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VILJOEN ET AL.

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Fetal Alcohol Syndrome Epidemiology in a South African Community: A Second Study of a Very High Prevalence Area*
DENIS L. VILJOEN, M.D., J. PHILLIP GOSSAGE, PH.D.,† LESLEY BROOKE, B.S. (HONS.),† COLLEEN M. ADNAMS, M.D., F.C.P.,† KENNETH L. JONES, M.D.,† LUTHER K. ROBINSON, M.D.,† H. EUGENE HOYME, M.D.,† CUDORE SNELL, D.S.W.,† NATHANIEL C.O. KHAOLE, M.D.,† PIYADASA KODITUWAKKU, PH.D.,† KWADWO OHENE ASANTE, M.D.,† RICHARD FINDLAY, M.D.,† BARBARA QUINTON, M.D.,† ANNA-SUSAN MARAIS, R.N.,† WENDY O. KALBERG, M.A., CED,† AND PHILIP A. MAY, PH.D.†
Department of Human Genetics, Faculty of Health Sciences, University of Witwatersrand, National Health Laboratory Services, South Africa, and the Foundation for Alcohol Related Research

ABSTRACT. Objective: The aim of the study was to determine the prevalence and characteristics of fetal alcohol syndrome (FAS) in a second primary school cohort in a community in South Africa. Method: Active case ascertainment, two-tier screening, and Institute of Medicine assessment methodology were employed among 857 first grade pupils, most born in 1993. Characteristics of children with FAS were contrasted with characteristics of a randomly selected control group from the same classrooms. Physical growth and development, dysmorphology and psychological characteristics of the children and measures of maternal alcohol use and smoking were analyzed. Results: The rate of FAS found in this study is the highest yet reported in any overall community in the world, 65.2-74.2 per 1,000 children in the first grade population. These rates are 33-148 times greater than U.S. estimates and higher than in a previous cohort study in this same community (40.5-46.4 per 1,000). Detailed documentation of physical features indicates that FAS children

in South Africa have characteristics similar to those elsewhere: poor growth and development, facial and limb dysmorphology, and lower intellectual functioning. Frequent, severe episodic drinking of beer and wine is common among mothers and fathers of FAS children. Their lives are characterized by serious familial, social and economic challenges, compared with controls. Heavy episodic maternal drinking is significantly associated with negative outcomes of children in the area of nonverbal intelligence but even more so in verbal intelligence, behavior and overall dysmorphology (physical anomalies). Significantly more FAS exists among children of women who were rural residents (odds ratio: 7.36, 95% confidence interval: 3.31-16.52), usually among workers on local farms. Conclusion: A high rate of FAS was documented in this community. Given social and economic similarities and racial admixture, we suspect that other communities in the Western Cape have rates that also are quite high. (J. Stud. Alcohol 66: 593-604, 2005)

N A PREVIOUS STUDY in the community in South Africa that was studied here, the fetal alcohol syndrome (FAS) rate among first graders was 40.5-46.4 per 1,000 (May et al., 2000). This rate contrasts with estimated FAS rates of 0.33-2.2 in the United States (Abel and Sokol, 1991; May and Gossage, 2001) and with an average for the developed world of 0.97 per 1,000 (Abel, 1998; Abel and Sokol, 1987). In a few high-risk American Indian reservation communities in the United States, the rate of FAS derived from active case ascertainment methods seldom exceeds 10 per 1,000 (Abel, 1995; May, 1991; May et al., 1983), with an average rate of 8 per 1,000 from 1970 to

