The Cleft Palate–Craniofacial Journal 52(3) pp. 377–380 May 2015 Ó Copyright 2015 American Cleft Palate–Craniofacial Association
BRIEF COMMUNICATION Prevalence of Cleft Lip and Cleft Palate in Rural North-Central Guatemala Jorge Matute, M.Sc., Elaine A. Lydick, M.S., Olga R. Torres, M.Sc., Karen K. Owen, Ph.D., Kathryn H. Jacobsen, M.P.H., Ph.D. Objective: To estimate the number of new cases of cleft lip and cleft palate in the department (state) of Alta Verapaz, Guatemala, in 2012. Design: Cross-sectional survey of midwives from communities identified through a two-stage cluster-sampling process. Midwives were asked how many babies they had delivered in the past year and how many of those newborns had various types of birth defects, as illustrated in pictures. Setting: Indigenous Mayan communities in rural north-central Guatemala. Participants: Midwives (n ¼ 129) who had delivered babies in the previous year. Main Outcome Measure: Reports of babies born with cleft lip and cleft palate. Results: A 1-year prevalence rate of 18.9 per 10,000 for cleft lip and 4.7 per 10,000 for cleft palate was estimated for Alta Verapaz. None of the cases of cleft lip also had cleft palate. Conclusion: The indigenous communities in north-central Guatemala might have a relatively high cleft lip prevalence rate compared with the global average. KEY WORDS:
cleft lip, cleft palate, indigenous population
Cleft lip and cleft palate are congenital deformities that may lead to malnutrition when infants with these birth defects have difficulty feeding and are unable to receive adequate nutrition. If not surgically corrected in infancy or early childhood, these conditions may lead to speech communication disorders and possibly increase the risk of psychosocial problems and depression (Hunt et al., 2005; John et al., 2006). The International Perinatal Database of Typical Oral Clefts (IPDTOC) estimates that the global prevalence of cleft lip (with or without cleft palate) among newborns is 7.9 per 10,000 births, and the worldwide prevalence of cleft palate is 6.6 per 10,000 births (IPDTOC Working Group, 2011; Tanaka et al., 2012). However, regional variations in prevalence have been observed (Vanderas, 1987; Vieira et al., 2002). Identifying areas with higher prevalence rates may be important for the identifi-
cation of possible genetic, environmental, and other risk factors. Alta Verapaz, a rural department (state) in northcentral Guatemala (Fig. 1), is one of the departments ´ served by Asociaci on Compa nero Para Cirug ´ıa ˜ (ACPC), a Guatemala-based nongovernmental organization that provides a variety of community health services, including a screening program that connects low-income rural residents to free surgical care, in collaboration with its US-based sister organization Partner for Surgery (Jacobsen and Bankoski, 2010). The ACPC also administers a nutritional support program for babies with cleft lip, cleft palate, and other disorders that can cause severe undernutrition. The population of Alta Verapaz is mostly indigenous; 93% of residents identify as members of Mayan cultural groups compared with 41% for Guatemala as a whole (PAHO, 2007). About 78% of residents live in poverty, defined by the National Statistics Institute (INE) as per capita annual spending on food of no more than Q9,031 (US$1,150); 38% live in extreme poverty, with annual food spending of less than Q4,380 (US$560) (INE, 2011). These rates are much higher than the national poverty rate of 54% and the national extreme poverty rate of 13% (INE, 2011). About 23% of residents of Alta Verapaz live more than an hour of road travel from a primary care facility, and 62% live more than an hour from a hospital even after accessing transportation (Owen et al., 2010). An evaluation of the local burden from birth defects was initiated by ACPC as a way of
Mr. Matute is Research Associate, CIENSA Centro de Inves´ y Salud, Guatemala City, Guatemala. Ms. tigaciones en Nutricion Lydick is graduate student, Department of Global & Community Health, George Mason University, Fairfax, Virginia. Ms. Olga R. Torres is President, CIENSA Centro de Investigaciones en ´ y Salud, Guatemala City, Guatemala. Dr. Owen is Nutricion Adjunct Professor, Department of Geography & GeoInformation Science, George Mason University, Fairfax, Virginia. Dr. Jacobsen is Associate Professor, Department of Global & Community Health, George Mason University, Fairfax, Virginia. This evaluation project was supported by funds from Partner for Surgery, McLean, Virginia. Submitted December 2013; Accepted May 2014. Address correspondence to: Kathryn H. Jacobsen, Department of Global & Community Health, George Mason University, 4400 University Drive, MS 5B7, Fairfax, Virginia 22030. E-mail [email protected]. DOI: 10.1597/13-347 377
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FIGURE 1 Location of Alta Verapaz within Guatemala.
