In his original 1885 description of the syndrome, Gilles de la Tourette emphasized the triad of multiple tics, coprolalia, and echolalia.
26
Although current diagnostic criteria do not include coprolalia as a necessary component of Tourette syndrome (TS),42
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.
16
Profane utterances, on the other hand, convey a religious connotation.16
In reality, the spectrum of these socially inappropriate utterances also includes references to animals (e.g., bitch, bull, pig)3
and racial epithets.40
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.11
, 12
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.
25
Perhaps one of the best characterized was the case of Dr. Samuel Johnson.25
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.47
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.
46
The result was a reclusive existence until the patient's death at the age of 85 years.26
Subsequently, this patient was included with eight others in Gilles de la Tourette's original paper.10
, 46
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.
46
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.46
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.
3
, 12
, 17
, 21
, 30
, 31
, 32
, , 38
, 46
Cultural factors and selection bias may help to explain these disparities. Copropraxia is less common than coprolalia17
, 26
, 38
and is rarely present in the absence of the latter.26
, 38
Jankovic17
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%.
32
This has led to the suggestion that cultural factors may act as modifiers for the manifestation of this symptom.16
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.
21
, 29
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.21
In contrast, McMahon found only 2 of 47 (4%) affected members in a large Nevada kindred.29
If one analyzes prevalence figures according to the level of specialization of the reporting clinic, tertiary referral centers exhibit a higher prevalence of coprophenomena
11
, 17
, 26
, 30
, 31
, 38
, 42
when compared with primary pediatric practices.10
, 12
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%
17
, 26
and for copropraxia from 7%11
to 21%.26
In contrast, analysis of two primary pediatric practices reveals a prevalence of coprolalia of only 8%.10
, 12
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.
10
, 42
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
11
whereas Jankovic et al17
and Micheli et al30
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.
3
, 42
Most commonly coprolalia follows the onset of motor or phonic tics by a few years, on the average 4 to 7 years later.3
Two sequential British studies from the same referral center group
26
, 30
revealed a mean age of onset of coprolalia between 14.5 and 15.1 years, with the youngest age that of 6 years,38
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).12
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.
2
, 3
, 9
, 13
Associated problems (e.g., OCD, ADHD, and a variety of other behavioral problems) however, may persist.3
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.
3
Goetz, in a study of 58 adults with TS diagnosed during childhood,13
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.12
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.
38
, 49
Robertson et al38
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 or perform obscene gestures
16
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.Four-letter words focused on anatomy, and sexual and bodily function were the most common both in the British
26
and in the American studies (Table 1)Table 1COMMON COPROLALIC UTTERANCES IN SIX COUNTRIES
| USA | UK | Denmark | Spain | Hong Kong | Japan |
|---|---|---|---|---|---|
| Fuck, (-er, -off) | Fuck | Kaeft (shut up) | Puta (whore) | Tiu (fuck) | Kusobaba (shit grandma) |
| Shit | Cunt | Svin (swine) | Mierda (feces) | Shui (useless person) | Chikusho (son of a bitch) |
| Bitch | Bastard | Fisse (vulva) | Coño (vulva) | Tiu ma (mother fucker) | Omanko (female genitalia and breasts) |
| Ass(hole) | Piss | Kusse (vulva) | Joder (fornicate) | Tiu so (aunt fucker) | |
| Bastard | Sod | Pik (penis) | Maricon (homosexual) | ||
| Pussy | Cock | Rov (ass) | Cojones (testicles) | ||
| Prick, dick, cock (sucker) | Shit | Pis (ass) | Hijo de puta (son of a whore) | ||
| Cunt | Gylle (animal feces) | Hostia (holy bread) | |||
| Fart | Sgu (by God) | ||||
| Nigger | Lort (shit) |
* Goldenberg et al 1994.
6
† Jankovic and Rohaidy 1987.
14
‡ Shapiro AK et al 1978.
23
§ Nuwer 1982.
13
¶ 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,
26
or they may be slurred and only partially pronounced.17
Patients may try unsuccessfully to disguise them with euphemisms and neologisms.26
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.12
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.
12
, 17
PATHOPHYSIOLOGY
The current view of TS as an organic disorder involving central dopaminergic mechanisms and disruption of normal striatal and limbic functions
16
, 26
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.26
, 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, in “senility,” as a sequelae of encephalitis lethargica, in vasculogenic hemiballismus, and in brain tumors, and is sometimes reversible with medical
28
or surgical14
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,
24
Leckman advanced the hypothesis that TS (and etiologically related forms of OCD) may be associated with a failure to inhibit subsets of CSTC minicircuits.23
, 24
Such circuits may be influenced by neurochemical systems originating in the brain stem and mediated by dopamine, serotonin, and norepinephrine.6
The observation that occasionally patients with severe aphasia following a stroke still may utter obscenities26
even as word substitutions could be interpreted as a manifestation of such a short-circuited pathway.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
24
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.34
In his comprehensive review on the subject, Nuwer 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. 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.
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.
20
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 in his work on high-probability phonemes or with Burd on his work on nocturnal coprolalia
5
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.34
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
26
and hemiballismus28
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”
26
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.In klazomania, a rare sequelae to encephalitis lethargica, coprolalia may accompany jerking, shaking, writhing, and other ticlike movements, as well as other symptoms. It also has been reported in OCDs independently of coexistence of TS.
34
TREATMENT
Pharmacology
When one analyzes reports
4
, 12
, 35
, 36
, 39
, 41
, 44
, 45
and review articles7
, 15
, 19
, 27
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
45
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 pimozide44
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.41
When Ross and Moldofsky reported about comparable efficacy of pimozide and haloperidol, their main focus was on decrease in tic frequency.
39
Coprolalia was present in 17% (13 of 78) of patients in the study by Bruun et al.4
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.23
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.35
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,
28
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.8
Recently, Scott et al
40
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,
15
, 16
including its important behavior dysfunction components. Several classroom modifications have been suggested to help patients achieve their highest academic potential.16
Some of these recommendations, such as allowing frequent breaks and a place to “discharge” tics and emotions,16
also would apply to the management of coprolalia. Other measures, such as help with timed testing,15
shortening writing assignments, testing orally, providing a daily assignment list of homework and test dates, and tutoring one on one16
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,
1
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.
14
Kurlan et al reported on the use of bilateral radiofrequency anterior cingulotomy in two TS patients with disabling obsessive compulsive and ritualistic behaviors.22
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 al37
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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