Young Adult Stroke: Neuropsychological Dysfunction and Recovery. Jose M. Ferro, MD, and Manuela Crespo, MD

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1 98 Young dult Stroke: Neuropsyhologial Dysfuntion and Reovery Jose M. Ferro, MD, and Manuela respo, MD Etiology, neuropsyhologial defiits, aphasia type, and reovery were retrospetively studied in 54 young adults with stroke. ardia embolism was the most ommon ause of stroke in patients younger than 40, while atheroslerosis was the most frequent etiology among those aged years. In 1 aphasi patients, Broa's aphasia was the most ommon while Wernike's and transortial aphasias were rare. ompared with an older aphasi population, young patients had signifiantly more nonfluent aphasias and fewer omprehension defiits. These differenes were related to stroke loalization: the majority of infarts loalized by omputed tomography in patients involved either the entire middle erebral artery territory or its superior or deep branhes, explaining the preponderane of nonfluent aphasia. Prognosis of aphasia in our patients was better than has been reported for non-age-seleted aphasia populations. Roughly one third of our patients reovered ompletely, one third improved, and one third had an unresolved language defiit. omplete reovery and signifiant improvement were observed even > months after stroke. In some patients, reovery was muh better than might have been predited from lesion site and size depited on omputed tomograms. (Stroke 88;:98-98) Stroke in young adults represents only a small fration (approximately 4%) of strokes in North meria 1 - and most western European ountries; muh higher rates have been reported from developing ountries. 4-5 The auses of erebral infartion in young adults have been thoroughly reviewed in reent omprehensive publiations 1 ; however, only a few studies - 8 have been devoted to prognosti fators and profiles of funtional reovery from stroke in this age group. No study desribes neuropsyhologial defiits and their rate of reovery. This artile is a retrospetive review of young adults with strokes who were evaluated in our unit during years, with emphasis on neuropsyhologial sequelae and outome. Subjets and Methods We reviewed the files of 54 patients aged years referred to the Language Researh Laboratory, entro de Estudos Egas Moniz, between January and February 8 for evaluation of neuropsyhologial defiits aused by hemispheri stroke. There were men and women; From the Language Researh Laboratory, entro de Estudos Egas Moniz and Stroke lini, Department of Neurology, Hospital de Santa Maria (M..) and University of Lisbon (J.M.F.), Lisbon, Portugal. ddress for reprints: Jose' M. Ferro, entro de Estudos Egas Moniz, Hospital de Santa Maria, 0 Lisbon, Portugal. Reeived ugust II, 8; aepted Marh 4, 88. were <40 years old and 15 were between 41 and 50 years of age. The diagnosis of stroke and its etiology were based on linial and laboratory data obtained after reviewing hospital reords and were onfirmed by appropriate imaging proedures in most ases (omputed tomography [T san], erebral angiography, two-dimensional ehoardiography). The anatomi distribution of the infart was investigated in 9 patients for whom T data were available. The involved vasular territories were loalized aording to the guidelines of Damasio, 9 Ringlestein et al, l0 andzulh." Neuropsyhologial evaluation was performed in the first month after stroke for patients, between the seond and third month for patients, and after months for 54 patients. The omprehensive neuropsyhologial battery inluded four subtests for aphasia; a -item version of the token test 1 ; and tests of alexia; agraphia; buofaial, limb, and onstrutional apraxia 1 ; and hemispatial neglet. 1 Diagnosis and lassifiation of aphasia were based on numerial taxonomi riteria aording to sores on the aphasia subtests. Patients evaluated more than one were lassified as follows: ompletely reovered, test sores improved to the normal range; improved, hange to a less severe type of aphasia; stabilized, no hange in the type of aphasia based on the evaluations performed; or reurrent stroke during follow-up.