determining the unmet need for nutritional support and surgical care in the communities they serve. METHODS Based on international statistics on birth defect rates and local information about the number of births attended by a typical midwife during a 1-year period, we estimated that about 140 midwives needed to be interviewed in order to have enough statistical power to estimate annual birth defect rates in Alta Verapaz. We used a two-stage clustersampling method to identify a representative sample of midwives from Alta Verapaz. First, 10 municipalities in the department were randomly sampled from a list of all 17 municipalities using a probability proportional to size method. Then two communities from each of the 10 sampled municipalities were randomly sampled for inclusion from a list of communities obtained from INE, again using a probability proportional to size method (Fig. 2) (INE, 2002). After consultation with government health personnel in Alta Verapaz, ACPC deemed the study to be exempt from review by a formal research ethics committee because the project was a program evaluation activity and no identifying information would be collected from midwives about the babies they had delivered. The study protocol was designed by CIENSA, a nonprofit health research consulting organization, and data were collected by CIENSA in collaboration with field staff from ACPC. After the data were collected, researchers from George Mason University were invited to assist with data analysis and interpretation.
Research personnel fluent in local Mayan dialects visited each of the 20 sampled communities to meet with community leaders. No list of midwives is available for Alta Verapaz, so community representatives were asked to introduce the research staff to the women in their communities who serve in this role. The data collection team attempted to recruit and interview all midwives named by community leaders, and those midwives were then asked to identify any other midwives practicing in adjacent communities. Because nearly every sampled community was home to fewer midwives than the seven needed to achieve the target sample size, as was expected for these small rural towns, additional midwives were recruited from neighboring communities until the desired number of midwives had consented to participate. All of the midwives in the originally sampled and additional communities who were asked to participate and had delivered at least one baby in the previous year consented to be in the study and completed an interview. The approximate locations of the 20 communities sampled as starting points for surveying are shown in Figure 2 (INE, 2002; SEGEPLAN, 2009). (Precise locations are not shown to protect the privacy of participants.) In total, 147 midwives from 87 communities in Alta Verapaz participated in the study, all of whom were certified to practice by the Ministry of Health. The mean age of the midwives was 52 years (range, 27 to 87 years). They had been practicing midwives for an average of 17 years (range, 0 to 60 years), with an average of 15 years of service (range, 0 to 55) in their current community. About 51% of the midwives practiced in a community less than 10 km from the nearest health center, 29% were 10 to 30 km from a health center, and 20% were more than 30 km from a health facility. All consenting midwives were interviewed by a research staff member in the local language. (In Alta Verapaz, Q’eqchi’ is the most widely spoken language, and 43% of indigenous residents speak no Spanish [UNDP, 2005].) Each midwife was asked her age, how long she had been a midwife, how long she had practiced in the community, if she was certified by the Ministry of Health, if she provided folic acid to pregnant women, and which months she had attended deliveries. Each midwife was also asked about the number of babies she had delivered in the previous 30 days, 3 months, 6 months, and 1 year. (Some midwives maintain notebooks with information about each of her deliveries, but most do not, so it was not possible to verify how much time had passed since each reported birth. The interviewers did not record the method of recall used by the participants.) Each woman was then shown pictures of cleft lip, cleft palate, and other birth defects and asked how many babies she delivered during the previous year had each of these birth defects. Midwives were not asked about the severity of a birth defect but simply identified the presence of a defect. All interviews were conducted between April 30 and May 22, 2012.
Matute et al., CLEFT LIP PREVALENCE IN GUATEMALA
FIGURE 2 Approximate locations of participating communities within Alta Verapaz.
