Behavioral profiles of children with infantile nephropathic cystinosis
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1 Behviorl profiles of children with infntile nephropthic cystinosis Gustvo Delgdo MD, Southern Cliforni Permnente Medicl Group; Amy Schtz PhD; Shron Nichols PhD, Deprtment of Neurosciences, School of Medicine; Mrk Appelbum PhD, Deprtment of Psychology; Doris Truner* MD, Deprtments of Neurosciences nd Peditrics, University of Cliforni, Sn Diego, School of Medicine, L Joll, USA. *Correspondence to lst uthor t Deprtment of Neurosciences, University of Cliforni, Sn Diego, School of Medicine, 9500 Gilmn Drive, L Joll, CA , USA. E-mil: dtruner@ucsd.edu Children with infntile nephropthic cystinosis hve evidence of visuosptil nd rithmetic deficits on bckground of norml intellectul nd verbl skills. This study imed to define further their behviorl phenotype. The Achenbch Child Behvior Checklist ws completed by prents of: 64 children nd dolescents with cystinosis (33 femles, 31 mles; men ge 8y 8mo, rnge 4 to 16y, SD 2y 11mo); 101 helthy controls (47 femles, 54 mles; men ge 8y 4mo, rnge 4 to 16y, SD 2y 11mo); 21 children nd dolescents with cystic fibrosis (CF), termed chronic-disese controls (9 femles, 12 mles; men ge 11y 3mo, ge rnge 4 to 17y, SD 3y 5mo). Compred with helthy controls, individuls with cystinosis hd evidence of significntly higher incidence of behviorl problems, including socil problems, somtic complints, nd ttention problems. Compred with the chronic-disese control group, the cystinosis group differed only on the Socil Problems scle, with 22% of prticipnts with cystinosis scoring in the t risk rnge wheres no prticipnt with CF received n elevted score on this scle. We conclude tht children nd dolescents with cystinosis hve evidence of significnt incidence of socil difficulties compred with individuls with nother chronic illness nd helthy prticipnts. The combintion of visuosptil problems, difficulty with rithmetic, ttention problems, nd socil difficulties seen in the cystinosis group constitutes behviorl phenotype of this genetic disorder. This cluster of cognitive nd behviorl symptoms is lso seen in the nonverbl lerning disbilities syndrome, nd suggests possible erly difference in brin development in children with cystinosis compred with children who do not shre this genetic disorder. See end of pper for list of bbrevitions. Cystinosis is n utosoml recessive metbolic disorder in which cystine crystls ccumulte in vrious body tissues including the kidney, corne, thyroid, nd brin (Ghl et l. 2001). The genetic bnormlity is deletion of the CTNS gene mpped to chromosome 17p13 (Town et l. 1998). This gene encodes membrne protein, cystinosin, which is responsible for trnsporting cystine cross the lysosoml membrne. Children develop renl Fnconi syndrome in infncy, nd if untreted hve renl filure before 10 yers of ge. With the dvent of tretment with orl cystemine, cystine-depleting compound, individuls with cystinosis re living longer nd helthier lives, nd renl filure my be delyed or prevented (Ghl et l. 1987, Mrkello et l. 1993). This hs llowed studies of neurologicl, cognitive, nd behviorl function in individuls with cystinosis (see Truner et l. 1988, 1989). Truner et l. (1988) reported tht children with cystinosis hd norml composite intelligence quotients (IQs) on the Stnford-Binet Intelligence Scle Fourth Edition (Thorndike et l. 1986) hd low scores on the bed memory subtest, suggesting the possibility of specific visul memory deficits. Although intelligence is norml in ptients with cystinosis, IQ tends to be somewht lower thn expected compred with prents nd siblings (Willims et l. 1994). Acdemic performnce lso ppers to be dversely ffected in some children with cystinosis. Bllntyne et l. (1997) reported tht children with