2 Ferro and respo Young dult Stroke years 1-40 years years FIGURE 1. Pie graphs of etiology of strokes in young adults between ages 15 and 0 (left), 1 and 40 (enter), and 41 and 50 years (right). ardia Embolism theroslerosis Non-atherosleroti vasulopathies Hematologi Diseases Pregnany, oral antioneptive E Other etiologies LJ Unknown O Intraerebral hemorrhage Results Following the guidelines of Hart and Miller, 1 patients were grouped into eight etiologi ategories (Figure 1): erebral atheroslerosis (89 patients), ardia embolism (8 patients inluding 54 with valvular heart disease), intraerebral hemorrhage (1 patients), vasospasm ( patients), strokes ourring during puerperium, pregnany, or due to oral ontraeptives (9 patients), hematologi diseases (5 patients), nonatherosleroti erebral vasulopathy (8 patients), and unknown etiology (9 patients). Etiology of stroke in the two younger age groups (15-0 years, 1-40 years) were almost idential. In the older patients (41-50 years), ardia embolism was less frequent, although not signifiantly so (* =.4,p<0.). mong the 4 patients with left-hemisphere lesions, 15 (1%) were aphasi, 11 (5% of 18 literates) were alexi, and 8 (% of 5 literates) had a writing disturbane. Buofaial apraxia (8 patients, 40%) was more ommon than limb apraxia (44 patients, %); 8 patients (41%) had onstrutional apraxia. Sine patients were referred to our laboratory mainly beause of speeh problems, only 0 patients with right-hemisphere strokes were tested. Of these, eight had hemispatial neglet and five showed onstrutional apraxia. rossed aphasia (aphasia due to right-hemisphere lesion in a right-handed person) was found only one. Table 1 shows the distribution of aphasia type among the 1 young adults with stroke in relation to the overall population with aphasia due to stroke evaluated at our unit during that period. Broa's aphasia was signifiantly (x = 15.0, p<0.001) more ommon while Wernike's (x = 8., p<0.005) and transortial sensory aphasia (^ =.41, p<0.5) were signifiantly less frequent among young adults. Fluent aphasia and aphasias with omprehension defiits were less ommon in young patients than in the overall stroke population (x = 1.0, p<0.001 and x =.4, p<0.001; respetively). Figure shows that this pattern is valid for all the young age groups. mong the 9 patients who had T, were exluded: 1 for tehnial reasons (artifats, poorly defined lesion boundaries, report but no T print available) that preluded detailed anatomi loalization; two had a normal T san, and nine had intraerebral hemorrhages. Infart loation on the remaining T sans is depited in Table aording to the involved vasular territories. The more ommon patterns onsisted of large infarts of the entire middle erebral artery (M) territory ( patients), involvement of the superior division of the M (9 patients), and deep lesions orresponding to the lentiulostriate territory or to a watershed infart between the ortial and subortial irulations ( patients). Parietal branhes of the M were involved in a few ases, while temporal infarts due to olusion of the inferior division of the M were unommon. Of the 9 patients who underwent T, were aphasi. Two had deep striatoapsular hemorrhages ausing mixed transortial and ondution apha- TBLE 1. Stroke in Young dults Years Old: Type of phasia Young Type of aphasia adults Nonfluent aphasias Global 0 Broa's 54 Transortial motor Transortial mixed Fluent aphasias Wernike's 1 Transortial sensory ondution nomi Total aphasias 1 Total strokes 54 *t$p<0.001, 0.005, 0.05, respetively. Total % 4* 1 4 9t 4t 0 0* 1

3 984 Stroke Vol, No 8, ugust years n - 9 1Z 481 0% X 01 W Z X Z u 8Z OZ 1 Z 0Z 1-40 years n Z B 51 Z. 8. 5Z FlGURE. Example of disparate results between lesion site and size on omputed tomogram and aphasia in young adult with stroke: large middle erebral artery infart produed only mild ondution aphasia. tal infart ausing only dysarthria, and the other was a 4-year-old woman with a massive M infart produing a mild transortial motor aphasia. Follow-up examinations were given to 4 (9%) of the 1 aphasi patients. mong these 4, (0%) reovered ompletely and 1 (%) improved; 1 (%) were stabilized and patients (5%) had a reurrent stroke (Table ). lthough signifiant improvement and omplete reovery were more ommon during the first months, some aphasi patients improved or even reovered fully later. mong 44 patients first seen in the aute period (the first month after stroke) (follow-up mean 11.9, range ±9.59 months), there were no signifiant differenes (# = 0., not signifiant) in outome among the three age groups (Table 4). 0Z years n - 98 Hi ^1 mm Z B * Z X 5Z W 8Z 1Z 9Z n qui Z p < 0. 