The goal of statistical analysis was to estimate the total number of new cases of cleft lip and cleft palate in Alta Verapaz in 2012 and then to estimate the prevalence rate among newborns. Because the prevalence rate is quite small, the Clopper-Pearson method was used to determine the 95% confidence interval (CI) for the prevalence rate in the department. The Clopper-Pearson method provides a conservative estimate of the CI for a binomial distribution (Clopper and Pearson, 1934). RESULTS In total, 129 midwives in Alta Verapaz reported assisting with 2,117 births over the previous 12 months. (Some consenting midwives had not delivered a baby in the previous year.) Of these births, four babies were reported to have been born with cleft lip and one with cleft palate. Cleft lip with cleft palate was not reported. These numbers translate to a 1-year prevalence rate of 18.9 per 10,000 for cleft lip (4/2,117) and 4.7 per 10,000 for cleft palate (1/2,117). Because of the small sample size, it is not possible to provide statistics at the subdepartment level. The government of Guatemala estimates that there were 34,986 total births in Alta Verapaz as a whole in 2012 (MSPAS, 2013). When the birth defect rates from the sampled population are applied to the department as a whole, an estimated 66 cases of cleft lip (95% CI ¼ 18, 169) and 16 cases of cleft palate (95% CI ¼ 0, 92) occurred among newborns in Alta Verapaz in 2012. DISCUSSION The 18.9 per 10,000 prevalence rate for cleft lip in the study population is higher than that reported from other countries in Latin America. For example, the prevalence rate for cleft lip with or without cleft palate has been reported to be 6.7 per 10,000 in Costa Rica
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(Tanaka et al., 2012), 11.4 in Chile (Nazer et al., 2001), 12.3 in Bolivia (McLeod, 2004), 12.9 in South America (IPDTOC, 2011), and 13.7 in Mexico (Tanaka et al., 2012). The prevalence rate in Alta Verapaz also appears to be higher than the rate reported from other world regions; for example, the prevalence rate is 8.6 per 10,000 in Europe (EUROCAT, 2014), 10.2 in Asia (Tanaka et al., 2012), and 10.6 in the United States (Parker et al., 2010). However, the 4.7 per 10,000 prevalence of cleft palate in the study population is similar to the rates reported by other studies from Latin America. A prevalence rate of 4.7 was reported in Argentina (Campana ˜ et al., 2010) and 4.8 in Chile (Nazer et al., 2001). The prevalence rate from the study population was slightly lower than the rates of 5.7 reported in Europe (EUROCAT, 2014) and 6.4 in the United States (Parker et al., 2010). A higher birth defect rate among the indigenous population of Guatemala may be related to low dietary and supplemental folic acid (Wehby and Murray, 2010). About 27% of midwives reported that folic acid is distributed to pregnant women at health care facilities, and 31% reported distribution by community health workers. Only two midwives said they provided folic acid to their clients. These statistics suggest relatively low folic acid coverage rates. Fumonisin mycotoxin exposure is another possible contributor. Fumonisin mycotoxin in maize occurs in high doses in rural Guatemalan diets (Torres et al., 2007) and may interfere with folic acid metabolism (Stevens and Tang, 1997). In rats (though not yet in humans), fumonisins have also been shown to have an association with neural tube defects (Marasas et al., 2004). It is possible that the lack of regular recordkeeping by midwives led to overestimates of the cleft lip prevalence rate and underestimates of the cleft palate rate. A visible birth defect such as cleft lip may be more memorable than a more hidden defect like cleft palate, causing midwives to incorrectly recall births of babies with cleft lip as having occurred within the previous year even if they happened longer ago. Similarly, our referral-based sampling approach may have led to an overestimation of the numerator if midwives known to have assisted with delivery of a baby with a birth defect were preferentially referred to the research team. Additionally, the prevalence rates may also be inaccurate because the denominator information about birth rates in Alta Verapaz had to be estimated from incomplete vital statistics data. However, this preliminary evidence suggests that Alta Verapaz—and perhaps, more generally, indigenous Mayan communities in Guatemala—might have a relatively high cleft lip prevalence rate compared with the global average. If this higher prevalence of cleft lip is validated with larger studies, Alta Verapaz may be a good site for examining the genetic, environmental, and
