Global Intellectual Deficits in Cystinosis
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1 Americn Journl of Medicl Genetics 49:83-87 (1994) Globl Intellectul Deficits in Cystinosis Brbr L.H. Willims, Jerry A. Schneider, nd Doris A. Truner Deprtments of Neurosciences (B.L.H.W.. D.A.T.) nd Peditrics (J.A.S., D.A.T.), University of Cliforni School of Medicine, L Jollu, Cliforni Fourteen fmilies of children with infntile nephropthic cystinosis were evluted using the Stnford-Binet Intelligence Scle, Fourth Edition [Thorndike et l., 1986: Stnford-Binet Intelligence Scle, Fourth Ed.]. The IQs of 15 children with cystinosis, their 23 sibs nd 24 prents were compred in order to evlute potentil effect of cystinosis on intelligence. Children with cystinosis hd significntly lower men I& thn their sibs nd their prents (P =,001). Thus, even though the men IQ of the children with cystinosis (94.4 * 10) ws within the verge rnge, there is evidence tht these children hve mild globl intellectul deficit reltive to their expected IQ bsed upon the IQs of other reltives. In ddition, to subset of the subjects we dministered mesure of scholstic bility, the Wide Rnge Achievement Test-Revised [Jstk nd Wilkinson, 1984 The Wide Rnge Achievement Test-Revised], which consists of spelling, reding, nd rithmetic subtests. The 11 cystinosis subjects scored significntly lower (P =.01) thn their 16 sibs nd their 14 prents in the re of spelling, wheres they did not significntly differ in their performnce in the res of reding nd rithmetic Wiley-Liss, Inc. KEY WORDS cystinosis, I&, cognitive development INTRODUCTION Infntile nephropthic cystinosis is n utosoml recessive disorder chrcterized by lysosoml ccumultion nd crystlline deposition of cystine in tissues including kidney, thyroid, corne, nd brin. The cystine deposits re known to cuse progressive renl nd thyroid dysfunction. Cystinosis ws originlly thought to spre the centrl nervous system; however, recent investigtions hve demonstrted cystine ccumultion in Received for publiction Mrch 11, 1993; revision received duly 6, Address reprint requests to Doris Truner, M.D., Division of Peditric Neurology, UCSD Medicl Center, 200 West Arbor Dr. #8467, Sn Diego, CA Wiley-Liss, Inc. the brin LVogel et l., 1990; Jons et l., 1987; Levine nd Ppro, 1982; Ross et l., This ccumultion my ccount for the specific cognitive deficit observed in these subjects [Truner et l., 1988,1989; Nichols et l., 1990,bl. These studies hve demonstrted n impirment in visul informtion processing in the presence of norml I&. Since there is strong positive reltionship between level of intelligence nd degree of kinship [Qler, 1965; Anstsi, one would predict tht the IQs of children with cystinosis, their sibs, nd their prents would be similr if globl intelligence remins unffected in cystinosis. However, if the cystine ccumultion in the brin does hve n effect on globl intellectul functioning, one would expect children with cystinosis to perform differently from other reltives on mesures of I&. The purpose of this study ws to exmine the IQs of children with cystinosis, their sibs, nd their prents in order to determine whether the children with cystinosis performed s well on mesure of globl intelligence s one might predict bsed on the performnce of other fmily members. METHODS Sixty-two subjects from 14 fmilies prticipted in this study, 15 with infntile nephropthic cystinosis, 19 sibs nd 4 hlf-sibs (henceforth together referred to s sibs ), nd 24 prents. Sixteen of the 23 sibs were heterozygous crriers of the cystinosis gene s were ll of the 24 prents. The children with cystinosis rnged in ge from 2.9 to 19.3 yers, the siblings from 2.6 to 34.1 yers, nd the prents from 26.2 to 62.3 yers. Nine of the children with cystinosis were femle, nd 6 were mle. Sixteen of the sibs were femle, nd 7 were mle. Thirteen of the prents were femle, nd 11 were mle. An bbrevited version of the Stnford-Binet Intelligence Scle, Fourth Edition [Thorndike et l., ws dministered to ech of these subjects s prt of lrger study. The bbrevited version consisted of Vocbulry, Pttern Anlysis, Quntittive Anlysis, Bed Memory, nd Memory for Sentences subtests. These were used to compute re scores representing the four subdivisions of the test (Verbl Resoning, AbstrctiVisu1 Resoning, Quntittive Resoning, nd Short-Term Memory), which in turn were compiled to form the composite I&. The Stnford-Binet is normed from ge 2 to 23 yers. The composite I& for ll subjects
