Figures
Abstract
Introduction
Although men and women have similar risk factors for cardiovascular disease, many social behaviors in developing countries differ by sex. Rural-to-urban migrants have different cardiovascular risk profiles than rural or urban dwellers. The objective of this study was to evaluate the sex differences with specific cardiovascular risk factors in rural-to-urban migrants.
Methods and Results
We used the rural-to-urban migrant group of the PERU MIGRANT cross-sectional study to investigate the sex differences in specific cardiovascular risk factors: obesity, hypertension, metabolic syndrome, as well as exposures of socioeconomic status, acculturation surrogates and behavioral characteristics. Logistic regression analysis was used to characterize strength of association between sex and our outcomes adjusting for potential confounders. The sample of migrants was 589 (mean age 46.5 years) and 52.4% were female. In the adjusted models, women were more likely to be obese (OR=5.97; 95%CI: 3.21–11) and have metabolic syndrome (OR=2.22; 95%CI: 1.39–3.55) than men, explaining the greatest variability for obesity and metabolic syndrome but not for hypertension.
Citation: Bernabe-Ortiz A, Benziger CP, Gilman RH, Smeeth L, Miranda JJ (2012) Sex Differences in Risk Factors for Cardiovascular Disease: The PERU MIGRANT Study. PLoS ONE 7(4): e35127. https://doi.org/10.1371/journal.pone.0035127
Editor: Yan Gong, College of Pharmacy, University of Florida, United States of America
Received: January 17, 2012; Accepted: March 13, 2012; Published: April 5, 2012
Copyright: © 2012 Bernabe-Ortiz et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: ABO, RHG, JJM and the CRONICAS Center of Excellence in Chronic Diseases at UPCH is funded by the National Heart, Lung and Blood Institute (NHLBI), National Institutes of Health, Department of Health and Human Services, under contract no. HHSN268200900033C. CPB was supported by the National Institutes of Health and Fogarty International Center through the International Clinical Research Fellows Program at Vanderbilt University (R24 TW007988). The PERU MIGRANT Study was funded by a Wellcome Trust Masters Research Training Fellowship and a Wellcome Trust PhD Studentship to JJM (GR074833MA). LS is supported by a Wellcome Trust Senior Research Fellowship in Clinical Science. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: J. Jaime Miranda is a PLoS ONE Editorial Board member. This does not alter the authors' adherence to all the PLoS ONE policies on sharing data and materials.
Introduction
Cardiovascular diseases are rapidly becoming the leading causes of morbidity and mortality in low- and middle-income countries (LMIC) [1]. In these settings, urbanization, due mainly to internal migration, is one of the main contributors to the transition towards increasing CVD [2], [3], [4]. Thus, rise in cardiovascular diseases in LMIC can be attributed to changes in social and health behaviors, such as physical inactivity, decreased fruit intake and increased intake of energy dense foods and salt, as well as tobacco use and alcohol consumption [5], [6].
Rural-to-urban migrants have different cardiovascular risk profiles than rural or urban dwellers; yet, most of these studies are limited to international migrant pattern from developing to developed countries, particularly those residing in the United States. Few studies have addressed the impact of rural-to-urban migration on cardiovascular outcomes in LMIC, e.g. the Kenyan Luo migration study [7], Yi People Study in China [8], Indian Migration Study in India [9], and the PERU-MIGRANT study in Peru [10]. Recently, a systematic review of rural-to-urban migration studies concluded that several cardiovascular risk factors are higher or more common in migrants than in rural groups, but lower or less common than in urban groups [11].
While men and women have similar risk factors for cardiovascular diseases, many social behaviors in LMIC differ by sex. For example, women who smoke have three times the risk of heart attacks and have their first heart attacks much earlier than men and woman non-smokers [12]. A Brazilian study demonstrated that high cholesterol and hypertension were more prevalent among women compared to men [13]. In Peru, three studies have shown that metabolic syndrome, abdominal obesity, and low high density lipoprotein-cholesterol (HDL) are higher in women than men while there seems to be no differences in hypertension, hypertriglyceridemia or high fasting glucose [14], [15], [16].