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nutritional factors that may contribute to the development of cleft lip. REFERENCES ´ Campana Camelo JS; Grupo de Estudio del ˜ H, Pawluk MS, Lopez ´ ECLAMC. Prevalencia al nacimiento de 27 anomal ´ıas congenitas seleccionadas, en 7 regiones geogra´ficas de la Argentina. Arch Argent Pediatr. 2010;108:409–417. Clopper CJ, Pearson ES. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika. 1934;26:404–413. European Surveillance of Congenital Abnormalities (EUROCAT). Cases and prevalence (per 10,000 births) for all full member registries from 2008 to 2012. Available at http://www. eurocat-network.eu/AccessPrevalenceData/PrevalenceTables. Accessed April 15, 2014. Hunt O, Burden D, Hepper P, Johnston C. The psychosocial effects of cleft lip and palate: a systematic review. Eur J Orthod. 2005;27:274– 285. ´ y Instituto Nacional de Estad ´ıstico (INE). Censo de poblacion ´ 2002. Guatemala City: INE; 2002. habitacion: Instituto Nacional de Estad ´ıstico (INE). Pobreza y desarrollo: Un enfoque departamental. Encuesta nacional de condiciones de vida: 2011. Guatemala City: INE; 2011. International Perinatal Database of Typical Oral Clefts (IPDTOC) Working Group. Prevalence at birth of cleft lip with or without cleft palate: Data from the International Perinatal Database of Typical Oral Clefts (IPDTOC). Cleft Palate Craniofac J. 2011;48:66–81. Jacobsen KH, Bankoski AJ. Predictors of compliance with scheduled surgery in rural Guatemala. Int Health. 2010;2:206–211. John A, Sell D, Sweeney T, Harding-Bell A, Williams A. The cleft audit protocol for speech–augmented: a validated and reliable measure for auditing cleft speech. Cleft Palate Craniofac J. 2006;43:272–288. Marasas WF, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-van Waes J, Missmer SA, Cabrera J, Torres O, Gelderblom WC, et al. Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr. 2004;134:711–716. McLeod NM, Urisote MLA, Saeed NR. Birth prevalence of cleft lip and palate in Sucre, Bolivia. Cleft Palate Craniofac J. 2004;41:195– 198.
Ministerio de Salud Publica ´ y Asistencia Social (MSPAS). Nacimientos por ano ´ departamento de residencia de la ˜ de ocurrencia, segun madre, per ´ıodo 2003–2012. Guatemala City: Gobierno de Guatemala; 2013. Nazer J, Hubner ME, Catala´n J, Cifuentes L. Incidencia de labio leporino y paladar hendido en la Maternidad del Hospital Cl ´ınico de la Universidad de Chile y en las maternidades chilenas participantes en el Estudio Colaborativo Latino Americano de ´ Malformaciones Congenitas (ECLAMC) per ´ıodo 1991–1999. Rev Med Chil. 2001;129:285–293. ´ EJ, Jacobsen KH. A geographic analysis of access Owen KK, Obregon to health services in rural Guatemala. Int Health. 2010;2:143–149. Pan American Health Organization (PAHO). Salud en las Americas ´ 2007. Volume II-Paıses. Washington, DC: PAHO; 2007:392–411. Parker SE, Mai CT, Canfield MA, Rickard R, Wang Y, Meyer RE, Anderson P, Mason CA, Collins JS, Kirby RS, et al. Updated national birth prevalence estimates for selected birth defects in the United States, 2004–2006. Birth Defects Res A Clin Mol Teratol. 2010;88:1008–1016. ´ ´ Secretar ´ıa de Planificacion y Programacion de la Presidencia (SEGEPLAN). Infraestructura de Datos Espaciales de Guatemala (IDEG), 2009. Available at http://ide.segeplan.gob.gt. Accessed November 10, 2013. Stevens VL, Tang J. Fumonisin B1-induced sphingolipid depletion inhibits vitamin uptake via the glycosylphosphatidylinositol-anchored folate receptor. J Biol Chem. 1997;272:18020–18025. Tanaka SA, Mahabir RC, Jupiter DC, Menezes JM. Updating the epidemiology of cleft lip with or without cleft palate. Plast Reconstr Surg. 2012;129:511e–518e. Torres OA, Palencia E, Lopez de Pratdesaba L, Grajeda R, Fuentes M, Speer MC, Merrill AH Jr, O’Donnell K, Bacon CW, Glenn AE, Riley RT. Estimated fumonisin exposure in Guatemala is greatest in consumers of lowland maize. J Nutr. 2007;137:2723–2729. ´ United Nations Development Programme (UNDP). Diversidad etnico´ en un Estado plural. cultural y desarrollo humano: la ciudadanıa Informe nacional de desarrollo humano: Guatemala. Guatemala City: UNDP; 2005. Report No. P964. Vanderas AP. Incidence of cleft lip, cleft palate, and cleft lip and palate among races: a review. Cleft Palate J. 1987;24:216–225. Vieira AR, Karras JC, Orioli IM, Castilla EE, Murray JC. Genetic origins in a South American clefting population. Clin Genet. 2002;62:458–463. Wehby GL, Murray JC. Folic acid and orofacial clefts: a review of the evidence. Oral Dis. 2010;16:11–19.