2 &i Willims et l. older thn this ws estimted using norms for 18- through 23-yer-olds. Bckground informtion on generl helth nd school performnce ws collected on subset of the subjects. The Wide Rnge Achievement Test-Revised (WRAT-R) [Jstk nd Wilkinson, ws lso dministered to subset of our subjects s mesure of their school performnce in the res of reding, spelling nd rithmetic. This subset included 11 of the cystinosis subjects, 16 of the sibs, nd 14 of the prents in our study. Informed consent ws obtined prior to testing ech subject in ccordnce with the Investigtionl Review Bord t the University of Cliforni, Sn Diego. The reltionship of subject I& with subject group, sex, ge, nd sib heterozygous crrier sttus ws nlysed by one fctor nlysis of vrince (ANOVA) using IQs compiled with nd without the Bed Memory subtest. The Bed Memory subtest ws excluded in some of the nlyses of I& becuse it hs been shown to be sensitive to the visul sptil deficits of cystinosis subjects [Truner et l., 1988, nd s such ws possible confounding vrible to the clcultion of I& in these subjects. The reltionship of subject I& with ge ws nlysed using simple regression nlysis. In ddition, the reltionship between subject group nd subject WRAT-R performnce ws nlysed by one fctor ANOVA for ech of the 3 subtests. Two of the 15 cystinosis subjects hd received renl trnsplnts severl yers prior to testing. Of the remining 13 subjects with cystinosis, 4 were tking cystemine t the time of testing, nd 9 were tking phosphocystemine. Four of the subjects were tking low dose regimen (1.3 g/m2/dy) of mediction, nd 9 were tking high dose regimen (1.95 g/m2/dy). Anlyses were run to determine whether tretment type, dose, durtion, or ge t onset of tretment were determinnt of I&. To determine the level of renl functioning, 13 of the 15 cystinosis subjects hd cretinine clernce mesured ner the time (within men = 1.9? l.6 months) of psychometric testing. Cretinine clernce (ml/ mid1.73 m2) ws defined using the following formul: height (cm) x 0.55iserum cretinine (mgidl) [Schwrtz et l., Regression nlyses were run to determine ifiq ws correlted with cretinine clernce (see Fig. 1). The thyroid function of the subjects with cystinosis in our study ws crefully monitored with T4 nd TSH determintions. None of the children were on crnitine tretment t the time of the study y = ~ R = I Cretinine Clernce (mllmin11.73m2) Fig. 1. Reltionship between I& nd cretinine clernce in 13 subjects with nephropthic cystinosis. Although there is trend towrd higher IQ with higher cretinine clernce, this reltionship 1s not significnt. RESULTS The men composite I& scores of the children with cystinosis, their sibs, nd their prents re summrized in Tble I. These men IQs ll lie within the norml rnge of the Stnford-Binet. The men I& scores of heterozygous sibs nd nonheterozygous sibs did not differ significntly nd were nd , respectively. Therefore for these nlyses they were considered s one group. All nlyses were run using the I& score compiled including the Bed Memory subtest nd the I& score compiled excluding the Bed Memory subtest. The results of nlyses of I& with Bed Memory nd those without Bed Memory were entirely consistent with one nother. ANOVA showed tht the 3 groups differed significntly on men composite I& (P =.001), nd plnned comprisons were significnt t 95% for comprisons of children with cystinosis to both their sibs nd prents. There were no significnt differences in I& between mles nd femles in ny of the 3 groups. Age did not TABLE I. Men Stnford-Binet IQs (4th Edition) Totl no. No. femle No. mle Age (yers) I& wlbm" I& wio BM Children with cystinosis * k 11 All siblings k ? ? 8.6 Crrier siblings k * k 10 Noncrrier siblings ? t 3.2 Prents k _t k 12.4b BM, Bed Memory. n = 23, unble to clculte the I& without Bed Memory of one of the femle subjects.