cystinosis, compred with normlly developing controls, performed significntly lower on tests of rithmetic nd spelling thn did controls. Subsequent studies hve further defined the nture of the cognitive dysfunction. Deficient performnce of ptients with cystinosis reltive to controls hs been demonstrted on tsks involving sptil reltions (Truner et l. 1989), visul motor skills (Scrvie et l. 1996), nd tctile perception (Colh nd Truner 1997). Recently, the nture of the visul processing deficit hs been more clerly specified (Bllntyne nd Truner 2000). Individuls with cystinosis demonstrte dissocition in visul processing bilities, with visuosptil functions being significntly more impired thn visul perceptul functions. So fr, only one study hs exmined the reltion between brin structurl chnges nd cognitive performnce in cystinosis. Nichols et l. (1990) compred mgnetic resonnce imging (MRI) findings with results of cognitive testing in individuls with cystinosis to determine whether corticl trophy ws ssocited with cognitive impirment. They showed tht ptients with greter degree of corticl trophy hd worse performnce on visul short-term memory tsk. The presence of specific visul processing nd tctile perceptul deficits, nd the reltively poorer chievement in rithmetic nd spelling, re reminiscent of the pttern seen with nonverbl lerning disbilities (NVLDs; Rourke 1982). Children with NVLD typiclly hve difficulty with visuosptil orienttion, poor visul memory, nd deficiencies in ttention to visul nd tctile input (Rourke 1988). Such children lso hve low socil competence nd difficulty dpting to novel situtions, which is often reflected in behviorl problems (Rourke 1989). Although the cognitive profiles ssocited with cystinosis hve been studied in some detil, the behviorl phenotype (O Brien nd Yule 1995) hs not been well chrcterized. The current study imed to define better the behviorl ptterns of children nd dolescents with cystinosis. We used the Achenbch Child Behvior Checklist (CBCL; Achenbch 1991), Developmentl Medicine & Child Neurology 2005, 47:
2 to ssess vrious spects of prticipnt behvior. Becuse children with cystinosis hve chronic medicl condition tht my set them prt from other children, it ws deemed importnt to compre the results of the CBCL in individuls with cystinosis not only with helthy controls but lso with chronic-disese control group consisting of children nd dolescents with cystic fibrosis (CF). The rtionle for choosing this chronic-disese control group ws tht the demnds of CF on socil interctions might be similr to those for cystinosis. In both conditions, children require dily medictions; both require intermittent hospitliztion nd, potentilly, more frequent bsences from school. Method PARTICIPANTS Prents of 186 children nd dolescents completed the CBCL. The children included 64 individuls with cystinosis (33 femles, 31 mles; men ge 8y 8mo, rnge 4 to 16y, stndrd devition [SD ] 2y 11mo), 101 typiclly developing, controls (47 femles, 54 mles; men ge 8y 4mo, rnge 4 to 16y, SD 2y 11mo), nd 21 children nd dolescents with CF (9 femles, 12 mles; men ge 11y 3mo, rnge 4 to 17y, SD 3y 5mo). Prents of children nd dolescents with cystinosis were either contcted by mil nd sked to prticipte, or sked to complete the CBCL t the nnul Ntionl Cystinosis Foundtion conference. No individul with cystinosis ws undergoing dilysis, ws in renl filure, or hd severe renl insufficiency, t the time the questionnire ws completed. Normlly developing controls were recruited from the community over the sme time period. At the University of Cliforni, Sn Diego (L Joll, CA, USA), prents of children with CF were sked to complete the questionnire during clinic visit or during their child s hospitl dmission. Informed consent ws obtined in ccordnce with UCSD Institutionl Review Bord procedures, nd the