BRIEF COMMUNICATION Prevalence of Cleft Lip and Cleft Palate in Rural North-Central Guatemala Jorge Matute, M.Sc., Elaine A. Lydick, M.S., Olga R. Torres, M.Sc., Karen K. Owen, Ph.D., Kathryn H. Jacobsen, M.P.H., Ph.D. Objective: To estimate the number of new cases of cleft lip and cleft palate in the department (state) of Alta Verapaz, Guatemala, in 2012. Design: Cross-sectional survey of midwives from communities identified through a two-stage cluster-sampling process. Midwives were asked how many babies they had delivered in the past year and how many of those newborns had various types of birth defects, as illustrated in pictures. Setting: Indigenous Mayan communities in rural north-central Guatemala. Participants: Midwives (n ¼ 129) who had delivered babies in the previous year. Main Outcome Measure: Reports of babies born with cleft lip and cleft palate. Results: A 1-year prevalence rate of 18.9 per 10,000 for cleft lip and 4.7 per 10,000 for cleft palate was estimated for Alta Verapaz. None of the cases of cleft lip also had cleft palate. Conclusion: The indigenous communities in north-central Guatemala might have a relatively high cleft lip prevalence rate compared with the global average. KEY WORDS:
cleft lip, cleft palate, indigenous population
Cleft lip and cleft palate are congenital deformities that may lead to malnutrition when infants with these birth defects have difficulty feeding and are unable to receive adequate nutrition. If not surgically corrected in infancy or early childhood, these conditions may lead to speech communication disorders and possibly increase the risk of psychosocial problems and depression (Hunt et al., 2005; John et al., 2006). The International Perinatal Database of Typical Oral Clefts (IPDTOC) estimates that the global prevalence of cleft lip (with or without cleft palate) among newborns is 7.9 per 10,000 births, and the worldwide prevalence of cleft palate is 6.6 per 10,000 births (IPDTOC Working Group, 2011; Tanaka et al., 2012). However, regional variations in prevalence have been observed (Vanderas, 1987; Vieira et al., 2002). Identifying areas with higher prevalence rates may be important for the identifi-
cation of possible genetic, environmental, and other risk factors. Alta Verapaz, a rural department (state) in northcentral Guatemala (Fig. 1), is one of the departments ´ served by Asociaci on Compa nero Para Cirug ´ıa ˜ (ACPC), a Guatemala-based nongovernmental organization that provides a variety of community health services, including a screening program that connects low-income rural residents to free surgical care, in collaboration with its US-based sister organization Partner for Surgery (Jacobsen and Bankoski, 2010). The ACPC also administers a nutritional support program for babies with cleft lip, cleft palate, and other disorders that can cause severe undernutrition. The population of Alta Verapaz is mostly indigenous; 93% of residents identify as members of Mayan cultural groups compared with 41% for Guatemala as a whole (PAHO, 2007). About 78% of residents live in poverty, defined by the National Statistics Institute (INE) as per capita annual spending on food of no more than Q9,031 (US$1,150); 38% live in extreme poverty, with annual food spending of less than Q4,380 (US$560) (INE, 2011). These rates are much higher than the national poverty rate of 54% and the national extreme poverty rate of 13% (INE, 2011). About 23% of residents of Alta Verapaz live more than an hour of road travel from a primary care facility, and 62% live more than an hour from a hospital even after accessing transportation (Owen et al., 2010). An evaluation of the local burden from birth defects was initiated by ACPC as a way of
Mr. Matute is Research Associate, CIENSA Centro de Inves´ y Salud, Guatemala City, Guatemala. Ms. tigaciones en Nutricion Lydick is graduate student, Department of Global & Community Health, George Mason University, Fairfax, Virginia. Ms. Olga R. Torres is President, CIENSA Centro de Investigaciones en ´ y Salud, Guatemala City, Guatemala. Dr. Owen is Nutricion Adjunct Professor, Department of Geography & GeoInformation Science, George Mason University, Fairfax, Virginia. Dr. Jacobsen is Associate Professor, Department of Global & Community Health, George Mason University, Fairfax, Virginia. This evaluation project was supported by funds from Partner for Surgery, McLean, Virginia. Submitted December 2013; Accepted May 2014. Address correspondence to: Kathryn H. Jacobsen, Department of Global & Community Health, George Mason University, 4400 University Drive, MS 5B7, Fairfax, Virginia 22030. E-mail [email protected]. DOI: 10.1597/13-347 377
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FIGURE 1 Location of Alta Verapaz within Guatemala.
