Children in South Asia Have Higher Body Mass–Adjusted Blood Pressure Levels Than White Children in the United States
http://www.100md.com
循环学杂志 2005年第3期
the Clinical Epidemiology Unit, Department of Community Health Sciences (T.H.J., J.H.)
the Section of Nephrology, Department of Medicine (T.H.J.), and the Department of Medicine (M.I.)
Aga Khan University, Karachi, Pakistan; the Division of Nephrology (T.H.J., A.S.L.) and the Division of Clinical Care Research (C.H.S.)
Tufts-New England Medical Center, Department of Medicine, Tufts University School of Medicine School, Boston, Mass
the National Heart and Lung Institute, Imperial College London, UK (N.P., N.C.).
Abstract
Background— Blood pressure during childhood is an established predictor of adult blood pressure, which in turn increases mortality as a result of cardiovascular disease. Adult South Asian populations are particularly predisposed to cardiovascular disease compared with whites, but the prevalence of high blood pressure and determinants of blood pressure in South Asian children have not been explored or compared with those of white children.
Methods and Results— Analyses were performed on 5641 South Asian children 5 to 14 years old included in the nationally representative National Health Survey of Pakistan (NHSP) (1990–1994) and on 4756 white children 5 to 14 years old included in Third National Health and Nutrition Examination Survey (NHANES III) (1988–1994). Anthropometric measurements were obtained. Blood pressure was measured twice in the seated position with a mercury sphygmomanometer and an appropriate-size cuff. High blood pressure was defined as a systolic or diastolic blood pressure level that was 95th percentile of age-, sex-, and height-percentile–specific reference level for the US population. Mean body mass index (BMI)–adjusted blood pressure values were compared among children in 2 data sets by use of linear regression analysis. The overall prevalence (95% CI) of high blood pressure in South Asian children 5 to 14 years old was 12.2% (11.3% to 13.1%): 15.8% (14.5% to 17.1%) in boys and 8.7% (7.6% to 9.8%) in girls. This is in sharp contrast with the predicted 5% prevalence of high blood pressure in children in the United States (P<0.001). The mean BMI-adjusted systolic blood pressure levels (SD) were 100 (11) versus 99 (11) mm Hg (P<0.001), and diastolic blood pressure levels (SD) were 63 (10) versus 52 (12) mm Hg (P<0.001) in NHSP versus NHANES III, respectively.
Conclusions— South Asian children have higher body-mass–adjusted blood pressure levels than white children in the United States. Further studies are needed to determine factors responsible for these differences. Immediate attention is needed to address high blood pressure and its risk factors in native South Asian children.
Key Words: blood pressure ; pediatrics ; epidemiology ; ethnic groups
Introduction
Migrant populations of South Asian origin (India, Pakistan, and Bangladesh) living in the West are at higher risk of cardiovascular disease (CVD) compared with whites,1–3 but the problems of noncommunicable diseases are not limited only to South Asian populations residing in the West. South Asian countries, home to approximately one quarter of the world’s population, are major contributors to the global burden of CVD at present, and this contribution is projected to grow, given their consistent population growth rates.4 Hypertension, the most common risk factor for CVD, has now become a major health problem in Pakistan, affecting 17.9% of all adults 15 years old and 1 in 3 adults 45 years old.5 Thus, prevention of high blood pressure and CVD needs urgent attention in South Asia.
The knowledge that blood pressure during childhood is an established predictor of adult blood pressure, which in turn increases mortality from CVD, clearly underscores the importance of studying childhood blood pressure and the need for establishing preventive measures in early life.6,7 The Fourth Report on the Diagnosis, Evaluation, and Treatment of High Blood Pressure in Children and Adolescents recommends age-, sex-, and height-specific values that are at >95th percentile of normative systolic and diastolic blood pressure values as diagnostic of high blood pressure in childhood.8 Unfortunately, data on age-specific blood pressure levels in children of South Asian origin are scarce. To date, studies of blood pressure in South Asian children have suffered from inadequate sample size or have been restricted to distinct communities.9–12
We therefore used data in South Asian children 5 to 14 years old included in the nationally representative National Health Survey of Pakistan (NHSP) (1990–1994) to determine the prevalence of high blood pressure in children in Pakistan. We also compared blood pressure levels among children 5 to 14 years old included in the NHSP with those surveyed in the United States during the Third National Health and Nutrition Examination Survey (NHANES III), 1988 to 1994.13 In addition, we studied the correlates of systolic and diastolic blood pressure in South Asian children.
Methods
NHSP (1990–1994)
Cross-sectional data were collected during the NHSP over a period of 4 years (1990–1994) by the Pakistan Medical Research Council, under the technical guidance and support of the US National Center for Health Statistics (NCHS).14 The overall design of NHSP was a modification of NHANES III conducted by the NCHS, tailored to the needs of Pakistan. The details of sampling, design, components, survey instrument, and quality control have been reported previously.5,15 Briefly, the survey was conducted on a nationally representative sample of 18 135 individuals 6 months to 110 years old from 2400 urban and rural households after informed consent had been obtained. A 2-stage stratified design was used. The urban and rural areas of each of the 4 provinces of Pakistan were taken as strata. There were 80 urban or rural primary sampling units. A total of 30 households were drawn into the sample from each unit, and all residents of the household were included in the study. The overall individual response rate was 92.6%. The total number of individuals 5 years old was 15 083. Out of these, 5641 subjects were between 5 and 14 years old.