study complied with the Ethicl Principles of the Americn Psychologicl Assocition. Fmilies in ll three groups were group-mtched for socioeconomic sttus using the Hollingshed Four Fctor Index of Socil Sttus (AB Hollingshed 1975; Yle University, unpublished). MEASURE The CBCL ws used to ssess the sociobehviorl chrcteristics of children nd dolescents in ll three groups. The CBCL is widely used nd well-stndrdized prentl report questionnire for children nd dolescents ged 4 to 18 yers tht hs stisfctory vlidity nd relibility (Achenbch 1991). The CBCL is 113 item checklist. Ech item is scored on 0 to 2 response scle, where 0=not true, 1=somewht or sometimes true, nd 2=very true or often true. The responses re bsed on current observtions or behviors observed within the 2 months before completion of the questionnire. From these items, the following nine behvior problem scles re derived: Withdrwn, Somtic Complints, Anxious/Depressed, Socil Problems, Thought Problems, Attention Problems, Delinquent Behvior, Aggressive Behvior, nd Sexul Problems. An Internlizing score is derived by combining scores from the Withdrwn, Somtic Complints, nd Anxious/Depressed scles, nd n Externlizing score is derived by combining the scores on the Delinquent Behvior nd Aggressive Behvior scles. A Totl Behvior Problems score is derived from the ddition of scores on ll nine behvior problem scles s well s scores on the items tht do not contribute to ny of the behvior problem scles (with the exception of the llergy nd sthm items, which do not contribute to ny scle or the totl score). Rw scores re trnslted to T scores, with scores bove 70 indicting cliniclly significnt problems, nd scores of 67 to 70 representing borderline clinicl rnge. ANALYSES A T score of 67 or bove on ech scle ws chosen s n indictor of possible psychosocil problems. For ech group, ptients were divided into cliniclly t risk group nd norml group by using the cutoff score of 67 on ech of the scles, nd, in ddition, two sets of χ 2 nlyses were performed to exmine differences between the groups. One set exmined differences between the cystinosis nd control groups. A second set of nlyses exmined differences between the cystinosis nd CF groups. Tble I: Men (SD) T scores of individuls cliniclly t risk (T score 67) on the Child Behvior Checklist (CBCL; Achenbch 1991) scles for cystinosis, cystic fibrosis, nd helthy control groups CBCL scles Cystinosis (n=64) Cystic fibrosis (n=21) Helthy control (n=101) Men (SD) % Men (SD) % Men (SD) % Withdrwn 54.8 (5.8) (4.2) (5.1) 3.0 Somtic Complints 61.2 (8.9) (8.1) (6.1) 5.0 Anxious/Depressed 54.3 (6.1) (5.6) (5.4) 4.0 Socil Problems 59 (10.0) (5.4) (4.6) 2.0 Thought Problems 54.5 (6.8) (5.7) (4.8) 2.0 Attention Problems 56.8 (9.5) (7.3) (4.0) 2.0 Delinquent Behvior 55.0 (6.3) (4.3) (4.8) 3.0 Aggressive Behvior 56.3 (7.6) (6.2) (3.7) 0 Sexul Problems 51.6 (4.8) (4.7) (6.2) 4.6 Internlizing 49.4 (10.0) (11.0) (10.0) 4.0 Externlizing 45.7 (9.1) (10.9) (11.1) 2.0 Totl Behvior Problems 46.7 (9.5) (10.3) (10.8) 3.0 Sexul problems re not prt of CBCL for children <11 yers old (cystinosis n=50, helthy controls n=87, cystic fibrosis n=10). 404 Developmentl Medicine & Child Neurology 2005, 47:
3 RESULTS Tble I lists the men T scores nd the percentge of children who obtined T score of 67 or bove for ech of the scles in ech of the three groups. Men T scores for ll three groups were well within the verge rnge. However, when the percentge of children in ech group who scored within the cliniclly t risk rnge (T score 67) ws tken into ccount, there were significnt differences mong groups. Upon comprison of the cystinosis group with the helthy control group, differences between rtes of cliniclly significnt scores were observed on the Totl Problems Summry scle (29% cystinosis vs 3% control group; χ 2 =13.17, p=0.001) nd the Internlizing Problems Summry scle (14% cystinosis vs 4% helthy control group; χ 2 =5.36, p=0.02), wheres there ws no significnt difference between the two groups on the Externlizing Summry scle. Exmintion of the individul clinicl scles lso found differences between the cystinosis nd control group in rtes of scores obtined in the cliniclly significnt rnge on Socil Problems (21.5% vs 2%; χ 2 =17.37, p ), Somtic Complints (27.7% vs 5%; χ 2 =17.14, p ), Attention Problems (18.5% vs 2%; χ 2 =13.91, p 0.001), Thought Problems (9% vs 2%; χ 2 =4.53, p=0.03), nd Aggression (11% vs 0%; χ 2 =11.36, p=0.001; Fig. 1). Direct comprison of the cystinosis nd CF groups reveled tht only the Socil Problems scle significntly differed between the two chronic-disese groups (21.5% cystinosis vs 0% CF group; χ 2 =5.40, p=0.025). Most of the items identified by prents of children with cystinosis s being problem in the socil domin were cting younger thn their ge, clinging to dults excessively, nd preferring to ply with younger children. Discussion This study demonstrtes tht children with cystinosis re t higher risk for behviorl difficulties, nd, in prticulr, socil problems, compred with either helthy controls or children with nother chronic illness: CF. Although the group mens for ll scles of the CBCL were within the norml rnge for ll three groups, the percentge of children in the cystinosis group with evidence of socil problems ws significntly higher thn the percentges of children in either the CF or control groups. Children with cystinosis were significntly more likely thn helthy controls to hve problems relted to ttention, somtic complints, nd ggression. The use of chronic-disese control group llowed us to control for possible nonspecific effects on behviorl nd socil function of chronic illness lone (Thompson et l. 1987, Mulhern et l. 1989, Grtstein et l. 1999). It my be expected tht living with chronic disese my cuse ny number of behviorl problems. The pttern seen in the cystinosis group of incresed socil problems, somtic complints, ttention problems, nd ggressive behviors suggests tht these individuls re experiencing more behvior problems thn typiclly developing children. However, when compred with nother group of children living with chronic illness (i.e. CF), children with cystinosis exhibited significntly higher incidence of socil problems only. The Socil Problems scle consists of eight items tht tp the following res of the child s behvior or socil experience: cts too young for his/her ge, clings to dults or is too dependent, does not get long with other children, is tesed lot, is not liked by other children, is overweight, is poorly coordinted or clumsy, nd prefers being with younger children (Achenbch 1991). Children with cystinosis tend to be poorly coordinted (Truner et l. 1988), but this fctor lone would not explin the differences in scores found in the current study. Immture behvior (cting younger, clinging to prents nd preferring to ply with younger children) ws more commonly reported in the cystinosis group thn in either the CF or control groups. Whether this reflects neurobiologicl influence on behvior in cystinosis is uncler. However, previous Cliniclly t risk prticipnts (%) b Cystinosis Cystic fibrosis Helthy Totl Problems Internlizing Externlizing Withdrwn Somtic Complints Anxious/Depressed Socil Problems Thought Problems Attention Problems Delinquent Behvior Aggressive Behvior Sexul Problems Child Behvior Checklist scles Figure 1: Percentge of individuls in cystinosis, cystic fibrosis, nd helthy control groups with T scores 67 for ech Child Behvior Checklist scle. Significnt difference between cystinosis nd helthy nd cystic fibrosis (CF) control groups; b significnt difference between cystinosis nd CF groups. Behviorl Profile in Cystinosis Gustvo Delgdo et l. 405