5 FIGURE. Bar graphs of type of stroke aphasia in different age groups. G, global; B, Broa's;, transortial motor; X, transortial mixed; W, Wernike's;, transortial sensory;, anomi;, ondution. sias. mong the patients with T-demonstrated infarts, had nonfluent aphasias ( global, Broa's, transortial motor) and five had fluent aphasias ( ondution, anomi, 1 Wernike's). Exept for two ases (parietal infartions ausing Broa's and global aphasia), nonfluent speeh was always assoiated with either prerolandi, subortial, or massive M infarts. One patient with Wernike's aphasia had a temporoparietal lesion. The two patients with anomi aphasia had prerolandi and subortial infarts. The two patients with ondution aphasia had large lesions with an unommon loalization for that type of aphasia (Figure ). mong patients with nonfluent speeh, two had less severe aphasias than would have been predited by their lesion site and size on T. One patient was a 45-year-old man with a large ortio-subortial fron- Disussion Our series is a retrospetive review olleted over several years, during whih period new imaging and diagnosti tools were introdued into linial pratie enabling a better understanding of stroke type and etiology. These fats strongly limit the interpretation of our data on stroke etiology. However, our results are quite omparable to published data,1-8 exept for a higher rate of ardia embolism as a result of rheumati valvular heart disease. This finding reflets the fat that rheumati valvular heart disease is still rather ommon in Portugal.15 The loalization of erebral infarts is strongly related to their pathophysiology. Emboli tend to involve the M territory, lodging at its bifuration or trifuration or oluding its frontal, operular, or parietal branhes. arotid thrombosis an produe

4 Ferro and respo Young dult Stroke 985 TBLE. Vasular territory Stroke in Young dults Years Old: lnfart Loalization by omputed Tomography Middle erebral artery Superior division + inferior division + lentiulostriate arteries Superior division + inferior division Superior division Superior division + anterior erebral artery Superior division + lentiulostriate arteries Superior division + angular artery Lentiulostriate arteries + angular artery Lentiulostriate arteries + watershed infart Lentiulostriate arteries \ Watershed infart Terminal territory + watershed infart 1 Terminal territory + watershed infart (middle and anterior erebral arteries) 1 Posterior parietal artery 1 ngular artery Inferior division + angular artery I Inferior division Watershed infart (middle and anterior erebral arteries) horoidal anterior artery + lentiulostriate arteries 1 horoidal anterior artery 1 Watershed infart (middle and posterior erebral arteries) Posterior erebral artery Posterior erebral artery (bilateral) Watershed infart, superfiial and deep irulation. No. patients (5%) (1%) massive M, watershed, or terminal territory infarts. Launes involve mainly deep strutures suh as the thalamus and internal apsule. hanges in infart loalization with age are rarely mentioned in the literature. Our data indiate that in young adults, infarts most ommonly involve either the entire M territory, its superior division and branhes, or the lentiulostriate or terminal zones. In general, temporal infarts ausing Wernike's aphasia are believed to be of emboli origin. 1 However, in this age group temporal infarts were infrequent, indiating that emboli rarely lodge in the M inferior division. ge-related hanges in embolus size, ardia output, and ollateral blood flow might explain this finding. In young adults, a large embolus stopping at the stem of the M makes the unollateralized lentiulostriate territory vulnerable to infartion. When emboli lodge in the M bifuration, the territory supplied by the angular and temporal arteries may esape ishemia through leptomeningeal anastomoses from the posterior erebral artery. 1 Several researhers have found that patients with Broa's aphasia were signifiantly younger than those with Wernike's aphasia ording to Eslinger and Damasio, that differene ould be due to 1) hanges in stroke loi with age; ) umulative effets of mental deline assoiated with aging plus damage to language areas regardless of stroke lous; ) age-related hanges in the anatomi and physiologi mehanisms underlying language funtion, suh that regardless of lesion loation, ertain aphasia types might beome more prevalent with age; or 4) better reovery from omprehension defiit in younger adults, thereby leading to a dereased prevalene of Wernike's aphasia. Our results learly indiate that lous of stroke is the major ause of age-related hanges in aphasia TBLE. Stroke in Young dults Years Old: phasia Evolution in 4 Patients Follow-up period mo mo 1 yr >1 yr Overall Evolution («= ) (n = 8) ("=) (n = 4) ompletely reovered Improved Stabilized Reurrent stroke 8 15 Evolution defined in text. Data are number of patients Referene Kertesz 0 5 values (%) Ferro' 55 1