determining the unmet need for nutritional support and surgical care in the communities they serve. METHODS Based on international statistics on birth defect rates and local information about the number of births attended by a typical midwife during a 1-year period, we estimated that about 140 midwives needed to be interviewed in order to have enough statistical power to estimate annual birth defect rates in Alta Verapaz. We used a two-stage clustersampling method to identify a representative sample of midwives from Alta Verapaz. First, 10 municipalities in the department were randomly sampled from a list of all 17 municipalities using a probability proportional to size method. Then two communities from each of the 10 sampled municipalities were randomly sampled for inclusion from a list of communities obtained from INE, again using a probability proportional to size method (Fig. 2) (INE, 2002). After consultation with government health personnel in Alta Verapaz, ACPC deemed the study to be exempt from review by a formal research ethics committee because the project was a program evaluation activity and no identifying information would be collected from midwives about the babies they had delivered. The study protocol was designed by CIENSA, a nonprofit health research consulting organization, and data were collected by CIENSA in collaboration with field staff from ACPC. After the data were collected, researchers from George Mason University were invited to assist with data analysis and interpretation.
Research personnel fluent in local Mayan dialects visited each of the 20 sampled communities to meet with community leaders. No list of midwives is available for Alta Verapaz, so community representatives were asked to introduce the research staff to the women in their communities who serve in this role. The data collection team attempted to recruit and interview all midwives named by community leaders, and those midwives were then asked to identify any other midwives practicing in adjacent communities. Because nearly every sampled community was home to fewer midwives than the seven needed to achieve the target sample size, as was expected for these small rural towns, additional midwives were recruited from neighboring communities until the desired number of midwives had consented to participate. All of the midwives in the originally sampled and additional communities who were asked to participate and had delivered at least one baby in the previous year consented to be in the study and completed an interview. The approximate locations of the 20 communities sampled as starting points for surveying are shown in Figure 2 (INE, 2002; SEGEPLAN, 2009). (Precise locations are not shown to protect the privacy of participants.) In total, 147 midwives from 87 communities in Alta Verapaz participated in the study, all of whom were certified to practice by the Ministry of Health. The mean age of the midwives was 52 years (range, 27 to 87 years). They had been practicing midwives for an average of 17 years (range, 0 to 60 years), with an average of 15 years of service (range, 0 to 55) in their current community. About 51% of the midwives practiced in a community less than 10 km from the nearest health center, 29% were 10 to 30 km from a health center, and 20% were more than 30 km from a health facility. All consenting midwives were interviewed by a research staff member in the local language. (In Alta Verapaz, Q’eqchi’ is the most widely spoken language, and 43% of indigenous residents speak no Spanish [UNDP, 2005].) Each midwife was asked her age, how long she had been a midwife, how long she had practiced in the community, if she was certified by the Ministry of Health, if she provided folic acid to pregnant women, and which months she had attended deliveries. Each midwife was also asked about the number of babies she had delivered in the previous 30 days, 3 months, 6 months, and 1 year. (Some midwives maintain notebooks with information about each of her deliveries, but most do not, so it was not possible to verify how much time had passed since each reported birth. The interviewers did not record the method of recall used by the participants.) Each woman was then shown pictures of cleft lip, cleft palate, and other birth defects and asked how many babies she delivered during the previous year had each of these birth defects. Midwives were not asked about the severity of a birth defect but simply identified the presence of a defect. All interviews were conducted between April 30 and May 22, 2012.
Matute et al., CLEFT LIP PREVALENCE IN GUATEMALA
FIGURE 2 Approximate locations of participating communities within Alta Verapaz.
