ORIGINAL ARTICLE. Patrick F. Sullivan, MD, FRANZCP; Kenneth S. Kendler, MD; Michael C. Neale, PhD

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1 ORIGINAL ARTICLE Schizophrenia as a Complex Trai Evidence From a Mea-analysis of Twin Sudies Parick F. Sullivan, MD, FRANZCP; Kenneh S. Kendler, MD; Michael C. Neale, PhD Conex: There are many published win sudies of schizophrenia. Alhough hese sudies have been reviewed previously, o our knowledge, no review has provided quaniaive summary esimaes of he impac of genes and environmen on liabiliy o schizophrenia ha also accouned for he differen ascerainmen sraegies used. Objecive: To calculae mea-analyic esimaes of heriabiliy in liabiliy and shared and individual-specific environmenal effecs from he pooled win daa. Daa Sources: We used a srucured lieraure search o idenify all published win sudies of schizophrenia, including MEDLINE, disseraion, and books-in-prin searches. Sudy Selecion: Of he 14 idenified sudies, 12 me he minimal inclusion crieria of sysemaic ascerainmen. Daa Synhesis: By using a muligroup win model, we found evidence for subsanial addiive geneic effecs he poin esimae of heriabiliy in liabiliy o schizophrenia was 81% (95% confidence inerval, 73%-90%). Noably, here was consisen evidence across hese sudies for common or shared environmenal influences on liabiliy o schizophrenia join esimae, 11% (95% confidence inerval, 3%-19%). Conclusions: Despie evidence of heerogeneiy across sudies, hese mea-analyic resuls from 12 published win sudies of schizophrenia are consisen wih a view of schizophrenia as a complex rai ha resuls from geneic and environmenal eiological influences. These resuls are broadly informaive in ha hey provide no informaion abou he specific ideniy of hese eiological influences, bu hey do provide a componen of a unifying empirical basis supporing he raionaliy of searches for underlying geneic and common environmenal eiological facors. Arch Gen Psychiary. 2003;60: From he Deparmens of Geneics and Psychiary, Universiy of Norh Carolina a Chapel Hill (Dr Sullivan); and he Virginia Insiue for Psychiaric and Behavioral Geneics, Virginia Commonwealh Universiy, Richmond (Drs Kendler and Neale). GENETIC epidemiological sudies of schizophrenia have had a guiding influence on schizophrenia research. In paricular, win and adopion sudies ha suggesed subsanial geneic influences on he liabiliy o schizophrenia 1 helped creae he empirical raionale for numerous ongoing searches o idenify he predisposing geneic loci. 2,3 Recenly, several groups 4-6 have presened evidence for genes ha may be involved in he eiology of schizophrenia. Alhough he primary win sudies of schizophrenia have been reviewed exensively 7,8 and have been quaniaively summarized, 9-12 we are aware of no meaanalysis of he primary sudies ha incorporaed ascerainmen correcions. Failure o correc for ascerainmen (he mixures of singly and doubly ascerained win pairs found in mos of hese sudies) could bias he resuls. The goal of his repor was o conduc a quaniaive mea-analysis of he published win sudies of schizophrenia. A key advanage of synheic mea-analyic vs radiional lieraure reviews is he poenial o yield less biased quaniaive summaries of he findings of many primary sudies We were also ineresed in an addiional benefi of mea-analysis: is capaciy o deec suble effecs for which individual sudies may possess insufficien saisical power. Twin sudies of uncommon discree rais, like hose for schizophrenia, possess limied saisical power in many circumsances (unless he sample or effec sizes are large). 17 Only when he resuls of several sudies are analyzed joinly in a meaanalysis can suble effecs be assessed wih a reasonable degree of confidence American Medical Associaion. All righs reserved.

