions of persons about the affected person.
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      In klazomania, a rare sequelae to encephalitis lethargica, coprolalia may accompany jerking, shaking, writhing, and other ticlike movements, as well as other symptoms.
      • Nuwer M.R.
      Coprolalia as an organic symptom.
      It also has been reported in OCDs independently of coexistence of TS.
      • Pitman R.K.
      • Jenike M.A.
      Coprolalia in obsessive-compulsi ve disorder: A missing link.

      TREATMENT

      Pharmacology

      When one analyzes reports
      • Bruun R.D.
      • Shapiro A.K.
      • Shapiro E.
      • et al.
      A follow-up of 78 patients with Gilles de la Tourette's syndrome.
      • Goldenberg J.N.
      • Brown S.B.
      • Weiner W.J.
      Coprolalia in younger patients with Gilles de la Tourette syndrome.
      • Ratzoni G.
      • Hermesh H.
      • Brandt N.
      • et al.
      Clomipramine efficacy for tics, obsessions, and compulsions in Tourette's syndrome and obsessive-compulsi ve disorder: A case study.
      • Regeur L.
      • Pakkenberg B.
      • Fog R.
      • et al.
      Clinical features and long-term treatment with pimozide in 65 patients with Gilles de la Tourette's syndrome.
      • Ross M.S.
      • Moldofsky H.
      A comparison of pimozide and haloperidol in the treatment of Gilles de la Tourette' syndrome.
      • Shapiro A.K.
      • Shapiro E.
      Controlled study of pimozide vs. placebo in Tourette's syndrome.
      • Shapiro A.K.
      • Shapiro E.
      • Eisenkraft G.A.
      Treatment of Gilles de la Tourette syndrome with pimozide.
      • Shapiro A.K.
      • Shapiro E.
      • Wayne H.
      Treatment of Tourette's syndrome with haloperidol, review of 34 cases.
      and review articles
      • Cohen D.J.
      • Friedhoff A.J.
      • Leckman J.F.
      • et al.
      Tourette syndrome: Extending basic research to clinical care.
      • Hyde T.H.
      • Weinberger D.R.
      Tourette syndrome: A model neuropsychiatric disorder.
      • King R.A.
      • Riddle M.A.
      • Goodman W.K.
      Psychopharmacology of obsessive-compulsive disorder in Tourette syndrome.
      • LeWitt P.A.
      Therapeutics of Tourette syndrome: New medication approaches.
      on the management of motor and phonatory tics, OCD, impulsivity and learning disabilities (including series unrelated to TS), the response of coprolalia and copropraxia to pharmacologic treatment is almost never addressed directly in the literature.
      When Shapiro et al
      • Shapiro A.K.
      • Shapiro E.
      • Wayne H.
      Treatment of Tourette's syndrome with haloperidol, review of 34 cases.
      stated that most patients had a 90% “reduction of symptoms after 1 year of treatment” with pimozide, they did not specifically address the response of coprolalia, present in 50% of their 34 patients. Although a subsequent report by Shapiro on 31 patients receiving open-label pimozide
      • Shapiro A.K.
      • Shapiro E.
      • Eisenkraft G.A.
      Treatment of Gilles de la Tourette syndrome with pimozide.
      mentioned the use of diaries that recorded percentage of benefit for each symptom, no mention was made of the response of coprolalia. The authors concluded that pimozide was more effective and induced fewer side effects than haloperidol. They suggested that perhaps this was due to weaker norepinephrine-blo cking properties as compared to haloperidol. Subsequently the same authors reported on a double-blind, crossover, placebo-controlled study of pimozide in 20 patients, with no mention of coprolalia.
      • Shapiro A.K.
      • Shapiro E.
      Controlled study of pimozide vs. placebo in Tourette's syndrome.
      When Ross and Moldofsky reported about comparable efficacy of pimozide and haloperidol, their main focus was on decrease in tic frequency.
      • Ross M.S.
      • Moldofsky H.
      A comparison of pimozide and haloperidol in the treatment of Gilles de la Tourette' syndrome.
      Coprolalia was present in 17% (13 of 78) of patients in the study by Bruun et al.
      • Bruun R.D.
      • Shapiro A.K.
      • Shapiro E.
      • et al.
      A follow-up of 78 patients with Gilles de la Tourette's syndrome.
      Fifty-nine patients on haloperidol alone experienced an average 79.2% improvement, but no specific mention of response of coprolalia was given. In Leckman's report on clonidine, an effect on behavioral symptoms is noted but no mention is made of coprolalia specifically.
      • Leckman J.F.
      • Hardin M.T.
      • Riddle M.A.
      • et al.
      Ratzoni et al reported on successful use of clomipramine for tics, obsessions, and compulsions in a TS patient but failed to mention coprolalia in their discussion.
      • Ratzoni G.
      • Hermesh H.
      • Brandt N.
      • et al.
      Clomipramine efficacy for tics, obsessions, and compulsions in Tourette's syndrome and obsessive-compulsi ve disorder: A case study.
      The limited information available points to antidopaminergic rather than serotonergic therapies as the ones potentially effective. A non-TS patient who presented with hemiballismus and coprolalia responded to the dopamine-depleting agent tetrabenazine,
      • Marti-Masso J.F.
      • Obeso J.A.
      Coprolalia associated with hemiballismus: response to tetrabenazine.
      although a noradrenergic or serotonergic-deple ting effect could not be excluded. A 25-year-old man with TS and OCD suffered worsening of tics and appearance of coprolalia for the first time when a serotonin uptake inhibitor (fluvoxamine) was used, and treatment with pimozide had to be added.
      • Delgado P.L.
      • Goodman W.K.
      • Price L.H.
      • et al.
      Fluvoxamine/pimozi de treatment of concurrent Tourette's and obsessive-compulsi ve disorder.
      Recently, Scott et al
      • Scott B.L.
      • Jankovic J.
      • Donovan D.T.
      Botulinum toxin injection into vocal cord in the treatment of malignant coprolalia associated with Tourette's syndrome.
      reported on the successful use of vocal cord injections of botulinum toxin (Botox) in a patient with malignant coprolalia refractory to dopamine blockade. The authors stated that Botox had caused an amelioration of the urge to utter obscenities possibly by interfering with peripheral feedback mechanisms and relief of local muscle contraction.

