LETTERS

Hyperacusis and Origins of Lowered Sound Tolerance

SIR: Nields et al.1 rightly highlighted the severe psychological sequelae of lowered sound tolerance in Lyme disease (as in many other conditions) and claimed a central origin for hyperacusis. There is a serious problem with intolerance denitions and nomenclature. Itard, who coined hypercousie, said it had a great number of varieties. Many loudness phenomena occur in damaged ears, although it remains to be seen if these decits are totally independent: 1. Hyperacusis, best considered as increased sensitivity to quiet sounds. I dened it2 as mean pure tone hearing between 250 and 4,000 Hz better than zero dB Hearing Level (HL). This is very similar to the denition of hyperacute hearing1 as ability to distinguish sounds below zero dB HL. 2. Audiosensitivity, dened as aversion to the output of television sets, radios, or sound systems at volume levels tolerated by normal listeners.2 3. Intolerance to other loud noises. Unlike strict audiosensitivity, in this condition stapedial reexes were found to be normal.2 4. Recruitment, when loud noises in impaired ears sound as loud in the deaf ear as in a normal ear.3 It does not physiologically explain increased loudness and should not be used for clinical intolerances. 5. Loudness discomfort level, where patients indicate the intensity at which sounds start to feel uncomfortably loud. This is a standard audiometric test, though I have not found it an accurate indicator of au-

diosensitivity, intolerance, or recruitment,2,3 stapedial reex measures being far better. Confusingly, Nields et al.1 dened sound tolerance at or below 100 dB HL as hyperacusis. 6. Tullio phenomenon, well described by Nields and Kveton,4 an idiosyncratic vestibular response to loud noise, probably due to labyrinthine stulas. 7. Audiogenic seizures from loud noises in susceptible animals,5 a standard assay for anticonvulsants like carbamazepine. Nields et al.1 state that hypersensitivity to sound can originate anywhere from ear to cortex. Agreed, but does it? The best-attested cause of audiosensitivity is Menieres disease, as in C. Darwin and Van Gogh.6 Fortunately, excellent clinical descriptions1,7,8 provide abundant clinical evidence for endolymphatic hydrops9 in Lyme disease: blurry vision, tinnitus, transient unilateral deafness, sensation of head pressure, extreme sound sensitivity, agoraphobia, gastrointestinal problems, dizziness, imbalance, nausea, vomiting, depersonalization, motion sickness, paranoia. Such recognizable clinical symptoms are not always conrmed by objective neuro-otological ndings. Nevertheless, there is a denite link with classic Menieres disease in some with Lyme disease10 (characteristic low tone or uctuant losses and vertigo attacks, as in early syphilis). There is no plausible encephalopathic cause for deafness and vertigo, even occurring separately.6 Another approach is to consider the pathogenesis of musical hallucinations (MHs) such as occur in Lyme disease.8 A review9 clearly showed a common mechanism for

all MHs, with incipient hydrops probably a necessary and sufcient cause. Risk factors included anything likely to reduce labyrinthine pressure, like fevers, dehydration, stulas, and weight loss (prominent in Lyme disease1). A further argument for a peripheral locus for auditory disorders comes from syphilis, which Lyme disease closely mimics. There is a large literature on syphilitic ear disease, including Menieres syndrome. Audiosensitivity was surprisingly common in composers, many of whom had otosyphilis, including Beethoven, Haydn,6 Rossini, Donizetti, Smetana, Delius, and Wolf, who plugged his ears with bread and shot noisy songbirds! Nields et al.1 noted a kindling phenomenon where repeated sound stimulation led to reduced tolerance. I have never seen this reported before, nor observed it myself, but have not specically checked with patients. This emphasizes the continuing value of careful clinical observations. In some rodents acoustic priming kindles audiogenic brainstem seizures, with secondary limbic epilepsy,11 especially in the amygdala. The inferior colliculus is widely believed to play a major but unexplained role in auditory seizure initiation. Brainstem potentials show enhanced excitability along the auditory pathway, but only the peripherally generated Wave Ia had signicantly shorter latency than in both control groups.12 Such cochlear hyperactivation is not surprising given deafness and cochlear pathology in genetically seizure-prone rodents. Most tinnitus clearly comes from the ear, but recent physiological work has led to the claim, reported in the Times (London), that it has a