2 Published Twin Sudies of Schizophrenia Included and Excluded From he Mea-analysis* Source Counry Sysemaic Recruimen Blinding o Zygosiy and Co-win Saus Basis for Diagnosis Diagnosic Crieria Ascerainmen Type Included Sudies Essen-Møller, Sweden Yes No Records and inerview Unsaed SA Kallmann, Unied Saes Yes No Records and inerview Unsaed IA ( = 0.42) Slaer and Shields, England Yes No Records and inerview Unsaed IA ( = 0.11) Kringlen, Norway Yes No Records and inerview Process SCZ CA Fischer e al, Denmark Yes No Records and inerview Process SCZ CA Tienari, Finland Yes No Records and inerview Unsaed CA Kendler and Robinee, Unied Saes Yes No Records only ICD-8 RPA Onsad e al, Norway Yes Yes Records and inerview DSM-III-R CA Kläning, Denmark Yes Yes Records and inerview ICD-10 IA ( = 0.29) Franzek and Beckman, Germany Yes Yes Records and inerview DSM-III-R SA Cannon e al, Finland Yes No Records only ICD-8 RPA Cardno e al, England Yes Yes Records and inerview ICD-10 IA ( = 0.47) Excluded Sudies Rosanoff e al, Unied Saes No No Records and inerview Unsaed Unknown Inouye, Japan No No Records and inerview Unsaed SA Abbreviaions: CA, complee ascerainmen ( = 1); IA, incomplee ascerainmen (01); ICD-8, Inernaional Classificaion of Diseases, Eighh Revision; ICD-10, Inernaional Classificaion of Diseases, 10h Revision; RPA, random populaion ascerainmen, correcion unnecessary, bu = 1 because all probands are ascerained; SA, single ascerainmen ( 0); SCZ, schizophrenic. *Twin samples from he same counry do no overlap. We considered sudies ha relied solely on medical regisry daa as unblinded because he reaing physicians were likely aware of family hisory. Sample based on men; boh wins had served in he US armed forces. METHODS PRIMARY STUDIES To idenify all relevan primary sudies, we performed compuerized PubMed searches for an inclusive lis of descripors and searched he reference liss of prior reviews of schizophrenia o idenify any repors no rerieved in he PubMed search. We idenified 14 published sudies of schizophrenia from independen samples in 6 European counries, Japan, and he Unied Saes (Table). If here were muliple publicaions from he same sample, only he mos recen was included. The nex sep in a mea-analysis is usually he applicaion of a se of inclusion crieria. For win sudies, hese include sysemaic recruimen, blinding o co-win diagnosic saus and zygosiy, and use of sysemaic daa collecion and diagnosic procedures. Many of hese sudies were conduced before hese crieria were common in psychiaric research ( of he 14 sudies were published before 1970). Only 4 sudies 27-29,31 me all he inclusion crieria, and all were published afer We considered sudies ha relied solely on hospializaion records as no being blind because he clinicians making he diagnosis may have been influenced by he co-win hisory. We chose o relax our a priori inclusion crieria for 4 reasons. Firs, he exclusion of mos sudies is no consisen wih our desire o obain mea-analyic esimaes of wha migh be suble saisical effecs. Second, we reained he capaciy o analyze he mehodologically superior vs inferior sudies. Third, we waned o avoid a bias of moderniy by including older sudies. Many of he older sudies were performed by prominen and highly respeced researchers who conduced he sudies in rigorous accordance wih he acceped research pracices of heir era, and conain informaion perinen o our research quesion. Finally, we were influenced by radiion: mos prior reviews 7,11 of win sudies of schizophrenia have included mos of hese sudies. Therefore, our final exclusion crierion was ha hese sudies ascerain subjecs in a sysemaic manner, which led o he exclusion of 2 sudies and he inclusion of 12 sudies, as shown in he Table. Nearly all of hese primary sudies were believed o suppor he srong role of geneic facors in he eiology of schizophrenia. STATISTICAL ANALYSIS A model for he paerns of familial resemblance was used o predic he observed concordan and discordan pair frequencies. The model included parameers for addiive geneic (a 2 ), common environmenal (c 2 ), and individual-specific environmenal (e 2 ) componens of variance. 