We present a 76-year-old right-handed woman, fluent in English and Chinese, who developed anomia at age 70 and then progressed to aphasia. Functional ...
Neurocase (2006) 12, 296–299 Copyright © Taylor & Francis Group, LLC ISSN: 1355-4795 print / 1465-3656 online DOI: 10.1080/13554790601126047
Primary Progressive Aphasia in a Bilingual Woman NNCS
CHRISTOPHER M. FILLEY1,2,3, GAIL RAMSBERGER4, LISE MENN5, JIANG WU2, BESSIE Y. REID and ALLAN L. REID Bilingual Aphasia
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Department of Neurology, University of Colorado School of Medicine, Denver, Colorado, USA Department of Psychiatry, University of Colorado School of Medicine, Denver, Colorado, USA 3 Denver Veterans Affairs Medical Center, Denver, Colorado, USA 4 Department of Speech, Language, & Hearing Sciences, University of Colorado at Boulder, Boulder, Colorado, USA 5 Department of Linguistics, University of Colorado at Boulder, Boulder, Colorado, USA 2
Multilingual aphasias are common because most people in the world know more than one language, but little is known of these syndromes except in patients who have had a stroke. We present a 76-year-old right-handed woman, fluent in English and Chinese, who developed anomia at age 70 and then progressed to aphasia. Functional neuroimaging disclosed mild left temporoparietal hypometabolism. Neurolinguistic testing was performed in both English and Chinese, representing a unique contribution to the literature. Results revealed conduction-like aphasia that was comparable in the two languages, although English was slightly better preserved. Primary progressive aphasia has disrupted 2 languages in a similar manner, suggesting their close neuroanatomic relationship in this case.
More than half the population of the world is multilingual, and thus the majority of patients with aphasia can be expected to have disturbances in more than one language (Fabbro, 2001). Whereas the clinical importance of understanding these cases is indisputable, the study of multilingual individuals with aphasia from a theoretical perspective provides a valuable approach to understanding the cerebral representation of language (Fabbro, 2001). These patients present the opportunity to address questions such as whether multiple languages are represented in similar or different brain regions, the influence of age of language acquisition, and the effect of premorbid experience with the involved languages (Fabbro, 2001; Fabbro, 2001; Paradis, 1977). Whereas many methodological issues have hampered research in this area, clinical and neuroimaging studies indicate that left hemisphere damage typically affects all the languages possessed by aphasic patients, although frequently in a highly variable fashion (Fabbro, 2001; Fabbro, 2001; Paradis, 1977). Clinical investigations have documented that bilingual aphasics do not necessarily present with the same type or severity of aphasia in the two languages (L1 and L2; Fabbro, 2001; Fabbro, 2001; Paradis, 1977). Recovery patterns may also differ; in one study, only 40% of bilingual aphasics exhibited parallel recovery of L1 and L2, while the remainder showed better recovery in either L1 or L2 (Fabbro, 2001). Most of the literature on polyglot aphasia concerns patients who have had a stroke. However, the increasing prevalence and awareness of neurodegenerative diseases, many of which Received 18 May 2006; accepted 16 November 2006. Address correspondence to Christopher M. Filley, M.D., Behavioral Neurology Section, UCHSC B-183, 4200 East Ninth Avenue, Denver, Colorado 80262, USA. E-mail: christopher.filley @uchsc.edu
impair language, lends considerable importance to the study of multilingual aphasia due to progressive neurologic involvement. Among the neurodegenerative diseases, primary progressive aphasia (PPA) stands out as particularly relevant in the context of bilingual aphasia. This disease, first recognized by Mesulam in 1982 (Mesulam, 2003; Kertesz et al., 2003; Gorno-Tempini, et al., 2004), offers a useful model for the observation of progressive language decline for as long as 14 years before dementia supervenes (Mesulam, 2003). Three forms of PPA have recently been described: nonfluent progressive aphasia, associated with left inferior frontal and insular atrophy; semantic dementia, with left anterior temporal atrophy; and logopenic progressive aphasia, in which left posterior temporal and inferior parietal atrophy occurs (Kertesz et al., 2003; Gorno-Tempini et al., 2004). In contrast to stroke-related aphasia, language dysfunction in all forms of PPA continues to worsen over time and may reveal additional insights into the cerebral representation, and dissolution, of multiple languages. We report a Chinese- (Shanghai dialect) and Englishspeaking woman with PPA. To our knowledge, this is the first case of this disease to be reported in a bilingual patient.
