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Inbreeding and Risk of Late Onset Complex Disease

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Inbreeding and Risk of Late Onset Complex Disease 925 LETTER TO JMG Inbreeding and risk of late onset complex disease I Rudan, D Rudan, H Campbell, A Carothers, A Wright, N Smolej-Narancic, B Janicijevic, L Jin, R Chakraborty, R Deka, P Rudan ............................................................................................................................... J Med Genet 2003;40:925–932 nbreeding has been shown in almost all species to be associated with impairment of function because of homo- Key points Izygosity of recessive alleles. This occurs across a wide range of traits and suggests a large number of deleterious alleles in N From arguments derived from population genetics, we the human genome. This has been predicted from the propose that the genetic basis of common late onset reduced early survival of offspring in first cousin marriages diseases includes a major class of deleterious recessive and from similar results in other organisms.1–3 As most alleles. Inbreeding is therefore predicted to increase the identified genetic variants causing complex disease in incidence of such diseases. 1 humans are partially recessive we predict that inbreeding N Among 10 late onset conditions studied in a genetic in humans might influence a wide range of complex diseases. isolate population, inbreeding was found to be a Numerous reports on the health effects of inbreeding have significant (positive) predictor for coronary heart focused mainly on its impact on reproduction, childhood disease, stroke, cancer, uni/bipolar depression, mortality, and rare Mendelian disorders.23For example, a 4– asthma, gout, and peptic ulcer, but not for type 2 5% increase in childhood mortality has been found in the diabetes offspring of first cousin marriages, and similar results have been reported in other species.245 However, the effects of N It appears that inbreeding causes an increase in inbreeding on late onset disorders are largely unknown, homozygosity at many genetic loci with small deleter- despite the fact that deleterious effects of inbreeding in other ious effects on homeostatic pathways, resulting in species are known to increase with age, as predicted by increased disease risk. selection theory.67The reported finding of greater inbreeding N The results indicate that between 23% and 48% of the effects for traits such as blood pressure and serum cholesterol incidence of these disorders in this population sample in middle age compared with early adult life is consistent (other than type 2 diabetes) could be attributed to with this.8 recent inbreeding. The global impact of inbreeding In order to investigate the hypothesis that the heritable could thus be substantial, as an estimated one billion component of late onset diseases includes a major class of people globally show rates of consanguineous mar- 9 deleterious recessive alleles, we recently studied the effects riages greater than 20%. of inbreeding on blood pressure among 2760 adult indivi- duals from 25 villages in a Dalmatian island isolate. The study showed a large effect of inbreeding on blood pressure equivalent to a rise in systolic blood pressure of ,20 mm Hg individuals selected randomly from voting lists to form and diastolic blood pressure of ,12 mm Hg in offspring of approximately 20–30% of the total population of these 14 first cousin marriages. The effect appeared to be mediated by villages was undertaken in late 1970s and early 1980s by the several hundred recessive alleles as a result of increased Institute for Anthropological Research in Zagreb in collabora- homozygosity.10 In support of this finding, several studies of tion with the Smithsonian Institute, Washington, USA. The small inbred communities worldwide have reported an mean adult ages in individual villages varied from 41 to 65 increased prevalence of hypertension.8 11–15 years (detailed age/sex profiles for each village are given in In the present study, we extend this observation by appendix 1). For each individual, information was collected investigating the relation between inbreeding and the on the highest level of education, occupation, diet, smoking prevalence of 10 late onset complex diseases of public health habits, and body mass index (table 1). importance. The study was carried out in 14 of the original 25 isolate villages on three neighbouring islands in middle Computation of individual inbreeding coefficients Dalmatia, Croatia. These island populations present a wide A single researcher (IR) computed individual inbreeding range of levels of inbreeding and endogamy, reduced genetic coefficients for each study participant, based on pedigree variation at both individual and (sub)population levels, and information on four to five ancestral generations, recorded 10 16–18 relative uniformity of environment, and thus provide a during the initial field work and supplemented by a study of good setting for investigating inbreeding effects. parish registries. The individual inbreeding coefficients (F) were then computed according to Wright’s path method19: METHODS Study