32 Addiive geneic influences are shared compleely by monozygoic (MZ) wins and correlae 0.5 beween dizygoic (DZ) wins. Common environmenal influences are shared compleely by he members of a win pair regardless of zygosiy, and accoun for DZ correlaions ha are greaer han half of he MZ correlaion. Individual-specific environmenal componens conribue separaely o each win and, herefore, accoun for less han a perfec resemblance beween MZ wins. These parameers were esimaed by maximum likelihood. The likelihood of he observed pairs of wins was compued using a bivariae normal hreshold model of liabiliy. 33 This model specifies ha individuals in he populaion have a frequency disribuion of liabiliy o schizophrenia ha is described by a normal disribuion. On his liabiliy coninuum, here exiss a hreshold such ha individuals above he hreshold have schizophrenia and hose below do no. The disribuion of win pair liabiliies is bivariae normal, wih uni variances and correlaions as prediced by he following saisical models: r MZ =a 2 +c 2 and r DZ =0.5a 2 +c 2. Alhough i is usual o fi submodels ha eliminae specific sources of variance, his pracice is inappropriae in a mea-analysis, and a common approach o selecing parsimonious models (via he Akaike informaion conen) can selec incorrec models. 34 Four differen ypes of subjec ascerainmen were used in he 12 win sudies in he Table. Each ype of ascerainmen is associaed wih differen ypes of daa. Firs, random populaion ascerainmen yields a full 22 coningency able (diagnosis of win 1diagnosis of win 2). In his insance, all 4 ypes of win pairs are observed direcly (ie, concordan unaffeced win pairs, he 2 discordan cells, and concordan af American Medical Associaion. All righs reserved.

3 feced win pairs), as in 2 win sudies 26,30 of schizophrenia. Second, complee ascerainmen is when concordan unaffeced win pairs are he only pairs no observed, so ha concordan and discordan affeced wins are ascerained, as in 4 win sudies 23-25,27 of schizophrenia. Third, 2 win sudies 29,35 of schizophrenia used single ascerainmen, in which pairs wih 2 probands are no observed and only 1 of he 2 possible discordan cells is observed ogeher wih concordan affeced pairs. Finally, incomplee ascerainmen is inermediae beween complee and single ascerainmen. The key quaniy is, he probabiliy of being ascerained given ha one is affeced. The value is 1 for complee ascerainmen, approaches 0 for single ascerainmen, and 01 for incomplee ascerainmen. The value can be esimaed as 2D/(2D+S), where D is he number of doubly ascerained pairs and S is he number of singly ascerained pairs. Four win sudies 20,21,28,31 of schizophrenia had incomplee ascerainmen. Each ype of ascerainmen requires a differen ascerainmen correcion. For random populaion ascerainmen, no correcion for ascerainmen is required because pairs are hough o be represenaive of he populaion and he likelihood is as follows: (1) ai b i ai b i (x 1,x 2 )dx 2 dx 1 where is he bivariae normal probabiliy densiy funcion; x 1 and x 2 are he liabiliies o schizophrenia for win 1 and win 2, respecively; and a i and b i are a 0 =, a 1 =, b 0 =, and b 1 = (where he subscrip 0 denoes unaffeced; and 1, affeced). Under nonrandom ascerainmen, he likelihood of pairs may be wrien as equaion 1 muliplied by an ascerainmen correcion. Under complee ascerainmen (=1), he ascerainmen correcion is as follows: (x 1,x 2 )dx 2 dx 1 (2) 1/ Under single ascerainmen ( 0), he correcion is as follows: (3) 1/ (x 1 )dx 1 Under incomplee ascerainmen (01), he correcion for single-proband pairs is as follows: (x 1 )dx 1 2 (x 1,x 2 )dx 2 dx 1 (4) /2 For double-proband pairs, he equaion is as follows: (x 1 )dx 1 2 (x 1,x 2 )dx 2 dx 1 (5) (2 )/2 A scrip ha uses he appropriae correcion for ascerainmen and he populaion hreshold esimae for simulaneous analysis of he 12 sudies is available on he Mx Examples Web sie (hp://www.vcu.edu/mx/examples.hml). 