4 studies using the CBCL showed tht prticipnts with CF, when compred with ptients with mixed neurologicl disorders, hd significntly lower sociobehviorl morbidity, prticulrly in the re of socil competence (Pumrieg et l. 1990). This is in contrst to our findings on children with cystinosis, whose gretest re of difficulty ws in socil competence. If the behviorl difficulties observed in children with cystinosis re not solely the result of deling with chronic illness, then wht other resons might explin the observed risk for socil dysfunction? Possible explntions include dmge to neuronl function from cystine ccumultion in the brin; difference in brin development cused by n s yet unknown function of the cystinosin gene; or n effect of one or more of the medictions used to tret the symptoms of cystinosis. Previous studies demonstrting impirments in visul processing (Bllntyne nd Truner 2000), visul memory (Truner et l. 1988, Nichols et l. 1990), tctile recognition (Colh nd Truner 1997), nd rithmetic (Bllntyne et l. 1997), combined with our current findings tht children with cystinosis hve n incresed incidence of socil difficulties, suggest tht individuls with cystinosis my be mnifesting behviorl phenotype similr to tht found in children with NVLDs. Children with NVLD hve pttern of dysfunction which includes problems with tctile perception, visuosptil skills, ttention, nonverbl memory, rithmetic, nd socil competence (Rourke 1982, 1988). Rourke (1989) hs suggested tht the socil deficits observed in individuls with NVLD my be understood by using cognitive developmentl model. Erly lerning is dependent on sensorimotor functioning, i.e. lerning through touch, vision, nd movement. However, children with NVLD, s well s children with cystinosis, hve been shown to hve specific deficits in visuosptil nd tctile skills. Socil interction, in prticulr, relies on the perception, evlution, nd ppliction of nonverbl cues, which hve been found to be deficient in children with NVLD (Rourke 1989). As such, children with NVLD my be expected to withdrw from socil situtions nd become socilly isolted, which my result in socil problems similr to those pinpointed in children with cystinosis in the present study. Rourke (1989) postultes tht dmge to or deficiency in white mtter erly in development my ccount for the NVLD syndrome. Interestingly, MRI studies of children nd dults with cystinosis demonstrte primrily bnormlities of white mtter (Nichols et l. 1990, Hodge et l. 1992). Although the cuse of the chnges to white mtter in cystinosis is unknown, these bnormlities my be present even in young children, nd suggest tht there my be n erly difference in myelintion, perhps cused by the metbolic bnormlities. Such n erly disruption in brin myelintion could ccount for the differences in cognitive function observed in individuls with cystinosis. All of the individuls prticipting in this study were receiving cystemine tretment, nd none hd significnt renl dysfunction or metbolic derngements t the time of the study. Becuse of this fct, it ws decided not to use children with chronic renl filure s chronic-disese control group. Children in the ltter group my be undergoing frequent dilysis nd hve metbolic disturbnces, such s uremi, which might result in behviorl disturbnces (Fielding et l. 1985; Eisenhuer et l. 1988; Reynolds et l. 1990, 1991; Dvis et l. 1996; Prk et l. 1996). It is difficult to determine the effect tht cystemine therpy hs on neurocognitive complictions in cystinosis. At present, most children with cystinosis hve been tking this cystinedepleting drug from erly life. The potentil effects on longterm neurobehviorl function s result of reducing cystine ccumultion re unknown. One limited retrospective study showed reversl of brin computed tomogrphy scn bnormlities