The goal of statistical analysis was to estimate the total number of new cases of cleft lip and cleft palate in Alta Verapaz in 2012 and then to estimate the prevalence rate among newborns. Because the prevalence rate is quite small, the Clopper-Pearson method was used to determine the 95% confidence interval (CI) for the prevalence rate in the department. The Clopper-Pearson method provides a conservative estimate of the CI for a binomial distribution (Clopper and Pearson, 1934). RESULTS In total, 129 midwives in Alta Verapaz reported assisting with 2,117 births over the previous 12 months. (Some consenting midwives had not delivered a baby in the previous year.) Of these births, four babies were reported to have been born with cleft lip and one with cleft palate. Cleft lip with cleft palate was not reported. These numbers translate to a 1-year prevalence rate of 18.9 per 10,000 for cleft lip (4/2,117) and 4.7 per 10,000 for cleft palate (1/2,117). Because of the small sample size, it is not possible to provide statistics at the subdepartment level. The government of Guatemala estimates that there were 34,986 total births in Alta Verapaz as a whole in 2012 (MSPAS, 2013). When the birth defect rates from the sampled population are applied to the department as a whole, an estimated 66 cases of cleft lip (95% CI ¼ 18, 169) and 16 cases of cleft palate (95% CI ¼ 0, 92) occurred among newborns in Alta Verapaz in 2012. DISCUSSION The 18.9 per 10,000 prevalence rate for cleft lip in the study population is higher than that reported from other countries in Latin America. For example, the prevalence rate for cleft lip with or without cleft palate has been reported to be 6.7 per 10,000 in Costa Rica
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(Tanaka et al., 2012), 11.4 in Chile (Nazer et al., 2001), 12.3 in Bolivia (McLeod, 2004), 12.9 in South America (IPDTOC, 2011), and 13.7 in Mexico (Tanaka et al., 2012). The prevalence rate in Alta Verapaz also appears to be higher than the rate reported from other world regions; for example, the prevalence rate is 8.6 per 10,000 in Europe (EUROCAT, 2014), 10.2 in Asia (Tanaka et al., 2012), and 10.6 in the United States (Parker et al., 2010). However, the 4.7 per 10,000 prevalence of cleft palate in the study population is similar to the rates reported by other studies from Latin America. A prevalence rate of 4.7 was reported in Argentina (Campana ˜ et al., 2010) and 4.8 in Chile (Nazer et al., 2001). The prevalence rate from the study population was slightly lower than the rates of 5.7 reported in Europe (EUROCAT, 2014) and 6.4 in the United States (Parker et al., 2010). A higher birth defect rate among the indigenous population of Guatemala may be related to low dietary and supplemental folic acid (Wehby and Murray, 2010). About 27% of midwives reported that folic acid is distributed to pregnant women at health care facilities, and 31% reported distribution by community health workers. Only two midwives said they provided folic acid to their clients. These statistics suggest relatively low folic acid coverage rates. Fumonisin mycotoxin exposure is another possible contributor. Fumonisin mycotoxin in maize occurs in high doses in rural Guatemalan diets (Torres et al., 2007) and may interfere with folic acid metabolism (Stevens and Tang, 1997). In rats (though not yet in humans), fumonisins have also been shown to have an association with neural tube defects (Marasas et al., 2004). It is possible that the lack of regular recordkeeping by midwives led to overestimates of the cleft lip prevalence rate and underestimates of the cleft palate rate. A visible birth defect such as cleft lip may be more memorable than a more hidden defect like cleft palate, causing midwives to incorrectly recall births of babies with cleft lip as having occurred within the previous year even if they happened longer ago. Similarly, our referral-based sampling approach may have led to an overestimation of the numerator if midwives known to have assisted with delivery of a baby with a birth defect were preferentially referred to the research team. Additionally, the prevalence rates may also be inaccurate because the denominator information about birth rates in Alta Verapaz had to be estimated from incomplete vital statistics data. However, this preliminary evidence suggests that Alta Verapaz—and perhaps, more generally, indigenous Mayan communities in Guatemala—might have a relatively high cleft lip prevalence rate compared with the global average. If this higher prevalence of cleft lip is validated with larger studies, Alta Verapaz may be a good site for examining the genetic, environmental, and
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