tandem gait performance in essential tremor

Paligraphia and Written Jocularity inGilles de la Tourette Syndrome

Gilles de la Tourette syndrome (GTS) is a neuropsychi-atric disorder of childhood onset, characterized by multiplemotor tics and one or more phonic tics. Tics are definedas sudden, rapid, recurrent, nonrhythmic, stereotyped move-ments, or vocalizations.1 Tics comprise a dynamic andhighly heterogeneous class of symptoms; in addition,an array of concomitant complex tic-related symptomshave been described in GTS populations.2 These includeinvoluntary, inappropriate swearing (coprolalia), involuntaryobscene gestures (copropraxia), copying others (echolaliaand echopraxia), repeating words and actions (palilalia andpalipraxia), and more complex nonobscene socially inappro-priate behaviors.3 Each of the aforementioned itemsharbours a written manifestation; echographia is a rewritingof phrases produced by the reader, coprographia is the exhi-bition of coprolalic tendencies in writing, and finally, thepaligraphia variant is a tendency to word iterations gener-ated by the patient. Although the range of tic-related symp-toms is omitted from current diagnostic criteria, the presenceof such features strengthens the diagnostic confidence of theclinician and is suggestive of ‘‘full-blown GTS.’’4 Moreover,such behaviors in association with tics are increasingly notedas socially detrimental and contributory to the impairmentin quality of life in patients with GTS.5

We report two cases of patients diagnosed with GTS whodisplayed abnormal repetition of written letters, words, orphrases (paligraphia).The first example (Case 1) of altered writing illustrated in

the present report was demonstrated at the Tourette Clinic,Department of Neuropsychiatry, BSMHFT and University ofBirmingham, UK. The patient, a man aged 47 who had beensuffering with GTS since early childhood, presented withmultiple motor tics mainly affecting his face in the form ofgrimacing, eye and mouth movements, and involuntaryvocalizations. He also reported several tic-related symptoms,including forced touching and licking compulsions, and wasdiagnosed with comorbid obsessive–compulsive disorder. Hewas medication free at the time of the assessment, when heprovided us with written evidence indicating his compulsiveperseverance, apparent in repetition and jocularity, includingwordplay (Fig. 1a). He produced a string of six words punc-tuated with grammar, comprising two words, one commenc-ing and the other terminating the sequence, which differ

only for the first letter (‘‘R’’-‘‘H’’). Four rhyming words areencapsulated within and are characterized by assonance(‘‘ie’’-‘‘ie’’-‘‘y’’-‘‘ie’’), some degree of alliteration (‘‘L’’-‘‘L’’)and sexual allusion. On direct questioning, the patientreported that he found the consonant sounds ‘‘yyy’’ and‘‘xxx’’ ‘‘particularly satisfying.’’

Case 2, a 9-year-old girl who was contacted for researchpurposes through Tourettes Action (UK), was requested toreturn a signed consent form along with a questionnairebooklet. Paligraphia is evident as the recurrent repetition ofher name in the signature space (Fig. 1b). Of note, the sec-ond and third iterations are slightly less distinct, possiblysuggesting a graphical form of self-echoing.

Paligraphia and echographia have been previouslyreported in the context of advanced degenerative, traumaticor vascular conditions, as well as in catatonic syndromes.6

Paligraphia is an involuntary alteration in writing typified bycompulsive reiteration, two or more times, of the subject’sown semantically adequate words or phrases. We report twoexamples of paligraphia in the context of GTS.

In Case 1, paligraphia was demonstrated by repetition ofwritten words with minimal syllabic variation and explicitjocularity, particularly in relation to the phonetic feature ofwords. The particularly satisfying feeling reported by thispatient after his written production reminds of the ‘‘justright’’ phenomena extensively described in GTS, for whichthe ambiguous term ‘‘compulsive tics’’ has been coined.7 Onthe other hand, a relief of anxiety might also have led tosuch emotional response. This raises the question whetherthe phenomenology of these symptoms resembles more thatof tics or, rather, of compulsions. Interestingly, Case 1 had adiagnosis of comorbid obsessive–compulsive disorder, a con-dition where specific alterations in handwriting performancehave been observed.8

Historically, instances of graphical self-repetition and writ-ten jocularity have been documented in the posthumous, andarduously debated, diagnosis of Wolfgang Amadeus Mozart.Several of Mozart’s letters display comic aspects includingword games and word scrambling as well as sexual insinua-tion.9 However, the opinion that he might have suffered fromGTS has been strongly challenged;10 hence, his playing with

FIG. 1. Examples of paligraphia in the context of Gilles de la Tourettesyndrome from Case 1 (A) and Case 2 (B).