Reliable estimates of prevalence, patterns and population distribution of cardiovascular risk factors in Latin American populations are needed in order to design effective treatment programs. The PERU MIGRANT study found that the impact of rural-to-urban migration on cardiovascular risk profile was not uniform across different risk factors, and was further influenced by the age at which migration occurred [10]. Moreover, a gradient was observed for some risk factors across study groups. The objectives of this study were to evaluate the sex differences in exposures to socioeconomic, acculturation and behavioral characteristics and assess the impact of sex on specific cardiovascular risk factors (obesity, hypertension, and metabolic syndrome) in a rural-to-urban migrant population.
Methods
Study Design, Setting, and Participants
The general objectives and design of the PERU-MIGRANT study have been previously published [17]. Briefly, a cross-sectional survey was performed using a single-stage random sampling and involving migrants from rural to urban areas in Peru. Potential participants, born in the rural setting of Ayacucho, who migrated to, and were currently living in the urban setting of Lima, were asked to participate. Ayacucho is a region of Peru located in the south-central Andes. Its capital is the city of Ayacucho and is relatively closed to Lima (8 hours by bus). The region was one of the hardest hit by terrorism, whose population massively migrated to coastal cities, especially to Lima.
The area called “Las Pampas de San Juan de Miraflores" was the setting where this study was undertaken. The sampling frame for this migrant group was the local census performed in 2000, updated in 2006, to identify all those who stated they had been born in the Department of Ayacucho and were currently living in Lima. The sample was stratified by sex and age groups to reduce the confounding due to these variables.
Data Collection
A team of community health workers was trained to enroll participants and to conduct the questionnaires assessing socio-demographic, acculturation and behavioral variables. As part of this evaluation, participants were invited to a clinic visit where height, weight, waist circumference (WC), systolic (SBP) and diastolic (DBP) blood pressure, as well as blood samples were obtained using standardized methods and calibrated tools [17]. Total cholesterol, triglycerides and HDL were measured in serum, whereas fasting glucose was assessed in plasma.
Outcomes and Variable Definitions
Three were our outcomes of interest: obesity, hypertension, and metabolic syndrome. Obesity was defined as body mass index (BMI) ≥30 kg/m2 for men and women according to accepted guidelines [18]. Hypertension was considered whether SBP ≥140 and/or DBP ≥90 mm Hg, or self-report of physician diagnosis and currently receiving anti-hypertensive medication [19], [20]. Because of established ethnic differences, we followed the International Diabetes Federation’s (IDF) cut-off points specific for non-European populations [21]. Thus, abdominal obesity according to IDF for our South American population was WC ≥90 cm (men) or ≥80 cm (women) [21], [22]. In addition to this, we also followed the Latin American Consortium in Obesity Studies (LASO) cut-off criteria of WC ≥97 cm (men) or ≥94 cm (women) [23], [24]. Finally, according to the harmonized criteria participants having 3 or more of the following criteria were defined as having metabolic syndrome: (1) abdominal obesity (ethnic specific cut-offs of WC >90 cm in men and >80 cm in women); (2) triglycerides ≥150 mg/dL or drug therapy for elevated triglycerides; (3) low HDL-cholesterol (<40 mg/dL in men and <50 mg/dL in women) or drug therapy for low HDL cholesterol; (4) SBP ≥130 mm Hg, DBP ≥85 mm Hg, or current pharmacologic treatment for hypertension; (5) fasting glucose ≥100 mg/dL or current antidiabetic medication use (insulin or oral agents) [21]. A detailed description of the socio-demographic, acculturation and behavioral variables is shown in File S1.
Statistical Analysis
STATA 11 for Windows (STATA CORP, College Station, Texas, USA) was used for all analyses. Initially, a brief description of the socio-demographic, acculturation, behavioral, and clinical variables was performed according to sex. Frequencies and percentages were used to present categorical variables. Then, age-adjusted odds ratios (OR) and 95% confidence intervals (95%CI) were estimated using logistic regression (crude model). Finally, the strength of the association between sexes (male as reference) and our outcomes of interest were estimated adjusting for potential confounders. Diverse models were generated including different confounders such as socio-demographic variables (education level, socioeconomic status using household assets); acculturation surrogates (language spoken at home, language preferences for listening, age at first migration, and lifetime urban exposure); and behavioral variables (smoking, alcohol consumption, and physical activity level).
Results
A total of 872 potential participants were contacted an asked to participated, but only 589 (participation rate: 67.5%) completed the survey. The sample of migrants was 589; 52.5% were females, on average the sample age was 47.8 years (SD±11.7), and had a mean of age of first migration of 14.7 years (inter-quartile range, IQR: 10–17).