      Nonpharmacologic

      Of all TS-related symptoms, coprolalia potentially could be the one responsible for forcing a student out of school. The physician may have to educate the school system about the child's affliction in all its clinical manifestations,
      • Hyde T.H.
      • Weinberger D.R.
      Tourette syndrome: A model neuropsychiatric disorder.
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      including its important behavior dysfunction components. Several classroom modifications have been suggested to help patients achieve their highest academic potential.
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      Some of these recommendations, such as allowing frequent breaks and a place to “discharge” tics and emotions,
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      also would apply to the management of coprolalia. Other measures, such as help with timed testing,
      • Hyde T.H.
      • Weinberger D.R.
      Tourette syndrome: A model neuropsychiatric disorder.
      shortening writing assignments, testing orally, providing a daily assignment list of homework and test dates, and tutoring one on one
      • Jankovic J.
      Tourette's syndrome: Phenomenology, Pathophysiology, Genetics, Epidemiology, and Treatment.
      could conceivably benefit the student with coprolalia by reducing the stress level.
      Behavioral therapy has a high rate of success with OCD particularly when behavioral rituals (ie, compulsive checking or cleaning) predominate,
      • Baer L.
      Behavior therapy for obsessive-compulsive disorder and trichotillomania: Implications for Tourette syndrome.
      but this author could find no mention as to response of coprolalia to this form of treatment.

      Neurosurgical Treatment

      Hassler performed stereotactic neurosurgery on three TS patients. The procedure involved bilateral coagulation of rostral intralaminar and medial nucei of the thalamus. He reported a dramatic improvement of tics and coprolalia.
      • Hassler R.
      • Dieckmann G.
      Traitment stéreotaxique des tics et cris inarticules ou coprolaliques considerés comme phénomêne d'obsession motrice au cours de la maladie de Gilles de la Tourette.
      Kurlan et al reported on the use of bilateral radiofrequency anterior cingulotomy in two TS patients with disabling obsessive compulsive and ritualistic behaviors.
      • Kurlan R.
      • Kersun J.
      • Ballantine H.T.
      • Caine E.D.
      Neurosurgical treatment of severe obsessive-compulsive disorder associated with Tourette's syndrome.
      There was modest although sustained behavioral amelioration, but tics were not improved. Coprolalia, present in one of the two patients, was not mentioned in the postoperative description. Robertson et al
      • Robertson M.
      • Doran M.
      • Trimble M.
      • et al.
      The treatment of Gilles de la Tourette syndrome by limbic leukotomy.
      reported on the successful use of limbic leukotomy (a combination of cingulotomy and lesions in the orbitomedial frontal areas) in a TS patient suffering from severe self-injurious compulsion. The patient also experienced a 75% reduction in motor tics. Once again, coprolalia was said to be present, but its the response to the surgery was not described.

      CONCLUSION

      Coprolalia, the uncontrollable utterance of obscenities and profanities, was recognized as a component of TS from the time of the first description of the syndrome. Copropraxia, the unontrollable performance of obscene gestures, is less commonly seen. Prevalence of coprolalia varies from 8% in primary pediatric practices to over 60% in tertiary referral centers. Coprolalia tends to peak in severity during adolescence and wane during adulthood. Most authors view coprolalia within the continuum of motor and phonatory tics; the pathogenesis may be related to dysfunction of basal ganglionic and limbic minicircuits. Coprolalia also has been seen in a variety of neurologic disorders, including as a sequelae of strokes and encephalitis as well as in choreiform and OC disorders. Treatment is primarily pharmacologic, with use of dopamine-blocking agents, but behavioral therapy measures also may be considered. Neurosurgical treatments may be considered in the most severely affected persons as a last resort.

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