------------------------------------------------------------*Correspondence to: Andrea E.Cavanna, Department ofNeuropsychiatry, University of Birmingham and BSMHFT, Birmingham,United Kingdom; [email protected]

Relevant conflicts of interest/financial disclosures: Nothing to report.Full financial disclosures and author roles may be found in the onlineversion of this article.

Published online 21 March 2011 in Wiley Online Library(wileyonlinelibrary.com). DOI: 10.1002/mds.23495

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words and inclusion of obscene references in letters couldhave had a different psychological explanation altogether.Case 2 comprises complete repetition of the patient signa-

ture, with each duplication evocative of a progressively faintingecho. The declining strength of this graphical reverberation isreflected in its sister phenomenon, as the reiteration of palilaliais characteristically composed of pronunciation of increasingrapidity and decreasing volume eventually progressing to nosound production.11 To date, palilalia has been reported asutterances of words or phrases that occur with a varied fre-quency, but to our knowledge, it has never been describedwith ‘‘graphic’’ characteristics.

Andrea E. Cavanna, MD, PhD,1,2,3,* Fizzah Ali,4

and Hugh Rickards, MD4

1Department of Neuropsychiatry, University ofBirmingham and BSMHFT, Birmingham,

United Kingdom2Sobell Department of Motor Neuroscience andMovement Disorders, Institute of Neurology,

University College London, London,United Kingdom

3Department of Mental Health Sciences,University College London, London,

United Kingdom*E-mail: [email protected]

4Department of Neuropsychiatry, University ofBirmingham and BSMHFT, Birmingham,

United Kingdom

References1. Jankovic J. Phenomenology and classification of tics. In: Jankovic

J, editor. Neurologic clinics. Philadelphia:WH Saunders Company;1997. p 267–275.

2. Cavanna AE, Servo S, Monaco F, Robertson MM. The behavioralspectrum of Gilles de la Tourette syndrome. J NeuropsychiatryClin Neurosci 2009;21:13–23.

3. Kurlan R, Daragjati C, Como P, et al. Non-obscene complexsocially inappropriate behavior in Tourette’s syndrome. J Neuro-psychiatry Clin Neurosci 1996;8:311–317.

4. Robertson MM, Banerjee S, Kurlan R, et al. The Tourette syndromediagnostic confidence index. Neurology 1999;53:2108–2112.

5. Cavanna AE, Schrag A, Morley D, et al. The Gilles de la Tourettesyndrome—quality of life scale (GTS–QOL). Neurology 2008;71:1410–1416.

6. Benson DF, Cummings JL. Agraphia. In: Vinken J, Bruyn GW, edi-tors. Handbook of clinical neurology. New York:American ElsevierPublishing Company; 1985. p 457–472.

7. Mansueto CS, Keuler DJ. Tic or compulsion? It’s tourettic OCD.Behav Modif 2005;29:784–799.

8. Mavrogiorgou P, Mergl R, Tigges P, et al. Kinematic analysis ofhandwriting movements in patients with obsessive–compulsive dis-order. J Neurol Neurosurg Psychiatr 2001;70:605–612.

9. Simkin B. Mozart’s scatological disorder. Br Med J 1992;305:19–26.

10. Monaco F, Servo S, Cavanna AE. Famous people with Gilles de laTourette syndrome? J Psychosom Res 2009;67:485–490.

11. Serra-Mestres J, Robertson MM, Shetty T. Palicoprolalia: an un-usual variant of palilalia in Gilles de la Tourette’s syndrome.J Neuropsychiatry Clin Neurosci 1998;10:117–118.

Luxie Loxie—Hannah Hannah—Anna. . .Blume

The report by Cavanna et al.1 on paligraphia, that is, rep-etition of written words and phrases, in Gilles de la Tourettesyndrome (GTS) is very instructive. Such exaggerated tend-ency to repeat may be another example of behaviors com-mon in children, which have ‘‘survived’’ in adult GTS. Ticsper se are probably not abnormal in young children butbecome a problem when they persist or even increase duringdevelopment. The same may be true for echo-phenomenaand some forms of obsessions or compulsions. Although,clearly, there is no reason to romanticize GTS symptomssome may be key holes through which we can look backinto earlier stages of development. In other words, they maytell us something about the ‘‘unshaped’’ brain.

Repetition of words, or word fragments, is a characteristicfeature of babies’ babbling. ‘‘Babababa. . .’’ etc. Why we liketo repeat, has many reasons including the joy to play withsomething newly acquired, a soothing sensation, reassurance,or others.