3 TABLE 11. Men Wide Rnge Achievement Test: Revised Results Reding Spelling Arithmetic Totl no. stndrd stndrd stndrd of subjects score score score Cystinosis subjects & & Siblings k & Prents t k * 11 Cystinosis nd I& 85 significntly correlte with I& for the sibs or the children with cystinosis. The men scores for the WRAT-R in the res of reding, rithmetic nd spelling re found in Tble 11. The three groups did not significntly differ in performnce on the reding nd rithmetic subtests of the WRAT-R. A one-wy ANOVA reveled tht group nd WRAT-R spelling performnce did significntly differ (P =.01) nd plnned comprisons showed tht the children with cystinosis (Spelling Stndrd Score = ) scored significntly lower thn their prents (SS = 103 t 12) nd sibs (SS = 100 t 16). The IQs of the 2 subjects evluted postrenl trnsplnt were 97 nd 87; the men of the remining 13 subjects ws 95.0? 11. When nlyses were run without the trnsplnted subjects, ANOVA showed tht the groups still significntly differed on I& (P =.009), but the plnned comprison showed tht the cystinosis subjects significntly differed from the sibs nd not the prents. There were no significnt differences found between the IQs of subjects who were medicted with cystemine compred to those tking the lterntive vrint of the drug, phosphocystemine. There ws lso no significnt difference between subjects who were tking high versus low doses of the 2 drugs. Neither the durtion of medicl tretment nor ge t onset of tretment correlted with IQ (Tble 111). Two of the 15 subjects hd cretinine clernce levels tht were below the norml to mildly bnorml rnge (<50 mliminll.73 m2). I& ws found not to be significntly correlted with cretinine clernce levels through regression nlysis (R =.341). Four of the subjects were being treted for hypothyroidism t the time oftesting. Their men I& ws 95.5 * 6 which did not differ significntly from the I& of the remining 11 subjects (men I& = 94.0 t 11). DISCUSSION Previous studies [Wolff et l., 1982,19891 hve shown I& to be within the norml rnge in subjects with cystinosis, nd bsed on these findings they hve concluded tht there ws no negtive effect on I& in cystinosis. However, these studies did not compre cystinosis subjects with their sibs or prents. Results of our present study indicte tht despite hving IQs within the norml rnge, children with infntile nephropthic cystinosis my hve previously undetected globl intellectul impirment. This conclusion is bsed on the significntly lower men I& of cystinosis subjects when compred to tht which would be predicted bsed on the IQs of their sibs nd prents. This result indictes possible neurotoxic effect of progressive cystine ccumultion in the brin. Other possible cuses for their poorer performnce include chronic renl filure, renl trnsplnttion, cquired hypothyroidism, side effects of their tretment mediction, ndlor psychosocil fctors relted to chronic illness. Previous studies hve shown tht children with cystinosis hve specific cognitive impirment in the processing of visul informtion. These deficits were not seen in subjects with chronic renl dysfunction from other cuses [Truner et l., 1988, Therefore, these studies indicte tht the visul sptil impirment in children with cystinosis seems to be relted to the underlying metbolic disorder rther thn to the effects of their renl dysfunction. The findings of the present study my lso relte to the underlying metbolic disorder. It is possible tht impired renl function could contribute to the reltive I& depression seen in our cystinosis subjects. To exmine this possibility, we determined cretinine clernce, s mesure of renl function, on 13 of the 15 subjects ner the time of their I& evlution. I& ws not significntly correlted with the cretinine clernce. Only 2 of the 15 subjects hd cretinine clernce levels tht were below the norml to mildly bnorml rnge (<50 mlimid1.73 m2). Since the mjority of the cystinosis subjects hd renl function within norml to mildly bnorml limits ner the time of testing, nd since the level of cretinine clernce did not significntly correlte with I& performnce, it is unlikely tht renl impirment contributed substntilly to the I& depression of these subjects. Two of the 15 cystinosis subjects in the study hd received kidney trnsplnts severl yers prior to our testing. It is difficult to ssess whether their renl fil- TABLE 111. Cvstemine Usge Dt Low dose/ High dose/ Low dose/ High dose/ phosphocystemine phosphocystemine cystemine cystemine (men c S.D.) (men? S.D.) (men & S.D.) (men) Number of subjects Men I& 95.3 L * & Men tretment durtion (in yers) 2.85 L t c.lo 6.61 Men tretment strting ge (in yers) 1.67 & c I