Sex Differences in Cardiovascular Risk Profile
Demographic, socioeconomic status (SES), acculturation, and behavioral variables stratified by sex are shown in Table 1. Compared to women, men were more likely to have higher socioeconomic status –completed secondary or higher education and household assets–, to use Spanish as the language of preference at home and more likely to be current smokers and binge drinkers. Women were more likely to be moderately physically active, whereas men were more likely to reported heavy physical activity.
Regarding our outcomes of interest, women had greater prevalences of obesity, assessed by BMI, and metabolic syndrome, whereas hypertension prevalence was similar. Women were more likely to be obese by BMI and WC definitions (Figure 1). According to metabolic syndrome components, abdominal obesity and low HDL were more common among females, whereas high blood pressure was more frequent among males (Table 2).
*Based on IDF WC cut-off criteria [WC ≥90 cm (men) or ≥80 cm (women)]. **Based on LASO WC cut-off criteria [WC ≥97 cm (men) or ≥94 cm (women)].
Determinants of Cardiovascular Risk Factors
In the multivariable models, after adjusting for other potential factors, sex was an independent predictor for obesity and metabolic syndrome (Table 3) and women were almost six times more likely to be obese and twice as likely of having metabolic syndrome. There was no evidence of an association between sex and hypertension; however, further adjustment for acculturation variables and also alcohol consumption provided strong evidence of an association between sex and hypertension. Nevertheless, this association was attenuated in the fully adjusted model (Table 3).
Discussion
In this study, using rural-to-urban migrant data, we observed important differences according to sex in the prevalence of obesity, metabolic syndrome, and hypertension after adjusting for well-known risk factors. The present analysis expands on previous observations by taking advantage of proxies for acculturation in the setting of rural-to-urban within-country migration and its relationship with major cardiovascular risk factors. Thus, our results are consistent with the literature, including other Peruvian studies, which have shown that metabolic syndrome and obesity are higher in women than men while there seems to be no differences in hypertension [14], [15], [25]. However, a previous report involving Brazilian population found that hypertension was more prevalent among women compared to men [13].
Regarding metabolic syndrome components, prevalence differences in this population are mainly due to abdominal obesity and low HDL among women than elevated blood pressure, which was more common among men. These results are compatible to previous studies [16], [26], [27]. In addition, a preliminary work in a similar socioeconomic setting of urban poverty showed that women are less likely to seek help for symptoms compatible to acute coronary syndrome [28]. Furthermore, our results suggest that women might be in disadvantage facing cardiovascular disease.
The reported prevalence of obesity in Latin American populations varies greatly (9.9% to 35.7%) [29]. General adiposity and abdominal obesity are associated with an increased risk of death from cardiovascular disease [30]; however, cut-offs derived from other populations for use in our population have been questioned. In the LASO study, waist-to-hip ratio was found to be the most accurate anthropometric indicator for high risk of cardiovascular disease [24]. Obesity has been associated with older age at first migration, language speaking proficiency, and language preferences in migrant population [31]. Thus, these variables were included in our models. After adjusting for acculturation variables, we found female migrants were more likely to be obese, have hypertension and have metabolic syndrome than men. These findings suggest that urbanization and the migration process do indeed have an important influential effect on cardiovascular disease profile, equal or more than socioeconomic factors per se, which differs by sex. Traditionally, migrants tend to be a highly self-selected group, whereby the healthier, wealthier residents of an area migrate to urban areas for better opportunities [32]. In this case, rural-to-urban migrants from Ayacucho (Peru) fled the area due to strong political violence [33] rather than only a migration for economic reasons: the migrants were not simply a small self-selected atypical group.
Of note, among biological markers for metabolic syndrome, a great proportion of women had HDL under the recommended cut-offs [22]. Although, on average, HDL mean was significantly lower among men (data not shown), the proportion of women with low HDL was 71.2%. These findings have been previously reported in different Peruvian women [14], [15], [16] and are also observed in our migrant population.
The study benefits from the use of a well-defined rural-to-urban within-country migrant population, as well as objective measures of anthropometry, biochemical and metabolic markers. However, the study is of limited generalizability because it was conducted in a specific group of migrants from a socially deprived urban part of Lima, Peru. The group of migrants was well established in the area, many having lived there for over 20 years. Due to the cross-sectional nature of the study, we are unable to comment about the causal relationship between sex and migration, and whether the differences are due to migration per se, or the urban environment.