Artistic repetition of written language was mastered byKurt Schwitters (1887–1948) who developed his unique styleof ‘‘Merzdichtung’’ (collected in ‘‘Anna Blume’’), derivedfrom the German word ‘‘Kommerz’’ (commerce).2 Collatingmaterial from different sources including advertisement,scribbles on walls, he created art through selection, rear-rangement, deforming and repetition. One example of hislater poems is ‘‘What a b what a b what a beauty,’’ whichhe wrote in 1944 during his exile in England.3

What a b what a b what a beauty;What a b what a b what a a;What a beauty beauty be;What a beauty beauty be;What a beauty beauty beauty be be be;What a be what a b what a beauty;What a b what a b what a a;What a be be be be be;What a be be be be be;What a be be be be be be be a beauty be be be;What a beauty.

His masterpiece, the ‘‘Ursonate,’’ one of the most extreme

Avantgarde pieces of the 20s of the last century, commenced

with ‘‘Fumms bo wo taa zaa Uu,. . .’’ and then went on in

longer and shorter repetitive sounds and word fragments,

following the structure of a sonata in different tempi.2,4

Although fiercely criticized by conservatives when read, it

------------------------------------------------------------*Correspondence to: Alexander Munchau, Department of Neurology,University Hospital Medical Center Hamburg-Eppendorf, Hamburg,Germany; [email protected]



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touched many people when read out loud by the author. It

was reported that at the premiere in 1925, the whole audi-

ence, including higher rank members of the German Army,

was tearing with laughter when the poem was read out by

Schwitters and still had tears in their eyes after the reading

when they approached the poet to express their gratitude and

enthusiasm.5 Apparently, they were moved by the beauty and

fun of playing with words over and over again, the evocation of

childish behavior amalgamated in this peace of art.Thus, rather than pathological behavior paligraphia, like

other paliphenomena, might be considered an expression ofthe brain’s primal inclination to reiterate, to play and playand play with words.

Alexander Munchau*

Department of Neurology, University HospitalMedical Center Hamburg-Eppendorf, Hamburg,

Germany*E-mail: [email protected]

References1. Cavanna AE, Ali F, Rickards H. Paligraphia and written jocularity

in Gilles de la Tourette syndrome. Mov Disord 2011 (in press).

2. Schwitters K. In: Schreck J, editor. Anna Blume und andere: Litera-tur und Grafik. Koln: DuMont; 1997.

3. Schwitters K.What a b what a b what a beauty. In: Weiss C, RihaK, editors. Eile ist des Witzes Weile. Stuttgart: Philipp Reclam;1987. p 92.

4. Schwitters K. Scherzo der Ursonate, gesprochen von Kurt Schwit-ters. In: Mon F, editor. Phonetische Poesie. Darmstadt: Luchter-hand Schallplatte, 1970.

5. Ammer A. Kurt Schwitters. Die Ursonate. In: Jens W, editor. Kin-dlers Neues Literatur Lexikon (Bd. 15), Nordlingen: C.H. Beck’scheVerlagsdruckerei; 1988. p 56.

Tandem Gait Performancein Essential Tremor

We read with interest the article by Louis et al1 analyzingtandem gait (TG) performance in patients with essentialtremor (ET). The authors assessed in detail several demo-graphic and clinical variables associated with TG difficultiesin 122 patients with ET. In addition, they studied associa-tions between midline tremors (jaw, voice, neck) and TGdisturbances. Their results showed that patients with moreprominent midline tremors, those with older age of tremoronset, and those with older age at the time of assessmentwere more likely to present with TG difficulty, detected by

------------------------------------------------------------*Correspondence to: Renato P. Munhoz, Movement Disorders Unit,Neurology Service, Hospital de Clınicas, Federal University of Parana,Curitiba, Brazil; [email protected]



the number of missteps during a 10-step tandem walk trial.The mean age of the sample was 64.9 6 15.4 years, withmean age of tremor onset of 40.5 6 22.6 years.

Gait disorders, including specific TG difficulties, have previ-ously been demonstrated in patients with ET2; however, Louiset al1 were the first to analyze its demographic and clinicalcorrelates. In their study, the associations of TG difficulties,older age, and older age of tremor onset in ET were carefullydiscussed by the authors, including previous findings showingthat older age of onset is commonly linked to a faster andmore malignant progression as well as a more degenerativepathology in the cerebellum. In addition, the authors note thatolder age per se is associated with worse balance performance,independent of the diagnosis of ET. We would like to suggestthe possibility that some of these cases may in fact be carriersof the fragile X premutation (FXP).3