4 86 Willims et l. ure erlier in life hd n impct on their I&. The composite I& scores of these 2 ptients were 87 nd 97 which re within the rnge of the cystinosis subjects without trnsplnts (men I&: 95.0 * 11). We cnnot rule out ltogether the possibility tht chronic renl problems nd renl trnsplnttion contribute to lower I&. However, since the 2 trnsplnted subjects hd I& levels comprble to those of the subjects without trnsplnts, trnsplnt sttus mkes no obvious contribution to the I& depression found in the present study. Acquired hypothyroidism is potentil compliction of infntile nephropthic cystinosis, due to the extensive ccumultion of cystine in the thyroid glnds of these subjects. The thyroid function of the subjects with cystinosis in our study ws crefully monitored with T4 nd TSH determintions. The children received tretment s soon s TSH levels becme elevted, prior to development of clinicl hypothyroidism. Since tretment is prompt, it is unlikely tht thyroid dysfunction plys significnt role in the I& depression seen in the subjects in our study. Depression of I& is recognized compliction of untreted congenitl hypothyroidism [Murphy et l., It is thought tht hypothyroidism hs its gretest effect on humn cognitive functioning in the first severl months of life [%vet et l., The subjects in our study undergoing tretment for hypothyroidism ll developed elevted TSH levels fter ge 2 yers nd were treted within 3 months of the increse. Only 4 of our subjects with cystinosis were on thyroid replcement mediction t the time of testing. Their men I& ws 95.5 & 6 which did not differ significntly from the I& of the remining 11 subjects (men I& = 94.0 r 11). Another possible fctor contributing to the I& differences of the children with cystinosis is the effect of cystemine nd phosphocystemine on the brin. It is unknown whether these medictions cn penetrte the blood brin brrier in humns. Thus, the effect of these drugs on brin levels of lysosoml cystine ccumultion is unknown. In our study, there re very few cystinosis children who hve never received cystemine tretment. Therefore, comprisons cnnot be mde between those subjects tht hve received tretment nd those tht hve not. Consequently, there is not enough informtion to know if cystemine hs ny effect, either positive or negtive, on I&. To exmine the effects of cystemine nd phosphocystemine tretment on I&, comprisons were mde between subjects bsed on tretment durtion nd ge t onset of tretment. Thirteen of the 15 children with cystinosis were prticipnts in study of cystemine or phosphocystemine tretment. The durtion of the tretment nd the ge of tretment onset did not correlte with I&. Thus, we hve no evidence tht the cystemine tretment sttus of the cystinosis subjects in this study contributed to their I& scores. Potentil psychosocil fctors tht might hve contributed to the observed difference in I.&. include feeling poorly becuse of the underlying illness, poor school ttendnce, nd the dverse impct of short stture nd the ppernce of being younger thn their chronologicl ge. Once these children were dignosed with their metbolic disorder, their medicl problems were wellcontrolled. There ws no evidence, by prentl report, tht the children were chroniclly ftigued or felt poorly most of the time. With reference to the short stture nd youthful ppernce, we hve no mens of ssessing the potentil negtive impct on I.&. of these conditions. We re in the process of conducting studies of behvior, personlity, nd socil skills in children with cystinosis. Such studies my provide more informtion regrding the effects of psychosocil difficulties on cognitive function or performnce. We do hve informtion regrding school ttendnce. One of the complictions of chronic illness is missing more school thn the verge child. This in turn my contribute to poorer performnce on stndrdized tests. Informtion on school ttendnce ws obtined on 13 of the 15 children with cystinosis nd on 15 of the 23 sibs. In generl, the children with cystinosis nd their sibs tended to receive public schooling, performed within the verge to bove verge rnge in school s did their sibs, nd missed bout the sme mount of school s their sibs. One child with cystinosis received home schooling s did his sib. Only one child with cystinosis received ny specil eduction, wheres 2 sibs received specil eduction nd one sib ws in speech therpy. Since the children with cystinosis in this group of subjects