Previous work by our group with the same dataset, examined the differences between the migrant group, and urban and rural dwellers but sex differences were not explored [10]. In addition, the PERU MIGRANT study did not address dietary patterns, contraceptives and hormone therapy use, or menopause status in this population. After menopause, the lipid profile changes in women, with increasing levels of LDL and decreasing levels of HDL cholesterol [34]. The role of sex hormones and how they affect CVD risk factors in this population was not assessed. Finally, our study may have been underpowered to detect some of the sex differences, for example between smoking and hypertension. However, our study involved a great number of migrants and is the first to show associations between sex and cardiovascular risk factors.
Conclusions
The findings in this rural-to-urban migrant population suggest that sex is an important factor associated with established cardiovascular risk factors. Regarding metabolic syndrome components, abdominal obesity and low HDL-cholesterol are more common among women, whereas elevated blood pressure component is more frequent among men. Secondarily, smoking and alcohol use are similarly more prevalent in men. Thus, treatment and prevention programs should address sex differences, as well as the unique health needs of migrant populations living in urban shantytowns.
Supporting Information
File S1.
Definitions of socio-demographic and behavioral variables.
https://doi.org/10.1371/journal.pone.0035127.s001
(DOCX)
Acknowledgments
Our special gratitude to various colleagues at Universidad Peruana Cayetano Heredia and A.B. PRISMA in Lima, Peru and several others in the United Kingdom, as well as to the staff and the team of fieldworkers who contributed to different parts of this study.
Author Contributions
Conceived and designed the experiments: AB-O CPB JJM. Performed the experiments: AB-O CPB JJM. Analyzed the data: AB-O CPB. Contributed reagents/materials/analysis tools: RHG LS JJM. Wrote the paper: AB-O CPB JJM. Conceived, designed and supervised the overall project: RHG LS JJM. Revised the manuscript for important intellectual content: AB-O RHG LS JJM. Gave final approval of the version submitted for publication: AB-O CPB RHG LS JJM.
References
- 1.
World Health Organization (2011) Global status report on noncommunicable diseases 2010. Geneva, Switzerland: WHO.
- 2. Patel RB, Burke TF (2009) Urbanization–an emerging humanitarian disaster. N Engl J Med 361: 741–743.
- 3.
United Nations Population Fund (2007) The State of World Population 2007: Unleashing the Potential of Urban Growth. New York, US: UNFPA.
- 4. Van Ginkel H (2008) Urban Future. Nature 456: 32–33.
- 5. Cecchini M, Sassi F, Lauer JA, Lee YY, Guajardo-Barron V, et al. (2011) Tackling of unhealthy diets, physical inactivity, and obesity: health effects and cost-effectiveness. Lancet 376: 1775–1784.
- 6. Epping-Jordan JE, Galea G, Tukuitonga C, Beaglehole R (2005) Preventing chronic diseases: taking stepwise action. Lancet 366: 1667–1671.
- 7. Poulter NR, Khaw KT, Hopwood BE, Mugambi M, Peart WS, et al. (1990) The Kenyan Luo migration study: observations on the initiation of a rise in blood pressure. BMJ 300: 967–972.
- 8. He J, Klag MJ, Whelton PK, Chen JY, Mo JP, et al. (1991) Migration, blood pressure pattern, and hypertension: the Yi Migrant Study. Am J Epidemiol 134: 1085–1101.
- 9. Ebrahim S, Kinra S, Bowen L, Andersen E, Ben-Shlomo Y, et al. (2010) The effect of rural-to-urban migration on obesity and diabetes in India: a cross-sectional study. PLoS Med 7: e1000268.
- 10. Miranda JJ, Gilman RH, Smeeth L (2011) Differences in cardiovascular risk factors in rural, urban and rural-to-urban migrants in Peru. Heart 97: 787–796.
- 11.
Hernandez AV, Pasupuleti V, Deshpande A, Bernabe-Ortiz A, Miranda JJ (2011) Effect of rural-to-urban within-country migration on cardiovascular risk factors in low- and middle-income countries: a systematic review. Heart.
- 12. Wenger NK (1995) Hypertension and other cardiovascular risk factors in women. Am J Hypertens 8: 94s–99s.
- 13. Castanho VS, Oliveira LS, Pinheiro HP, Oliveira HC, de Faria EC (2001) Sex differences in risk factors for coronary heart disease: a study in a Brazilian population. BMC Public Health 1: 3.