Case report This 76-year-old right-handed woman (author B.Y.R.) has had slowly progressive language disturbance for six years. Her first symptom was subtle word finding impairment, followed by articulatory deficits and paraphasic errors. She has never experienced memory loss, personality change, executive dysfunction, impaired object or face recognition, or visuospatial deficits; depression developed for the first time after the illness began. Anti-depressant drugs have been helpful for
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Bilingual Aphasia her mood, but there has been no clear response of language problems to donepezil or memantine. The patient was born into a well-educated, Western-influenced family in Shanghai. She learned the Shanghai dialect of Chinese initially, but had early informal exposure to English from several older siblings who had studied in school, and she began formal study of British English (1 hour per day) at age 8. Much of her higher education was in English-language schools, including a degree in music pedagogy obtained in Ireland in 1951. She excelled at languages, music, and graphic arts, earned 2 degrees in teaching, and then worked in educational, drafting, and administrative settings for many years in the United States. Her husband (author A.L.R.) is an American, and English has been her household language for nearly 40 years. Her medical history is notable for hypertension, diabetes mellitus (DM), hypercholesterolemia, hypothyroidism, and childhood tuberculosis; DM has produced no hypoglycemic or other complications that could affect cognition. A sister has clinically-diagnosed Alzheimer’s disease. Neurologic examination disclosed normal cranial nerves, motor system, coordination, gait, and reflexes; mild peripheral neuropathy was present. Mental status examination was conducted in English. Her score on the Mini-Mental State Examination (MMSE; Folstein et al., (1975)) was 27/30; two points were missed on orientation and one on repetition. Her score on the Frontal Assessment Battery (Dubois et al., 2000) was normal (17/18). Speech was mildly accented but fluent, showing the influence of British English rather than Chinese. She had moderate anomia (despite an exceptional vocabulary), poor repetition, and minimally affected auditory comprehension. Reading, writing, praxis, gnosis, calculations, right-left-orientation, clock drawing (to 11:10), and comportment were preserved. Routine laboratory tests were unremarkable. An electroencephalogram was normal. Brain magnetic resonance imaging was normal for her age, with no focal atrophy and minimal white matter hyperintensity. Single photon emission computed tomography (SPECT) showed mild left temporal and parietal hypometabolism (Figure 1). Neurolinguistic testing using an adaptation of the Boston Diagnostic Aphasia Examination (BDAE; Goodglass and Kaplan, 1983) disclosed a pattern most consistent with conduction aphasia (Figure 2). Authors G.R. and L.M. evaluated
the English and author J.W. the Chinese, modifying the BDAE slightly to create fully parallel forms for Shanghai Chinese and English that were culturally and linguistically appropriate, and pro-rated the scores accordingly. Spoken output in both languages was marked by word-finding pauses, occasional articulatory awkwardness, and brokenoff phrases that disturbed the melodic line, but was otherwise fluent (e.g., normal phrase length and variety of forms). [See English speech sample, Appendix A.] Repetition and word finding were characterized by a predominant pattern of phonemic paraphasias in both languages. Performance on the Apraxia Battery for Adults (Dabul, 1986) revealed mildly increased articulatory difficulty with increasing word length, but no other symptoms of apraxia of speech, limb apraxia, or buccofacial apraxia. No weakness or incoordination of the speech musculature was observed. Speech errors were thus characterized as phonemic paraphasias rather than articulatory errors due to a motor speech disorder (e.g., apraxia of speech). As can be seen in Figure 2, performance in English and Chinese was comparably impaired in all areas with the possible exceptions of paraphasia, repetition, and conversation. Paraphasias were more evident in English, but repetition and conversation were more impaired in Chinese. The disparity in repetition performance between the 2 languages was not sufficiently large to permit a confident conclusion that a true difference existed. These observations may simply be due to normal intra-subject variation, or they may reflect inadvertent differences in the difficulty of items on the English and Chinese versions of the task. Conversation deficits were somewhat more evident in Chinese, as reflected in the Aphasia Severity Score (4.0 for English, 3.5 for Chinese), but again, this difference was not of sufficient magnitude to support a definitive conclusion. A version of the Boston Naming Test (Kaplan et al., 1976), with most of the bilingually/biculturally inappropriate items removed, also showed better performance in English (28/45) than Chinese (23/45), presumably due to much greater exposure to the English forms over the last 40 years. The striking naming difficulty characteristic of conduction aphasia, consisting of multiple paraphasic attempts at long noncompound words (harmonica, escalator; Kohn, 1984), was not paralleled in Chinese, in which all long words are compounds (escalator = self-move-electric-stair). An unusual feature of this case, for both English and Chinese, was the patient’s total inability to recall or recite poems, song lyrics, and prayers that were once completely familiar to her, although her production of automatized sequences (counting, days of the week) was normal.