cohort The village populations of three neighbouring islands in the eastern Adriatic, part of Middle Dalmatia, Croatia (Brac, where mi and ni refer to the number of paths from a common Hvar, and Korcula, see fig 1), represent well characterised ancestor, and c refers to the number of common ancestors. genetic isolates. The tendency towards inbreeding in each The genealogical inbreeding coefficient for each village was village has been influenced by geographic isolation, political then computed as the average of all individual F values. To (‘‘Pastrovic’’) privileges given to residents of certain commu- further support these estimates, F was calculated from nities, and sociocultural factors.16–18 A survey of 1339 adult isonymy as suggested by Tay and Yip,20 and mean values www.jmedgenet.com 926 Letter Figure 1 Map of the Dalmatian island genetic isolate showing study islands and villages (numbered 1 to 14). were derived for each of the 14 villages. Estimates based on type diabetes, gout, and peptic ulcer) following those isonymy are generally thought to be positively biased, and so presented in Merck’s Manual. In collaboration with local to provide an upper bound for F (table 1). general practitioners, two medical doctors, who were blind to the inbreeding status of each individual, inspected the Follow up data on disease status of cohort individuals medical records between March and October 2000 and Population census data in 1981, 1991, and 2001 from study recorded whenever appropriate diagnostic criteria were met. villages show significant depopulation with minimal immi- Diagnoses were supported wherever possible by medical gration over the last two decades. Thus only 480 individuals records from the local general hospital in Split. who were still resident in the study villages were available for follow up in the year 2000. Specific diagnostic criteria were Statistical analysis and modelling established for each of 10 commonly occurring disorders in Disease prevalence was first investigated by comparisons this population (coronary heart disease, stroke, cancer, between villages grouped by the level of inbreeding as high, schizophrenia, epilepsy, uni/bipolar depression, asthma, adult moderate, or low (table 2). Disease prevalence rates were Table 1 Genetic and environmental characteristics of 14 village populations ranked according to average inbreeding coefficient computed from genealogical data Village (island) N(sam) N(pop) F(gen) F(iso) Edu (%) Occu (%) Diet (%) Smo (%) BMI (avg) Gdinj (H) 135 153 0?049 0?107 2?380?893?84?625?1 Pupnat (K) 96 326 0?044 0?034 2?189?791?89?326?7 Cara (K) 139 464 0?032 0?040 1?589?094?922?626?4 Dracevica (B) 20 66 0?031 0?031 2?485?790?523?828?6 Racisce (K) 103 290 0?027 0?034 1?987?583?623?127?3 Bogomolje (H) 90 102 0?025 0?030 2?584?093?84?923?0 Vrisnik (H) 105 216 0?015 0?023 2?182?391?613?525?5 G Humac (B) 43 214 0?013 0?016 2?581?387?538?827?3 Zastrazisce (H) 133 210 0?013 0?013 4?086?393?65?925?1 Lumbarda (K) 59 354 0?012 0?025 4?785?289?821?326?2 Smokvica (K) 97 866 0?008 0?019 3?181?481?427?826?0 Svirce (H) 152 375 0?008 0?008 2?080?183?212?825?7 Dol (H) 102 154 0?005 0?004 4?275?886?38?426?1 Nerezisca (B) 65 106 0?002 0?004 1?860?779?534?828?0 Islands: H, Hvar; B, Brac; K, Korcula. BMI (avg), average body mass index among examinees; Diet, proportion of examinees regularly consuming traditional Mediterranean diet; Edu, proportion of examinees with some college education; F(gen), average inbreeding coefficients computed from genealogical data; F(iso), average inbreeding coefficients computed from isonymy; N(pop), number of individuals in the village population in year 2000 (year in which disease prevalence was determined); N(sam), number of individuals in the sample (represents 20–30% random samples of total village population obtained between 1979 and 1981); Occu, proportionof examinees working in agriculture and fishery; Smo: proportion of examinees smoking (smoking recorded using Brinkman index*). .................................................................................................................................... *Brinkman GL, Coates EO. The effect of bronchitis, smoking and occupation on ventilation. Am Rev Respir Dis 1963;87:384–9. www.jmedgenet.com Letter 927 Table 2 Age and sex standardised prevalences of 10 complex diseases in groups of villages with relatively ‘‘high,’’ ‘‘moderate,’’ and ‘‘low’’ average inbreeding coefficient values ‘‘High inbreeding’’ ‘‘Moderate inbreeding’’ ‘‘Low inbreeding’’ (N = 1401) (N = 998) (N = 1501) Average Fgen = 0.036 Average Fgen = 0.013 Average Fgen = 0.006 Average Fiso = 0.052 Average Fiso = 0.019 Average Fiso = 0.009 Coronary heart disease 13.28% 11.95% 11.23% Stroke 2.43% 2.79% 1.73% Cancer 4.54%*** 3.44%* 1.93% Schizophrenia 1.23%*** 0.96%* 0.14% Uni/bipolar depression 10.26%*** 7.63%** 4.51% Asthma 3.63% 2.64% 2.60% Type II diabetes 6.02% 7.35% 6.77% Gout 9.25%*** 7.19%*** 3.96% Peptic ulcer 6.92%*** 4.29%** 2.18% Epilepsy 1.47%*** 0.78% 0.31% Statistical significance (p values) in highly and moderately inbred groups is calculated against the low inbreeding group: *p,0.05; **p,0.01; ***p,0.001.
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