nd resolution of neurologicl symptoms in two out of four ptients treted with cystemine over period of months to yers (Broyer et l. 1996). It is possible tht our popultion with cystinosis might hve hd more severe behviorl dysfunction without the benefit of cystemine therpy. There re severl possible confounding fctors in interpreting the dt from the present study. Perhps there is greter psychosocil consequence of disese mnifesttions in ptients with cystinosis thn those with CF, which results in lower socil competence. For instnce, incresed urinry frequency, common to ptients with cystinosis, my influence socil development more thn deling with shortness of breth or pulmonry infections in ptients with CF. Further, some uthors hve cutioned bout the use of the CBCL in children with chronic illnesses, s certin items tht refer to medicl dignoses or physicl symptoms might erroneously be ttributed to behviorl problems when they could be mnifesttion of side effects from mediction or directly from the medicl condition (Perrin et l. 1991). Of the items on the CBCL, there re only few questions tht directly relte to illness or mediction, rther thn the ctul behviorl problems (e.g. pin in eyes or stomch, being tired or dizzy). By including chronic-disese control group, we hve imed to ccount for ny items tht my be endorsed purely on the bsis of hving chronic illness. The fct tht the two chronicdisese groups differ only on the Socil Problems scle is strong evidence tht individuls with cystinosis hve socil difficulties tht cnnot be ccounted for solely on the bsis of hving chronic illness. Despite the questions rised bove, the present study does demonstrte high incidence of socil problems in children with cystinosis compred with individuls with CF nd with controls. The underlying resons for this finding remin to be determined, but the pttern of cognitive nd behviorl deficits observed in cystinosis ppers to constitute behviorl phenotype for this genetic disorder. Future studies of behvior nd cognition in children with cystinosis vrints, who hve different genetic ltertions, will help to better determine how specific this behviorl phenotype is to the 17p13 deletion. DOI: /S Accepted for publiction 10th August Acknowledgments This work ws supported by grnt RO1 HD23854 from the Ntionl Institutes of Helth (DA Truner, PI), nd by gift from the Ntionl Cystinosis Foundtion to Dr Truner. The uthors thnk the children with cystinosis, nd their fmilies, for their prticiption in this study, nd for their ongoing support of our reserch. We thnk Dr Michel Light nd Dr Mrk Pin for their help in recruiting ptients with CF, the ptients with CF nd their fmilies for their willingness to prticipte, nd Dr Angel Bllntyne for reviewing the mnuscript. 406 Developmentl Medicine & Child Neurology 2005, 47:
5 References Achenbch TM. (1991) Mnul for the Child Behvior Checklist Burlington, VT: Deprtment of Psychitry, University of Vermont. Bllntyne AO, Scrvie KM, Truner DA. (1997) Acdemic chievement in individuls with infntile nephropthic cystinosis. Am J Med Genet 74: Bllntyne AO, Truner DA. (2000) Neurobehviorl consequences of genetic metbolic disorder: visul processing deficits in infntile nephropthic cystinosis. Neuropsychitry Neuropsychol Behv Neurol 13: Broyer M, Tete MJ, Guest G, Bertheleme JP, Lbrousse F, Poisson M. (1996) Clinicl polymorphism of cystinosis encephlopthy: results of tretment with cystemine. J Inherit Metb Dis 19: Colh S, Truner DA. (1997) Tctile recognition in infntile nephropthic cystinosis. Dev Med Child Neurol 39: Dvis MC, Tucker CM, Fennell RS. (1996) Fmily behvior, dpttion, nd tretment dherence of peditric nephrology ptients. Peditr Nephrol 10: Eisenhuer GL, Arnold WC, Livingston RL. (1988) Identifying psychitric disorders in children with renl disese. South Med J 81: Fielding D, Moore B, Dewey M, Ashley P, McKendrick T, Pinkerton P. (1985) Children with end-stge renl filure: psychologicl effects on ptients, siblings nd prents. J Psychosom Res 29: Ghl WA, Reed GF, Thoene JG, Schulmn JD, Rizzo WB, Jons AJ, Denmn DW, Schlesselmn JJ, Corden BJ, Schneider JA. (1987) Cystemine therpy for children with nephropthic cystinosis. N Engl J Med 316: Ghl WA, Thoene J, Schneider JA. (2001) Cystinosis: disorder of lysosoml membrne trnsport. In: Scriver CR, Beudet AL, Sly WS, Vlle D, Childs B, Kinzler KW, Vogelstein B, editors. The Metbolic nd Moleculr Bsis of Inherited Disese. 8th edn. New York: McGrw-Hill. p Grtstein MA, Short AD, Vnntt K, Noll RB. (1999) Psychosocil djustment of children with chronic illness: n evlution of three models. Dev Behv Peditr 20: Hodge BL, Hesselink JR, Truner DA. (1992) MRI study of white mtter chnges in cystinosis. Society Neurosci Abstr 18: 333. (Abstrct) Mrkello TC, Bernrdini IM, Ghl WA (1993) Improved renl function in children with cystinosis treted with cystemine. N Engl J Med 328: Mulhern RK, Wssermn AL, Friedmn AG, Firclough D. (1989) Socil competence nd behviorl djustment of children who re long-term survivors of cncer. Peditrics 83: Nichols SL, Press GA, Schneider JA, Truner DA. (1990) Corticl trophy nd cognitive performnce in infntile nephropthic cystinosis. Peditr Neurol 6: O Brien G, Yule W. (1995) Behviourl Phenotypes. Clinics in Developmentl Medicine No London: Mc Keith Press. Prk CH, Kim DY, Kim KS, Cho WH, Prk SB, Kim HC. (1996) Clinicl nd psychosocil consequences of renl trnsplnttion in children. Trnsplnt Proc 28: Perrin EC, Stein REK, Drotr D. (1991) Cutions in using the Child Behvior Checklist: observtions bsed on reserch bout children with chronic illness. J Peditr Psychol 16: Pumrieg AJ, Breiger D, Person D, Dreyer C, Seilheimer DK. (1990) Behviorl symptoms in cystic fibrosis vs. neurologicl ptients. Psychosomtics 31: Reynolds JM, Grrld EM, Postlethwite RJ, Jmeson RA. (1990) Psychosocil issues in children on hospitl hemodilysis: nurses views. Peditr Nephrol 4: Reynolds JM, Grrld EM, Postlethwite RJ, Goh D. (1991) Chnges in psychosocil djustment fter renl trnsplnttion. Arch Dis Child 66: Rourke BP. (1982) Centrl processing deficiencies in children: towrd developmentl neuropsychologicl model. J Clin Neuropsychol 4: Rourke BP. (1988) Syndrome of nonverbl lerning disbilities: developmentl mnifesttions in neurologicl disese, disorder, nd dysfunction. Clin Neuropsychol 2: Rourke BP. (1989) Nonverbl Lerning Disbilities: The Syndrome nd the Model. New York: The Guilford Press. Scrvie KM, Bllntyne AO, Truner DA. (1996) Visuomotor performnce in children with infntile nephropthic cystinosis. Percept Mot Skills 82: Thompson KL, Vrni JW, Hnson V. (1987) Comprehensive ssessment of pin in juvenile rheumtoid rthritis: n empiricl pproch. J Peditr Psychol 12: Thorndike R, Hgn E, Sttler J. (1986) Stnford-Binet Intelligence Scle. 4th edn. Chicgo: Riverside Publishing. Town M, Jen G, Cherqui S, Attrd M, Forestier L, Whitmore SA, Cllen DF, Gribouvl O, Broyer M, Btes GP, vn t Hoff W, Antignc C. (1998) A novel gene encoding n integrl membrne protein is mutted in nephropthic cystinosis. Nture Genet 18: Truner DA, Chse C, Scheller J, Ktz B, Schneider JA. (1988) Neurologic nd cognitive deficits in children with cystinosis. J Peditr 112: Truner DA, Chse C, Bllntyne A, Tlll P, Schneider J. (1989) Ptterns of visul memory dysfunction in children with cystinosis. Ann Neurol 26: 436. (Abstrct) Willims BLH, Schneider JA, Truner DA. (1994) Globl intellectul deficits in cystinosis. Am J Med Genet 49: List of bbrevitions CBCL CF NVLD Achenbch Child Behvior Checklist Cystic fibrosis Nonverbl lerning disbilities Behviorl Profile in Cystinosis Gustvo Delgdo et l 407
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