Discussion
Fig. 1. SPECT scan. Mild left temporal and parietal hypometabolism is present.
We present neurologic, neuroimaging, and neurolinguistic data in this bilingual woman with progressive aphasia. The most notable feature of this unusual case is the appearance
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Boston Diagnostic Aphasia Examination Baseline Scores English Chinese Rating Scale Profile of Speech Characteristics Severity = 3.5 in Chinese and 4.0 in English 3 = The patient can discuss almost all everday problems with little or no assistance. 4 = Some obvious loss of fluency in speech or facilty of comprehension, without significant limitation on ideas expressed or form of expression.
Fluency Melodic line
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Fig. 2. Comparison of aphasia characteristics in English and Chinese using the BDAE.
of aphasia related to neurodegeneration in a woman who had native/near-native fluency in 2 completely unrelated languages. In contrast to the familiar temporal course of stroke-related aphasia, in which improvement typically occurs after the onset, this case offers the opportunity to observe the clinical features of aphasia related to neurodegeneration. The clinical and neuroimaging data in this woman are most consistent with the diagnosis of PPA. This disease, which falls in the spectrum of frontotemporal lobar degeneration (FTLD), is characterized by progressive anomia leading to aphasia, followed by evolution to dementia over a variable number of years. In our case, the profile of fluent aphasia with impaired confrontation naming, phonemic
paraphasic errors, and near normal auditory comprehension, combined with normal memory, gnosis, and other cognitive functions, is consistent with PPA. In particular, this case appears to be an example of logopenic progressive aphasia, a PPA subtype in which impaired word-finding and repetition are accompanied by mild comprehension deficits (Kertesz et al., 2003; Gorno-Tempini et al., 2004). Consistent with this neurobehavioral profile is the SPECT scan showing mild left temporal and parietal hypometabolism, a finding reported in similar cases (Gorno-Tempini et al., 2004). The impaired repetition in our patient is most consistent with conduction aphasia (Kohn, 1984 and Kohn, 1992). The deficits in word repetition resemble those of this aphasia
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Bilingual Aphasia syndrome, consisting primarily of multiple well-articulated but incomplete attempts when producing words of 4 or more syllables, each attempt containing some of the phonemes of the target. The target is occasionally produced without being recognized (Appendix B). Repetition deficit is also typical of logopenic progressive aphasia, and has been correlated with atrophy of left posterior temporal and inferior parietal areas (Gorno-Tempini et al., 2004). The origin of this deficit has been suggested to be a deficiency of phonological short-term memory and not a motor speech impairment (Gorno-Tempini et al., 2004). The patient’s performance in English and Chinese is comparable, although repetition, conversation, and naming are slightly superior in English. Performance differences at this point are not sufficiently robust to allow a definitive conclusion, as they may result from normal variation and/or differences in task difficulty between the 2 languages. We hypothesize that the recency of English usage may account for its better preservation, as B.Y.R. first learned Chinese as a child, but has spoken English as her primary language for many years. This possibility invokes a long-standing discussion about the distinction between Ribot’s Rule (Ribot, 1883), which posits that the earliest language is the one best preserved after aphasia, and Pitres’ Law (Pitres, 1895), which holds that the language most employed after aphasia is the one best maintained. However, a clear answer as to whether either of these dictums applies in our case will only be possible with the acquisition of longitudinal data. In post-stroke multilingual aphasia, many patterns of differential language impairment have been noted, and no empirical evidence exists to support any explanation for such differences (Fabbro, 2001). Moreover, the relevance of these models to progressive aphasia related to neurodegeneration is uncertain. An unexpected inability to recall or recite familiar memorized material (poems, song lyrics, prayers) is also present in both languages. A search of the relevant literature disclosed no explanation for this finding, which remains puzzling because highly familiar material would typically remain accessible to a patient with preserved memory and the absence of dementia, and her speech is only mildly impaired. We can only speculate that this deficit may relate in some way to the effects of neurodegeneration associated with PPA. The similarity of linguistic deficits in Chinese and English implies that, in this case of PPA, the two languages are represented in closely related areas of the left perisylvian cortex. This conclusion finds support from functional neuroimaging data obtained from normal bilinguals demonstrating a similar left cerebral representation of the lexicon in both L1 and L2 (Fabbro, 2001). Overall, the findings in our case suggest that the disease affects a common localization of the 2 languages, but in a differential manner reflecting variation in prior usage or other, unidentified factors. Longitudinal follow-up, currently underway, will show how performance in the two languages develops with further disease progression.