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1982 (May et al., 2002). The clinic-based rate of FAS for African Americans of low socioeconomic status (SES) from a few inner-city areas is 2.29 per 1000 (Abel, 1995, 1998). Estimations of FAS prevalence in the United States come from birth records, child disability registries, clinic-based studies and a few population-based initiatives (Stratton et al., 1996; May, 1996). Because of the wide variation in methodologies, comparison of FAS prevalence and characteristics among populations is difficult and almost impossible. For example, all but three active case ascertainment studies, where outreach in major geographical areas focuses on aggressive case finding, were carried out among American
University of Cape Town and the Foundation for Alcohol Related Research. Colleen M. Adnams is with the Department of Paediatrics, University of Cape Town. Kenneth L. Jones is with the Division of Dysmorphology/Teratology, Medical Center, University of California, San Diego. Luther K. Robinson is with Dysmorphology and Clinical Genetics, State University of New York at Buffalo. H. Eugene Hoyne is with the Division of Medical Genetics, Stanford University School of Medicine. Cudore Snell is with the Department of Social Work, Howard University. Kwadwo Ohene Asante is in Pediatrics, British Columbia. Richard Findlay is with the Department of Pediatrics, King/Drew Medical Center. Barbara Quinton is with the Department of Pediatrics, Howard University.

Received: August 2, 2004. Revision: March 23, 2005. *This project was funded by the National Institute on Alcohol Abuse and Alcoholism grants RO1 AA09440 and R01 AA11685, the National Institute on Minority Health and Health Disparities and the Foundation for Alcohol Related Research of South Africa. †Philip A. May is with the University of New Mexico, Center on Alcoholism, Substance Abuse and Addictions (CASAA), 2650 Yale SE, Albuquerque, NM 87106. Correspondence should be sent to him at that address, or via email at: pmay@unm.edu. J. Phillip Gossage, Piyadasa Kodituwakku and Wendy O. Kalberg are with CASAA, the University of New Mexico. Lesley Brooke, Nathaniel C.O. Khaole and Anna-Susan Marais are with the

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JOURNAL OF STUDIES ON ALCOHOL / SEPTEMBER 2005 Method Although indications that alcohol was teratogenic had been raised earlier in Europe (Sullivan, 1899; Lemoine et al., 1968), the diagnosis of FAS was formulated by Jones and Smith in 1973 (Jones and Smith, 1973), with further delineation in recent years (Aase, 1994; Aase et al., 1995; Hoyme et al., 2005; Stratton et al., 1996; Rossett, 1980; Sokol and Clarren, 1989, 1995). FAS is a pattern of anomalies and developmental deficits in children who were exposed prenatally to large amounts of alcohol. Children with FAS have a characteristic pattern of facial and body dysmorphology and delayed physical growth and development, as well as specific mental and behavioral deficits (Stratton et al., 1996). For a diagnosis of FAS, all three categories of problems must be present (Stratton et al., 1996), and the diagnosis should be made only after excluding other genetic and teratogenic anomalies (Hoyme et al., 2005). Even though an FAS diagnosis can be made without confirmation of maternal drinking (Stratton et al., 1996), a detailed maternal history is best to confirm gestational drinking. In this study, no attempt was made to diagnose lowerseverity fetal alcohol outcomes, previously called “fetal alcohol effects.” Currently these other diagnoses are referred to as “alcohol-related birth defects” or “alcohol-related neurodevelopmental deficits” (Stratton et al., 1996). The continuum of effects, from mild to severe, is called “fetal alcohol spectrum disorder.” Only the most definite diagnosis was used in this study—full-blown FAS/not FAS. Diagnostic components of the IOM were strictly used: (1) facial and other dysmorphology, recorded using a quantified checklist (see Hoyme et al., 2005), where high scores indicate more features consistent with FAS; (2) diminished growth for age (occipitofrontal head circumference [OFC], weight and height; (3) developmental delay (in intelligence, behavioral functioning and social skills); and, if possible, (4) confirmation of maternal alcohol consumption from maternal or collateral sources. Once data were collected and analyzed by independent examiners for each component, a structured case conference was held (Figure 1) for final diagnoses (see Hoyme et al., 2005). Every child with an FAS diagnosis met each of the IOM criteria 1-3 above, and criteria for number 4 were met in 90.6% of cases. Two-tier screening system In the previous study in this community (May et al., 2000), dysmorphology, growth and developmental data for more than 406 unselected first grade children were collected initially to provide norms for this particular population relative to National Center for Health Statistics growth charts and clinical presentation. The unique racial mixture of the WCP necessitated this first step. For example, pre-