The fragile X syndrome with mental retardation and typi-cal physical stigmata results from the expansion of a CGGtrinucleotide repeat in the FMR1 gene. Normally, FMR1 has6 to 40 CGG repeats, whereas the full mutation results fromexpansions with more than 200 repeats. Those with interme-diate expansions are considered carriers of the FXP, associ-ated with the fragile X–associated tremor/ataxia syndrome(FXTAS), including cases misdiagnosed as ET.4 FXP carriersfrequencies are estimated to be 1 per 260 females and 1 per760 males, with a penetrance to FXTAS close to 50% at theage of 60 and up to 100% for individuals older than 80.Although cases have been reported in both men and women,FXTAS is probably more frequent in male subjects, who typ-ically present with onset in the sixth decade,3 which overlapsthe mean age of the sample studied by Louis et al.1 We alsohighlight the fact that although gait difficulties are cardinalfeatures of FXTAS, some cases may present these featureslater in the disease course, with more prominent tremor inthe earlier stages. Finally, although most cases of FXTAShave been found in men and Louis et al.1 did not find anassociation between missteps and sex, we believe that someof these patients may be FXP carriers, and FXTAS should beincluded as an additional alternative possibility to accountfor these interesting findings.

Renato P. Munhoz, MD, MSc*and Helio A. G. Teive, MD, PhD

Movement Disorders Unit, Neurology Service,Hospital de Clınicas, Federal University of

Parana, Curitiba, Brazil*E-mail: [email protected]

References1. Louis ED, Rios E, Rao AK. Tandem gait performance in essential

tremor: clinical correlates and association with midline tremors.Mov Disord. 2010;25:1633–1638.

2. Stolze H, Petersen G, Raethjen J, Wenzelburger R, Deuschl G. Thegait disorder of advanced essential tremor. Brain. 2001;124:2278–2786.

3. Baba Y, Uitti RJ. Fragile X-associated tremor/ataxia syndrome andmovements disorders. Curr Opin Neurol. 2005;18:393–398.

4. Leehey MA, Munhoz RP, Lang AE, et al. The fragile X premuta-tion presenting as essential tremor. Arch Neurol. 2003;60:117–121.


932 Movement Disorders, Vol. 26, No. 5, 2011

Reply: Tandem Gait Performance inEssential Tremor

We thank Munhoz and Teive for their comments; how-ever, we expect that few if any of our essential tremor (ET)cases were carriers of fragile X premutations. Althoughthere have been rare reports of patients with fragile X pre-mutations presenting with ET-like clinical features and ETdiagnoses,1 a spate of studies published in 2004 documentedthat the proportion of ET cases with such fragile X premu-tations (55–200 CGG repeats) is near 0%. Thus, in oursample of 81 familial ET cases in the United States, nonecarried the premutation.2 A study in Singapore in that sameyear of 71 ET cases similarly showed that none carried thepremutation.3 A third study,4 in the United States, reportedthat none of the 196 ET cases were premutation carriers.Combining the 3 studies, 0 of 348 ET cases were carriers.In the study under question,5 we assessed gait in 122 ETcases. Given the published data cited above,2–4 it is highlyprobable that none of our 122 ET cases were FXTAScarriers.

Elan D. Louis, MD, MSc1,2,3,4* andAshwini K. Rao, EdD, OTR5

1G.H. Sergievsky Center,College of Physicians and Surgeons,Columbia University, New York,

New York, USA;2Department of Neurology,

College of Physicians and Surgeons,Columbia University, New York,

New York, USA;3Taub Institute for Research on Alzheimer’sDisease and the Aging Brain, College of

Physicians and Surgeons, Columbia University,New York, New York, USA;

4Department of Epidemiology, Mailman School ofPublic Health, Columbia University, New York,New York, USA; *E-mail: [email protected] 5Program in Physical Therapy, Department ofRehabilitation Medicine, College of Physiciansand Surgeons, Columbia University, New York,

New York, USA

References1. Leehey MA, Munhoz RP, Lang AE, et al. The fragile X premuta-

tion presenting as essential tremor. Arch Neurol. 2003;60:117–121.

2. Garcia Arocena D, Louis ED, Tassone F, et al. Screen forexpanded FMR1 alleles in patients with essential tremor. Mov Dis-ord. 2004;19:930–933.

3. Tan EK, Zhao Y, Puong KY, et al. Fragile X premutation allelesin SCA, ET, and parkinsonism in an Asian cohort. Neurology.2004;63:362–363.

4. Deng H, Le W, Jankovic J.Premutation alleles associated with Par-kinson disease and essential tremor. JAMA. 2004;292:1685–1686.

5. Louis ED, Rios E, Rao AK.Tandem gait performance in essentialtremor: clinical correlates and association with midline tremors.Mov Disord. 2010;25:1633–1638.

------------------------------------------------------------*Correspondence to: Elan D. Louis, G.H. Sergievsky Center, Collegeof Physicians and Surgeons, Columbia University, New York, NewYork, USA; [email protected]




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