References Dabul B. Apraxia Battery for Adults. Austin, TX: PRO-ED, Inc., 1986. Dubois B, Slachevsky A, Litvan I, Pillon B. The FAB: A Frontal Assessment Battery at bedside. Neurology 2000; 55: 1621–26. Fabbro F. The bilingual brain: Bilingual aphasia. Brain Lang 2001; 79: 201–10. Fabbro F. The bilingual brain: Cerebral representation of languages. Brain Lang 2001; 79: 211–22. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state:” A practical method of grading the cognitive state of patients for the clinician. J Psychiatr Res 1975: 12: 189–98. Goodglass H, Kaplan E. The Assessment of Aphasia and Related Disorders. Philadelphia: Lea and Febiger, 1983. Gorno-Tempini ML, Dronkers N, Rankin KP, et al. Cognition and anatomy in three variants of primary progressive aphasia. Ann Neurol 2004; 55: 335–46. Kaplan E, Goodglass H, Weintraub S. Boston Naming Test. Experimental edition. Boston: Aphasia Research Center, Boston University, 1976. Kertesz A, Davidson W, McCabe P, et al. Primary progressive aphasia: Diagnosis, varieties, evolution. J Int Neuropsychol Soc 2003; 9: 710–9. Kohn SE. The nature of the phonological disorder in conduction aphasia. Brain Lang 1984; 23: 97–115. Kohn SE, editor. Conduction Aphasia. Hillsdale, NJ: Lawrence Erlbaum Associates, 1992. Mesulam M-M. Primary progressive aphasia – A language-based dementia. N Engl J Med 2003; 349: 1535–42. Paradis M. Bilingualism and aphasia. In: Whitaker H, Whitaker HA, editors. Studies in Neurolinguistics. New York: Academic Press, 1977; 3: 65–121. Pitres A. Etudes sur l’aphasie chez les polyglottes. Rev Med 1895; 15: 873–99. Ribot T. Les maladies de la mémoire. Paris: Librairie Germer Balliere, 1883.
Appendix A: Speech sample, BDAE Cookie Theft (Goodglass and Kaplan, 1983) The mother is … doing di – washing dishes and uh she is thinking and uh she is not aware the water is uh flooding the floor; a nice day, the win-win-window is open, an’ the children were uh trying to – get some – cookies in the uh the higher … (gesture, something horizontal) uh, on a upper – shelf; and the boy had to step on a – stool to reach to the – n – cookies and uh he is going to fall – fall down, and the sister was saying I want – one too.
Appendix B: Multiple attempts to name the ‘escalator’ picture on the Boston Naming Test (Kaplan et al., 1976) es-esKIGala, es, es, esKELa, ski, ESki, guh, gluh, esKELa, esKEL-ter, kes, ESkelay-ter, esKET-ter, esKETeler, ESketevei-, ?, esKELeter (and several more fragments & variations). The essentially correct production ESkelay-ter (in boldface) was unrecognized by B.Y.R., and she was unable to repeat the word when it was modeled by the examiner.