36 To es for heerogeneiy, he parameers of he model (a 2 and c 2 ) were se equal across he sudies, and he fi of his model was compared via he likelihood-raio es o he fi of he model in which he a 2, c 2, and e 2 parameers were allowed o differ beween sudies. Because he variance of he laen disribuion canno be esimaed separaely from he hresholds, we used he common pracice of sandardizing o uni variance by imposing he following nonlinear consrain: a 2 +c 2 +e 2 =1. Effecively, here are only 2 free parameers per sample (a 2 and c 2 ), so he comparison ess for heerogeneiy have a df=2 for each sample beyond he firs. RESULTS Figure 1 depics he MZ and DZ win correlaions from 12 win sudies of schizophrenia and he mea-analyic DZ Terachoric Correlaion Coefficien MZ Terachoric Correlaion Coefficien Figure 1. Plo of dizygoic (DZ) vs monozygoic (MZ) erachoric correlaion coefficiens (circles) and he mea-analyic summary esimae () for 12 win sudies of schizophrenia. Terachoric correlaions were esimaed by Mx (a saisical daa modeling sofware). 36 The dashed line indicaes he expeced correlaions if he familial resemblance is enirely due o common environmenal effecs; he solid line, he expeced correlaions if he familial resemblance is enirely due o addiive geneic effecs. summary esimaes. Seven of he 12 sudies and he meaanalyic summary esimae (r MZ =0.92; 95% confidence inerval [CI], ; and r DZ =0.52; 95% CI, ) lie beween lines depicing exreme cases in which a rai is enirely due o addiive geneic effecs (100% a 2 ) or enirely due o common environmenal effecs (100% c 2 ), suggesing he presence of boh addiive geneic and common environmenal effecs in he eiology of schizophrenia. Figure 2 presens he variance componen esimaes from Mx for 12 win sudies of schizophrenia and he mea-analyic summary esimaes. Figure 2A depics addiive geneic effecs, and Figure 2B depics common environmenal effecs. For addiive geneic effecs, he poin esimaes from all bu 2 sudies 23,24 are in excess of 50%. The 95% CIs for he esimaes are ofen large because of he relaively small sample sizes of he individual sudies. The mea-analyic summary for addiive geneic variance in liabiliy o schizophrenia was esimaed a 81% (95% CI, 73%-90%). The 95% CI for he join esimae overlapped wih he 95% CIs for ,23,26-31 of he 12 sudies. For common environmenal effecs, he poin esimaes for ,23-25,29 of he 12 sudies were nonzero, wih 6 greaer han 15%. The 95% CIs ended o be large owing o he limied saisical power o deec his effec in he individual sudies. The mea-analyic summary for common environmenal effecs for he liabiliy o schizophrenia was esimaed a 11% and, noably, he 95% CI did no include 0 (95% CI, 3%-19%). The 95% CI for his esimae overlapped wih he CIs of all bu 2 23,24 of he 12 sudies. An inspecion of Figures 1 and 2 suggess ha here is heerogeneiy across he 12 individual win sudies. A American Medical Associaion. All righs reserved.

4 A Essen-Møller, Kallmann, Slaer and Shields, Kringlen, Fischer e al, Tienari, Kendler and Robinee, Onsad e al, Franzek and Beckman, B Kläning, Cannon e al, Cardno e al, All Sudies Essen-Møller, Kallmann, Slaer and Shields, Kringlen, Fischer e al, Tienari, Kendler and Robinee, Onsad e al, Kläning, Franzek and Beckman, Cannon e al, Cardno e al, All Sudies Esimae, % Figure 2. Graphical depicion of variance componen esimaes for 12 win sudies of schizophrenia and he mea-analyic summary. A, Addiive geneic variance. B, Common environmenal variance. The esimaes and heir 95% confidence regions were esimaed by Mx (a saisical daa