- 14. Medina-Lezama J, Zea-Diaz H, Morey-Vargas OL, Bolanos-Salazar JF, Munoz-Atahualpa E, et al. (2007) Prevalence of the metabolic syndrome in Peruvian Andean hispanics: the PREVENCION study. Diabetes Res Clin Pract 78: 270–281.
- 15. Seclen S, Villena A, Larrad MT, Gamarra D, Herrera B, et al. (2006) Prevalence of the metabolic syndrome in the mestizo population of peru. Metab Syndr Relat Disord 4: 1–6.
- 16. Malaga G, Zevallos-Palacios C, Lazo M de L, Huayanay C (2010) [High frequency of dyslipidemia and impaired fasting glycemia in a high altitude Peruvian population]. Rev Peru Med Exp Salud Publica 27: 557–561.
- 17. Miranda JJ, Gilman RH, Garcia HH, Smeeth L (2009) The effect on cardiovascular risk factors of migration from rural to urban areas in Peru: PERU MIGRANT Study. BMC Cardiovasc Disord 9: 23.
- 18.
World Health Organization (2002) Reducing risks, promoting healthy life. Geneva, Switzerland: WHO.
- 19. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, et al. (2003) Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension 42: 1206–1252.
- 20. Mancia G, De Backer G, Dominiczak A, Cifkova R, Fagard R, et al. (2007) 2007 Guidelines for the management of arterial hypertension: The Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Eur Heart J 28: 1462–1536.
- 21. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, et al. (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120: 1640–1645.
- 22.
International Diabetes Federation (2006) The IDF consensus worldwide definition of the metabolic syndrome. Brussels, Belgium: IDF Communications.
- 23. Bautista LE, Casas JP, Herrera VM, Miranda JJ, Perel P, et al. (2009) The Latin American Consortium of Studies in Obesity (LASO). Obes Rev 10: 364–370.
- 24. Herrera VM, Casas JP, Miranda JJ, Perel P, Pichardo R, et al. (2009) Interethnic differences in the accuracy of anthropometric indicators of obesity in screening for high risk of coronary heart disease. Int J Obes (Lond) 33: 568–576.
- 25. Baracco R, Mohanna S, Seclen S (2007) A comparison of the prevalence of metabolic syndrome and its components in high and low altitude populations in peru. Metab Syndr Relat Disord 5: 55–62.
- 26. Cardenas Quintana H, Sanchez Abanto J, Roldan Arbieto L, Mendoza Tasayco F (2009) [Prevalence of metabolic syndrome in people 20 years old and more. Peru, 2005]. Rev Esp Salud Publica 83: 257–265.
- 27. Escobedo J, Schargrodsky H, Champagne B, Silva H, Boissonnet CP, et al. (2009) Prevalence of the metabolic syndrome in Latin America and its association with sub-clinical carotid atherosclerosis: the CARMELA cross sectional study. Cardiovasc Diabetol 8: 52.
- 28. Benziger CP, Bernabe-Ortiz A, Miranda JJ, Bukhman G (2011) Sex differences in Health Care-Seeking Behavior for Acute Coronary Syndrome in a Low Income Country - Peru. Crit Pathw Cardiol 10: 99–103.
- 29. Filozof C, Gonzalez C, Sereday M, Mazza C, Braguinsky J (2001) Obesity prevalence and trends in Latin-American countries. Obes Rev 2: 99–106.
- 30. Pischon T, Boeing H, Hoffmann K, Bergmann M, Schulze MB, et al. (2008) General and abdominal adiposity and risk of death in Europe. N Engl J Med 359: 2105–2120.
- 31. Bernabe-Ortiz A, Gilman RH, Smeeth L, Miranda JJ (2010) Migration surrogates and their association with obesity among within-country migrants. Obesity (Silver Spring) 18: 2199–2203.
- 32. Takenaka A, Pren KA (2010) Leaving to get ahead: assessing the relationship between mobility and inequality in Peruvian migration. Lat Am Perspect 37: 29–49.
- 33. Pedersen D, Tremblay J, Errazuriz C, Gamarra J (2008) The sequelae of political violence: assessing trauma, suffering and dislocation in the Peruvian highlands. Soc Sci Med 67: 205–217.
- 34.
Schenck-Gustafsson K (1996) Risk factors for cardiovascular disease in women: assessment and management. Eur Heart J 17 Suppl D. pp. 2–8.