re so similr to their sibs in terms of school ttendnce nd performnce, it is unlikely tht the psychosocil effects of chronic illness nd school bsence re relted to the significntly lower I& reltive to their sibs noted in this study. In ddition, to further exmine school performnce, subset of 11 cystinosis subjects in this study ws compred to their 16 sibs nd 14 prents on the WRAT-R. The cystinosis subjects did not perform significntly differently from their sibs nd prents on mesures of reding nd rithmetic. However, they did perform significntly less well thn their sibs nd prents on the spelling subtest. Further studies re required to determine the significnce of potentil isolted problem with spelling in this group. The lower globl I& scores found in this study do not pper to be direct function of the problems with visul processing noted in children with cystinosis. To ddress this possibility, nlyses were run excluding the Bed Memory subtest from the I& tbultion. This tsk evlutes short-term visul memory, nd Truner et l. [ previously reported tht subjects with cystinosis perform more poorly on this test thn do unrelted controls. Even with the Bed Memory subtest excluded from the nlyses, the significnt differences in I& remined. Thus, it is likely tht their lower I& scores re not due solely to their visul processing deficit, but rther to more globl intellectul impirment. Finlly, it is possible tht the cognitive chnges we re observing re not due to the cystinosis, but rther to closely linked gene tht is lso ffected. This is n intriguing possibility tht is being explored further. Now tht children with cystinosis re surviving into dulthood, the effects of progressive cystine ccumultion on the brin need to be exmined. Further study is needed to clrify the origin of these cognitive deficits s
5 Cystinosis nd I& 87 well s to ssess the potentil effects of vrious tretment modlities. ACKNOWLEDGMENTS This reserch ws supported by NIHPHS grnt NIH- 2R01 HD23854 nd in prt by grnt from the generl clinicl reserch center: M01-RR00827 of the NCRR, NIH. REFERENCES Anstsi A (1958): Differentil Psychology (3rd edition). New York, NY: The Mcmilln Compny, pp Jstk S, Wilkinson GS (1984): The Wide Rnge Achievement Test- Revised. Wilmington, Delwre: Jstk Assocites, Inc. Jons AJ, Conley SB, Mrshll R, Johnson RA, Mrks M, Rosenberg H (1987): Nephropthic cystinosis with centrl nervous system involvement. Am J Med 83: Levine S, Ppro G (1982): Brin lesions in cse of cystinosis. Act Neuropthol (berl) 57: Murphy GH, Hulse JA, Smith I, Grnt DB (1990): Congenitl Hypothyroidism: Physiologicl nd Psychologicl Fctors in Erly Development. J Child Psycho1 Psychit 31: Nichols SN, Bllntyne AO, Hodge EL, Truner DA (1990): Further chrcteriztion of the visul processing deficit in nephropthic cystinosis. Society for Neuroscience Abstrcts 16:1240. Nichols SL, Press GA, Schneider JA, Truner DA (1990b): Corticl trophy nd cognitive performnce in Infntile Nephropthic Cystinosis. Peditr Neurol 6: Ross DL, Strife CF, Towbin R, Bow KE (1982): Nonbsorptive hydrocephlus ssocited with nephropthic cystinosis. Neurol 32: %vet JF, Westbrook D, Ehrlich RM (1984): Neontl Thyroid Deficiency: Erly Tempermentl nd Cognitive Chrcteristics. J of the Am Acdemy of Child Fsychit 23:lO-22. Schwrtz GJ, Hycock GB, Edelmnn CM Jr, Spitzer A (1976): A simple estimte of glomerulr filtrtion rte in children derived from body length nd plsm cretinine. Peditr 58: Thorndike R, Hgen E, Sttler J (1986): Stnford-Binet Intelligence Scle, Fourth Ed. Chicgo, Illinois: Riverside Publishing. Truner DA, Chse C, Bllntyne A, Tlll P, Schneider J (1989): Ptterns of visul memory dysfunction in children with cystinosis. Ann of Neurol 26:436. Truner DA, Chse C, Scheller J, Ktz B, Schneider J (1988): Neurologic nd cognitive deficits in children with cystinosis. J of Peditr 112: Ilk LE (19651: The Psychology of Humn Differences (3rd edition). New York, NY: Appleton-Century-Crofts, pp Vogel DG, Mlekzdeh MH, Cornford ME, Schneider JA, Shields WD, Vinters HV (1990): Centrl nervous system involvement in nephropthic cystinosis. J Neuropthol nd Experimentl Neurol 49: Wolff G, Ehrich JH, Offner G, Bodehl J (19891: Cognitive nd scholstic functioning in ptients with Infntile Nephropthic Cystinosis. VIIth Congress of the Interntionl Ped Nephrol Assn, Toronto, # Wolff G, Ehrich JH, Offner G, Brodehl J (1982): Psychosocil nd intellectul development in twelve ptients with Infntile Nephropthic Cystinosis. Act Peditr Scnd 71:
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