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LETTERS central origin,13 especially in the inferior colliculus. The standard animal model involves salicylates, which lowered activity in cochlear nucleus and inferior colliculus but increased it in auditory cortex.14 However, salicylate acts on the cochlea and can cause hydrops and otogenic MHs.9 This controversy could be rapidly settled by the production of clinical cases of tinnitus due to a brain lesion in patients with normal ears and hearing. Despite a specic appeal,13 no such case has appeared. Lyme disease is mimicked by experimental activation of the amygdala by procaine.1 However, procaine also overactivates the cochlea,15 producing audiosensitivity, elementary auditory hallucinations (i.e., tinnitus), and seizure activity, as when the labyrinth is overstimulated by loud noise12 or movements.5 In line with the maxim that the better and more original todays idea, the further back one has to go to nd out who thought of it rst, a peripheral locus of audiosensitivity had a sound 18th-century basis. E. Darwin was an acute observer, and there were plenty of febrile patients.16 Inammation of the brain is attended with intolerance of light and sound; which shews that the extremities of the nerves of those senses are at the same time inamed. After extensive dissections of man and beast, Comparetti17 stated that tinnitus and hypersensitive uid were characterized by labyrinthine uid deciency (Sed, humore deciente, annon potius debilior sensus, quam exquisitior?) Even when this occurred, as it so often did, in hysteria, hypochondria, and mental illness, he still said it was of labyrinthine origin. Itard in 1821 also noted that symptomatic audiosensitivity, as occurs in otitis, also occurred in hysteria and hypochondria.2 A. G. GORDON , London, UK diological hypersensitivity, differing in clinical presentation and pathophysiology, and there is a need for clear terminology to distinguish them. It was beyond the scope of our paper to go into these entities in detail, and Dr. Gordon offers some helpful clarication. There are, however, some terms that are used differently in our sources1,2 from those Dr. Gordon cites. Most notably, what he terms hyperacusis is what we would designate as hyperacute hearing, and what he calls audiosensitivity is what we term hyperacusis. An additional clinical entity that can mimic or compound hyperacusis is phonophobia, a cortically determined avoidance of and greater sensitivity to anticipated than unanticipated sounds. Clearly there is a need for standardization in the usage of these terms. Dr. Gordon is mistaken in stating that we claimed a central origin for hyperacusis. We rather hypothesized a central origin for a particular form of hyperacusis observed in some patients with latestage Lyme disease. This form of hyperacusis, characterized among other things by a kindling-like intensication of sound intolerance in response to subthreshold sound stimulation, is very rare among hyperacusis patients in general and responds poorly to treatments such as Tinnitus Retraining Therapy that appear to be effective for the more common forms of hyperacusis. Dr. Gordon rightly points out that Lyme disease, like syphilis, can affect the inner ear, causing hearing loss, vertigo, and/or the Tullio phenomenon. Among his arguments in favor of a peripheral origin for Lyme diseaseinduced hyperacusis is that Lyme disease can cause a clinical syndrome similar to Menieres disease. Mistakenly, however, he assumes a conuence of symptoms that can occur in Lyme

References

1. Nields JA, Fallon BA, Jastreboff PJ: Carbamazepine in the treatment of Lyme diseaseinduced hyperacusis. J Neuropsychiatry Clin Neurosci 1999; 11:9799 2. Gordon AG: Abnormal middle ear muscle reexes and audiosensitivity. Br J Audiol 1986; 20:9599 3. Gordon AG: Peripheral audiosensitivity. Br J Psychiatry 1992; 160:720721 4. Nields JA, Kveton JF: Tullio phenomenon and seronegative Lyme borreliosis. Lancet 1991; 338:128129 5. Gordon AG: Epilepsy and vertigo. Epilepsia 1999; 40:11681169 6. Gordon AG: Seeking Haydns secrets (letter). Cerebrovasc Dis 1999; 9:54 7. Fallon BA, Nields JA, Parsons B, et al: Psychiatric manifestations of Lyme borreliosis. J Clin Psychiatry 1993; 54:263 268 8. Fallon BA, Nields JA: Lyme disease: a neuropsychiatric illness. Am J Psychiatry 1994; 151:15711583 9. Gordon AG: Do musical hallucinations always arise from the inner ear? Med Hypotheses 1997; 49:111122 10. Hanner P, Edstro m S, Rosenhall U, et al: Hearing impairment in patients with antibody production against Borrelia burgdorferi antigen. Lancet 1989; i:1315 11. Simler S, Vergnes M, Marescaux C: Spatial and temporal relationships between c-Fos expression and kindling of audiogenic seizures in Wistar rats. Exp Neurol 1999; 157:106119 12. Coleman JR, Ross KC, Mullaney MM, et al: Latency alterations of the auditory brainstem response in audiogenic seizure-prone Long-Evans rats. Epilepsy Res 1999; 33:3138 13. Gordon AG: The functional neuroanatomy of tinnitus. Neurology 1998; 51:647648 14. Wallha usser-Franke E, Braun S, Langner G: Salicylate alters 2-DG uptake in the auditory system: a model for tinnitus? Neuroreport 1996; 7:15851588 15. Gordon AG: Unilateral auditory hallucinations: ear or brain? (letter). J Neurol Neurosurg Psychiatry 1997; 63:814 16. Darwin E: Zoonomia. London, Johnson, 1801 17. Comparetti A: Observationes anatomicae de aure interna comparata. Patavii, S. Bartholomaeus, 1789