5 98 Stroke Vol, No 8, ugust 88 TBLE 4. Stroke in 44 Young dults Years Old: phasia Evolution During First Month fter Stroke Evolution ompletely reovered Improved Stabilized Reurrent stroke <0 (» = 9) No. % ge (yr) 1-40 No. % (n = ) No. 0 % 0 Total (JV=44) 1 type. In fat, the large number of nonfluent aphasias in young adults is the neuropsyhologial ounterpart of the predominane of prerolandi and subortial infarts in this age group. Our data suggest that the third and fourth explanations of Eslinger and Damasio may also influene the different distribution of aphasia type with age. In fat, aphasia types haraterized by impairment of omprehension, whether nonfluent (global) or fluent (Wernike's, transortial sensory), were less frequent in our young patients, indiating that omprehension defiits are either less prevalent or have a superior reovery in young adults. few patients provided exeptions to the lassi rules of lesion loation in aphasia. In two patients, postrolandi lesions produed nonfluent aphasias, while in four other patients, a more severe aphasia would have been expeted from the lesion size. Our series points out that young adults generally have a favorable prognosis, with lak of improvement demonstrated in only %. Improvement of aphasia in this age group is learly superior to that indiated in the literature on reovery (8% and 5%, respetively). 1-0 Moreover, signifiant hanges in aphasia type and severity were observed even several months after onset, showing that reovery ontinues into the hroni period, a finding rare in older patients. 0 lthough some hanges in aphasia features with age an possibly be related to modifiations in the neural network subserving language, most hanges are seondary to a different loalization of erebral infarts with age. These hanges are related to differenes in etiology and other as yet not learly established fators, suh as different embolus size or route. Referenes 1. Hart RG, Miller VT: erebral infartion in young adults: pratial approah. Stroke 8;:1-1. Grindal B, ohen RJ, Saul RF, Taylor JR: erebral infartion in young adults. Stroke 8;9:9-4. dams HP, Butler MJ, Biller J, Toffol GJ: Non hemorrhagi erebral infartion in young adults. rh Neurol 8; 4: Radhakrishair K, shok PP, Sridharan R, Mousa ME: Stroke in the young: Inidene and pattern in Benghazi Libya. da Neurol Sand 8;: braham J, Shetty G, Jose J: Strokes in the young. Stroke 1 ;:58-. Hahinsky V, Norris JW: The young stroke, in The ute Stroke. Philadelphia, F Davis, 85, pp Marshall J: The ause and prognosis of stroke in people under 50 years. J Neurol Si 8;5: Snyder BD, Ramirez-Lassepas M: erebral infartion in young adults: Long term prognosis. Stroke 80; 11: Damasio H: omputed tomographi guide to the identifiation of erebral vasular territories. rh Neurol 8; 40:18-. Ringlestein EB, Zeumer H, ngelou D: The pathogenesis of strokes from internal arotid artery olusion. Diagnosti and therapeutial impliations. Stroke 8; : Zulh KJ: The erebral Infart. Berlin, Springer-Verlag, Ferro JM: Neurologia do omportamento: Estudo de orrelagao om a Tomografia xial omputorizada. Fauldade de Mediina de Lisboa, 8 1. Ferro JM, Kertesz, Blak SE: Subortial neglet: Quantitation, anatomy and reovery. Neurology 8;:8-9. Ferro JM, Kertesz : omparative lassifiation of aphasi disorders. J lin Exp Neuropsyhol 8;9: Estatistias da Saude -8. Lisboa, Portugal, Instituto Naional de Estatistia, 8 1. Mohr JP, Gautier J, Hier DB, Stein RW: Middle erebral artery, in Barnett HJM, Mohr JP, Stein BM, Yatsu FM (eds): Stroke. New York, hurhill, 8, vol 1, p Sindermann F, Dihgons J, Bergleiter R: Olusion of the middle erebral artery and its branhes: ngiographi and linial orrelates. Brain 9;9: Obler LK, lbert M, Goodglass H, Benson F: phasia type and aging. Brain Lang 8;:18-. Obler LK, lbert ML: Language in the elderly aphasi and in the demented patient, in Sarno MT (ed): quired phasia. New York, ademi Press, 81, pp Kertesz : phasia and ssoiated Disorders: Taxonomy, Loalization and Reovery, New York, Grune & Stratton, 9 1. De Renzi E, Faglioni P, Ferrari P: The influene of sex and age on the inidene and type of aphasia. ortex 80; 1:-0. Basso, apitani E, Laiaona M, Luzzatti : Fators influening type and severity of aphasia. ortex 80; 1:1-. Eslinger PJ, Damasio R: ge and type of aphasia in patients with stroke. J Neurol Neurosurg Psyhiatry 81; 44:-81 KEY WORDS erebrovasular disorders young adults ognition disorders aphasia