modeling sofware), 36 accouning for ascerainmen probabiliies. Horizonal bars indicae 95% confidence inervals; verical bars, parameer esimaes. formal es for homogeneiy was srongly rejeced ( 2 20=113.9, P.001). Criically, when we compared he mehodologically superior sudies 27-29,31 wih he mehodologically inferior sudies, 19-21,23-26,30 we found similar poin esimaes for addiive geneic effecs (77% vs 78%) and common environmenal effecs (17% vs 14%). In addiion, ,30,31 of he 12 win sudies used unique populaion prevalence esimaes for schizophrenia. Because prevalence can influence he variance componen esimaes, we performed he analyses again, wih all sudies forced o have populaion prevalences for schizophrenia of 0.5%, 0.75%, and 1%. The paern of resuls was similar o ha described previously, wih high esimaes of addiive geneic effecs and esimaes of common environmenal effecs whose 95% CIs did no include 0. Esimaes of common environmenal effecs were larger wih decreasing prevalence. COMMENT MAIN RESULTS One principal resul of his quaniaive mea-analysis of 12 published win sudies of schizophrenia was expeced, and he oher was quie surprising. Consisen wih prior summaries of he win lieraure on schizophrenia, he meaanalyic summary esimae of is heriabiliy is high (poin esimae, 81%; 95% CI, 73%-90%), and his resul may provide a useful summary of a diverse lieraure. However, we also deermined ha here are small bu significan common environmenal effecs on liabiliy o schizophrenia (poin esimae, 11%; 95% CI, 3%-19%). This laer esimae is unexpeced and of considerable ineres. LIMITATIONS Before discussing hese findings furher, i is imperaive ha we consider 2 key limiaions. Firs, he mehodological qualiy of he published win sudies of schizophrenia was no uniformly high compared wih, for example, ha for major depression 37 or various smoking behaviors. 38 Mos sudies in his work did no include several criical feaures (blinding and a sandardized diagnosic approach) ha are generally viewed as cenral o he inerpreabiliy of win sudies of medical disorders. In fairness, mos of hese win sudies of schizophrenia were conduced before he imporance of hese mehodological feaures was widely recognized and viewed as essenial. In fac, many of he earlier win sudies represened monumenal and even heroic effors by individual psychiariss who devoed years of personal effor despie limied resources o accumulae he samples quaniaively summarized herein. For he reasons described in he Primary Sudies subsecion of he Mehods secion, we chose o include 12 of 14 sudies ha me pos hoc modificaions of our a priori crieria. Second, he 12 sudies included in his meaanalysis of schizophrenia were saisically heerogeneous. The presence of heerogeneiy of he variance componen esimaes raises 2 quesions Wha is he source of heerogeneiy? and Does i limi he validiy of he mea-analyic esimaes? I is likely ha differences in mehods across sudies are a source of heerogeneiy given ha he 4 sudies 27-29,31 ha me our a priori inclusion crieria had greaer evidence for he homogeneiy of he componens of variance. This is unsurprising, and is consisen wih he increased reliabiliy generally found wih more rigorous mehodological approaches o psychiaric diagnosis. In addiion, heerogeneiy could have resuled from oher sample-specific characerisics, like he male-female or MZ/DZ raios. However, i is also possible ha here exiss rue variaion in he eiology of schizophrenia during he decades spanned by hese sudies or across he differen counries and ehnic ancesries of he individuals in hese sudies. There are repors of associaions of schizophrenia wih poenial eiological facors ha would be expeced o vary across populaions and over ime, such as discree periods of famine, 39 season of birh, 40 or prenaal exposure o influenza or oher viral infecions American Medical Associaion. All righs reserved.