Indians (Clarren et al., 2001; May et al., 2002). Passive, record-based systems and clinic-based methods that investigate FAS among clients presenting for medical services (e.g., in prenatal clinics) are most commonly used in other U.S. and European populations (Abel, 1995; Abel and Sokol, 1987, 1991; Chavez et al., 1988; Egeland et al., 1995, 1998; May, 1996). Active case ascertainment for FAS studies was endorsed by a study committee of the Institute of Medicine (IOM) as the most accurate method for epidemiological studies of FAS, but such studies are logistically challenging, expensive and time consuming (Stratton et al., 1996). This article summarizes a second active case ascertainment initiative in a first grade cohort to assess the prevalence of FAS in the Western Cape Province (WCP) of the Republic of South Africa. Although FAS had been diagnosed in South Africa before (Palmer, 1985), a first study in this community was prompted by a binational (United States and South African) commission initiated by the vice presidents of the two countries (National Institute on Alcohol Abuse and Alcoholism, 1996, 1998). An initial, comprehensive inquiry in 1997 produced the highest rate of FAS ever reported, more than 40 per 1,000, and raised many issues regarding the exact conditions producing FAS in South Africa and generally in human populations (Adnams, 2001; May et al., 2000; Viljoen et al., 2002). Fruit, grape and wine production dominate the region. Wine production over the past 300 years has influenced the modal drinking patterns. Wine was historically distributed daily to workers as partial payment for labor, under what was called the “Dop” system. Dop was outlawed by multiple statutes, and there is general public sentiment against its practice, but residual patterns of regular, heavy episodic alcohol consumption by some are a legacy. Furthermore, increased contemporary availability of inexpensive commercial beer, wine and distilled spirits, primarily in “takeaway”(carry-out) sources and shebeens (illegal bars), has maintained or exacerbated severe drinking (London et al., 1995; Mager, 2004; Parry, 1998). Episodic drinking is a major form of recreation among subsegments of the WCP population, causing many problems (King et al., 2004). The population of the WCP is 3,721,200: 57% “Cape Coloured” (mixed race), 18% black, 25% white and 1% of other races. Cape Town is the major city, but 40% of the population lives outside of the metropolitan area in small towns and rural areas. The study community is similar in social and economic character to others in the Winelands of WCP, with a 1996 population of 45,255 (35,364 urban and 9,861 rural; Bureau of Census, 1997). The vast majority are classified as Coloured. Coloured denotes people in South Africa originating from intermarriage of African tribal populations (particularly the Khoi and San), European whites and Asians (primarily Malaysians).

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FIGURE 1.

The Methodological Flow of the Wave II Western Cape, South Africa FAS Study

liminary information suggested that the interpupillary distance (IPD) and the inner canthal distance (ICD) in local subpopulations were greater than U.S. norms; and in many children the proximal portion of the philtral columns were smoother than found in America. Small head size is more common in this population, but a child with isolated microcephaly (or another single trait) and no additional features of FAS was diagnosed with microcephaly (or the isolated trait). The growth and clinical data from the first study were utilized primarily to calibrate the expectations of the clinicians and to set the cutoff criteria for Tier II screening in all phases of the study (see below). Four two-person teams (one expert pediatric dysmorphologist and a physician being trained in FAS diagnosis) worked independently but simultaneously, using standardized assessment criteria. Twelve of the 13 elementary schools of the community were accessed in both studies. The school that declined participation was a private, all-white school with 60 first graders. More than 90% of the children in the study were Coloured; the remainder were black or white. Relatively low mobility of the local population ensured that most of the study children underwent gestation locally. In the previous South Africa study, cutoff points were set to ensure capture of all FAS children, and they were used again in this study. In this study, 863 (93.6%) of 922 children on the rolls in first grade classrooms had parental consent to participate and received Tier I screening, where height, weight and OFC were measured. If a child was at or below the 10th centile on OFC and/or on both height and weight, he or she was referred for a complete physical examination (Tier II). Two hundred and ninety-nine (34.9%) children met these criteria (see Figure 1). In our first study,

one child with FAS from the community was not in a standard school (

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