In Reply
SIR: Dr. Gordon rightly points out that there are many forms of au-

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LETTERS disease but that do not, as in Menieres disease, typically occur together. Among the protean manifestations of Lyme disease, some symptoms occur more or less independently while others form symptom-clusters suggestive of a common locus of pathology. Although Lyme disease can indeed cause hearing loss, the vast majority of patients who develop hyperacusis due to Lyme disease do not have hearing impairment. Most do, however, experience other sensory hyperacuities (e.g., to light, taste, smell, touch, and vibration) that uctuate in intensity concomitantly with their hyperacusis. We have observed kindling-like effects not only in the context of hyperacusis alone, but also across sensory modalities. Exposure to bright or ickering light, for instance, is associated (in some patients) with a lowered sound tolerance threshold. It was these phenomena that led us to postulate central involvement in the production of Lyme diseaseinduced hyperacusis. Further research into the various kinds of hearing sensitivity and their respective pathogeneses and into the pathogenesis of the neurological and neuropsychiatric effects of Lyme disease is needed in order to determine how and why hyperacusis occurs in Lyme disease and how best to treat it. We appreciate Dr. Gordons contribution to the understanding of these phenomena. JENIFER A. NIELDS, M.D. Faireld, CT BRIAN A. FALLON, M.D. New York, NY PAWEL JASTREBOFF, M.D. Atlanta, GA
References

non J, Moller A. Needham Heights, MA, Allyn and Bacon, 1995, pp 7387 2. Jastreboff PJ, Gray WC, Mattos DE: Tinnitus and hyperacusis, in Otolaryngology: Head and Neck Surgery, 3rd edition, vol 4, edited by Cummings CW, Frederickson JM, Harker LA. St. Louis, MO, MosbyYear Book, 1998, pp 31983222

Cotards Syndrome in a Young Male Bipolar Patient

SIR: We here describe a rare case of Cotards syndrome in a young male bipolar patient and the positive response to electroconvulsive therapy (ECT). The Cotards syndrome among adolescents and young adults is very uncommon, and the description of the syndrome in young males is exceptional. Since 1880, when Cotard described a patient with delusions of negation and immortality, some modications have been made to arrive at the present concept of Cotards syndrome. This syndrome is typically related to depression (although it also has been described in schizophrenia and organic diseases) and to middle-aged or older people. Berrios and Luques statistical analysis of 100 cases reported in the literature showed a mean age of 5214.5 years.1 Greater age was found to increase the likelihood of developing Cotards syndrome. Nevertheless, there are 7 cases reported in the literature affecting young people,25 almost 90% of those affected being females. Case Report A 20-year-old male was diagnosed as having a bipolar disorder because of three manic episodes suffered during the year prior to admission. No previous depressive episodes were detected. He had a family history of bipolar disorder in a second-degree relative. While he was on treatment with lithium car-