5 The presence of heerogeneiy across sudies does no necessarily invalidae he mea-analyic approach we used o summarize hese sudies. Raher, here is a se of advanages and disadvanages. The criical advanage of including heerogeneous sudies is he capaciy o summarize he variance componen esimaes when here is rue eiological variaion. I is unlikely ha schizophrenia has a single eiology, bu insead is an end resul of heerogeneous processes ha resul in a similar clinical porrai. Therefore, he inclusion of heerogeneous sudies is consisen wih his belief and offers he poenial of a more accurae and less sample-specific summary of he fundamenal naure of his complex illness. On he oher hand, he criical disadvanage is if heerogeneiy is an index of a shared mehodological flaw (eg, bias in recruimen or diagnosis). In his insance, heerogeneiy reflecs he presence of individual sudies ha are flawed and could resul in imprecise and inaccurae esimaes. On balance, we believe ha i is more advanageous han disadvanageous o include heerogeneous sudies. This conenion is suppored by he similariy of parameer esimaes from he mehodologically superior vs inferior sudies. In fac, he poin esimae for common environmenal effecs was higher in he superior sudies (17%) han in he inferior sudies (14%). COMMON ENVIRONMENT AND SCHIZOPHRENIA The mos noable finding from his mea-analysis was ha variance in liabiliy o schizophrenia was esimaed o have a nonzero conribuion of environmenal influences shared by members of a win pair. This finding is ironic because i is unusual o find a behavioral rai or disorder wih significan common environmenal influences 44,45 and schizophrenia is ofen described as one of he more geneic psychiaric disorders. The magniude of he finding suggess ha hese influences, while significan, have a modes impac on liabiliy o schizophrenia. When considering his surprising finding furher, we discovered ha significan common environmenal effecs for schizophrenia were repored previously by Rao e al (20%) 9 and McGue e al (19%). 10 When hese 2 aricles were published in he early 1980s, here was a sharp division wihin psychiary as o wheher schizophrenia resuled from biological/geneic facors or environmenal facors, such as adverse maernal-child relaionships. These perspecives were ofen framed as muually exclusive (naure or nurure). The sronger geneic componen o schizophrenia was clearly he more influenial resul from hese aricles. Our rediscovery of suble, bu nonrivial, common environmenal effecs for schizophrenia is likely o be inerpreed differenly han in he 1980s. The radiional phrases, common environmen and shared environmen, are misnomers in ha hey generally evoke psychiaric risk facors like parenal rearing behavior and raumaic life evens. In he conex of he assumpions and definiions of win analyses, however, common environmen refers o any process ha makes members of a win pair similar regardless of zygosiy. These processes include he classic environmenal facors previously noed, bu also encompass profoundly biological processes such as exposure o infecious agens, macronurien or micronurien dieary characerisics, and exposure o environmenal oxins, eraogens, and oher inrauerine facors. In addiion, i is possible ha some porions of he significan common environmenal effecs are arifacual (eg, due o assoraive maing or a subsanially biased zygosiy assignmen). Moreover, he environmens of members of win pairs end o diverge over ime. The environmens of wins are mos similar in uero and in he immediae posnaal period, wih increasing divergence over infancy, childhood, adolescence, and adulhood. Therefore, he presence of significan common environmenal effecs on liabiliy o schizophrenia suggess ha hese effecs would be mos likely o occur early in life. This predicion is consisen wih a neurodevelopmenal eiology of schizophrenia and wih he lieraure on early risk facors for schizophrenia. For example, several reviews 49,50 including a recen mea-analysis 51 of large, prospecive, and populaion-based sudies found consisen evidence o suppor he saus of pregnancy complicaions, abnormal feal developmen, and delivery complicaions as risk facors for schizophrenia. An addiional repor 52 srongly suggess he imporance of maernalfeal Rh blood group incompaibiliy as a specific risk facor for schizophrenia. In conclusion, hese mea-analyic resuls from 12 published win sudies of schizophrenia suppor a view of schizophrenia as a complex rai ha resuls from boh geneic and shared environmenal eiological influences. These resuls are broadly informaive in ha hey provide no informaion abou he specific number or ideniy of hese eiological influences, bu provide a componen of a unifying empirical basis supporing he raionaliy of searches for underlying geneic and common environmenal eiological facors. Submied for publicaion December 2, 2002; final revision received April 2, 2003; acceped April 11, This sudy was suppored by gran MH from he Naional Insiue of Menal Healh, Behesda, Md (Dr Neale). We hank Irving I. Goesman, PhD, for criical commens on earlier drafs of his aricle. Corresponding auhor: Parick F. Sullivan, MD, FRANZCP, Deparmen of Geneics, Universiy of Norh Carolina a Chapel Hill, Campus Box 7264, Chapel Hill, NC ( REFERENCES 1. Kendler KS, Diehl SR. Schizophrenia: geneics. In: Kaplan HI, Sadock BJ, eds. Comprehensive Texbook of Psychiary. 6h ed. Balimore, Md: Williams & Wilkins; 1995: Almüller J, Palmer LJ, Fischer G, Scherb H, Wjs M. 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