1. Jastreboff PI: Tinnitus as a phantom perception: theories and clinical implications, in Mechanisms of Tinnitus, edited by Ver-

bonate 800 mg/day, the patient suffered a short period of overactivity. Progressively over a 2-week period he became more isolated; he had a depressed mood, lost his appetite, and started to lie in bed most of the time, presenting a severe psychomotor retardation. Two days before his admission he showed nihilistic delusions concerning his body (my liver and stomach are being destroyed, my heart doesnt beat, I dont have muscles) and concerning existence (I am dead). The family brought the patient to our emergency room. On admission to our inpatient psychiatric unit his most prominent psychopathology was a at affect, psychomotor retardation, ideas of negation, and delusions of being dead. Physical examination was normal. Laboratory assessment (complete blood count, electrolyte and creatinine levels, and thyroid hormones) was within normal values. At this time lithium levels were 0.56 mEq/l. The dexamethasone suppression test was negative. Brain CT did not demonstrate any pathology. A diagnosis was made of bipolar disorder, severe depressive episode with psychotic symptoms (DSM-IV). Imipramine was added at a daily dosage of 225 mg. Three days after initiating treatment with imipramine, the patient became mute, refused to eat and drink, and presented a marked psychomotor inhibition and muscular rigidity (a catatonic state). Electroconvulsive therapy (ECT) with bilateral electrode placement and brief pulse stimulus was initiated on a 3 days/ week basis. Lithium treatment was discontinued because of the potential risk for developing a confusional state in association with ECT. After the sixth ECT session the patients condition improved promptly. A hypomanic episode appeared progressively after the

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LETTERS eighth ECT session. Because of the presence of this hypomania, the patients family decided that ECT sessions should be interrupted at the 10th session, with a total convulsive time of 574 seconds. Imipramine dose was decreased to 150 mg/day. Two days after discontinuing ECT, the patient progressively developed slowness in movements and speech, and 2 days later, he relapsed with hypochondriacal delusions (that his muscles were degenerating, that his tonsils were deteriorating, that his heart had become smaller). He also showed a feeling of derealization and depersonalization. At this point, we decided to add haloperidol 8 mg/day to the treatment. Because of an oculogyric crisis, biperiden 4 mg/day was also added. After 3 days the symptoms began to improve. The patient was discharged 14 days later, in a state of almost full remission. Discussion This is one of the few reported cases of Cotards syndrome in a young patient and provides further support for the conceptualization of the de lire des ne gations as a syndrome rather than a specic disease. Among the other 7 cases25 published in the literature affecting young people, 6 cases24 occurred, like ours, in bipolar patients (some of them diagnosed after having manic symptoms while they were in treatment with ECT). This case provides more arguments for including bipolar disorder as a rst differential diagnosis option when managing Cotards syndrome among adolescents and young adults. It is also remarkable that of the 8 cases reported in young people, 6 are female. In the Berrios and Luque review,1 no gender differences were detected in the global frequency of Cotards syndrome, but the presence of organic disorder was more frequent in females. The reason for this higher prevalence in young females versus young males could be explained by a publication bias. The clinical picture of this patient shares some characteristics with those reported among people under 23 years of age in the literature:3 a family history of affective disorder, a psychiatric history (from 6 months to 1 year) of affective disorder before the onset, a good response to ECT, and the inversion of the mood to a manic state during the treatment of the episode. Although according to the criteria proposed by Berrios and Luque1 this patient had most of the delusional symptoms of Cotard type I (hypochondriacal delusions, nihilistic delusions concerning the body and existence) with a suggested nosological origin in delusional disorders, the past history, the presence of psychotic depression, and the therapeutic response to antidepressant treatment suggest its origin in affective disorders. As previously reported, ECT is an appropriate treatment option for young patients with Cotards syndrome, despite its cognitive secondary effects and the risk of manic symptoms in the bipolar disorder patients group. We also nd helpful the co-administration of tricyclic antidepressants and antipsychotics, followed by the standard management of a bipolar disorder. I. BAEZA, M.D. ` , M.D. J. SALVA M. BERNARDO, M.D., PH.D. Institut Cl nic de Psiquiatria i Psicologia, Hospital Cl nic i Universitari de Barcelona, Barcelona, Spain
References

1. Berrios GE, Luque R: Cotards syndrome: analysis of 100 cases. Acta Psychiatr Scand 1995; 91:185188 2. Halfon O, Mouren-Simeoni MC, Dugas M: Le syndrome de Cotard chez ladolescent. Soc medico-psychologique 1985; 143:876 879 3. Fillastre M, Fontaine A, Depecker L, et al: Cinq cas de syndrome de Cotard de ladolescent et de ladulte jeune. Ence phale 1992; 18:6566 4. Cohen D, Cottias C, Basquin M: Cotards syndrome in a 15-year-old girl. Acta Psychiatr Scand 1997; 95:164165 5. Camarero M, Real V: S ndrome de Cotard en adolescente. Psiquiatr a Biolo gica 1997; 4:213214

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