Data on demographic, lifestyle, socioeconomic, and health-related variables were collected by use of a questionnaire validated in local languages. Physicians at mobile examination centers performed a standardized physical examination. Mothers were proxy respondents for children <12 years old. Trained technicians performed anthropometric examinations. Blood pressure was measured by certified physicians in a standardized manner. Blood pressure certification consisted of measurement performance on live volunteers. As in NHANES III, the physician selected one of 5 (infant, child, adult, large adult, and thigh) cuff sizes for blood pressure measurement on the basis of the size of the participant’s arm. Blood pressure was measured in the seated position by use of a mercury sphygmomanometer with the right forearm horizontal on a table. After the appropriate-size cuff for children had been applied (covering approximately two thirds of the upper arm), the cuff was gradually inflated to approximately 20 mm Hg above the point at which the radial pulse disappeared. The pressure within the cuff was then released at a rate of approximately 2 mm Hg/s while auscultating with a stethoscope over the brachial artery. The onset of sound (Korotkoff phase I) was indicative of systolic blood pressure, and the disappearance of the sound (Korotkoff phase V) was taken as indicative of diastolic blood pressure.16 Two readings were recorded at an interval of 1 to 2 minutes, and the cuff was completely deflated between the readings. The mean of 2 readings was calculated for final analysis.
Weight and height were recorded for each individual in light clothing without shoes. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared. Pulse rate was measured by noting pulsations of the radial artery at the right wrist in the sitting position. Quality control for the survey and blood pressure measurements included a visit to the field by expert consultants, duplicate examination by field supervisors, calibration protocols, and retraining exercises.15
Urban and rural areas were classified according to the definition used by the Federal Bureau of Statistics, according to which thinly populated, largely agricultural areas (<5000 people) with poor availability of basic amenities (eg, electricity) are considered rural.14 Ethnicity was reported as "mother tongue," which is specific for each of the 5 major ethnic subgroups of Pakistan: Muhajir, Punjabi, Sindhi, Pashtun, and Baluchi. Levels of socioeconomic status were defined through a count of the number of items owned. An index of household item (eg, television, refrigerator, automobile) ownership was constructed by summing up items owned by the household. This methodology has been shown to be particularly useful for measuring health inequalities that result from the direct effects of material conditions and has been validated previously.17,18 Two components of saturated fat intake were defined: (1) intake of ghee (hydrogenated oil/clarified butter), depending on whether or not these were consumed daily, and (2) meat (animal fat) intake, depending on whether or not the meat was consumed at least every other day. High intakes of calcium and potassium were defined as daily consumption of dairy products and fruits, respectively.
High blood pressure in children was defined as systolic or diastolic blood pressure of 95 percentile of age-, sex-, and height-specific levels of blood pressure of the reference US population.8
A family history of hypertension was defined by the presence of hypertension (systolic blood pressure 140 mm Hg or diastolic blood pressure 90 mm Hg based on the mean of 2 readings, or current therapy with antihypertensive medications) in any adult member (15 years old) of the household.
NHANES III (1988–1994)
NHANES III is a nationally representative cross-sectional survey of the population in the United States. Details of its design and conduct have been published previously.13 As in NHSP, blood pressure measurements were obtained in the seated position for children 5 years old or older in a standardized manner with a mercury sphygmomanometer.13 Although 3 readings of blood pressure were recorded, to be consistent with NHSP, a mean of the first 2 readings was calculated for our analysis (http://www.cdc.gov/nchs/about/major/nhanes/nh3data.htm; accessed December 2004). A total of 6980 children 5 to 14 years old were included in NHANES III. Of these, 2224 belonged to the black race and were excluded from this analysis.
Statistical Analysis
Age- and height-percentile–specific systolic and diastolic blood pressure values for South Asian children 5 to 14 years old from NHSP data were plotted on normograms derived for the US population.8 The overall and age-specific prevalence of high blood pressure was computed for South Asian children and compared with the overall prevalence of the same in children in the United States by use of 2 test.
Linear regression analyses were used for the outcomes of systolic and diastolic blood pressure levels to determine the association of ethnicity (United States versus Pakistan) after adjustment for BMI.
To assess the reproducibility of blood pressure readings in the 2 surveys, the mean difference (SEM) between the first and the second readings and the correlation between the 2 were computed.
The associations of systolic and diastolic blood pressure with sociodemographic and clinical characteristics were studied by use of univariate and multivariate analyses in children 5 to 14 years old in the NHSP data. The candidate predictor list included ethnicity; age; sex; BMI; low versus high socioeconomic status; urban versus rural dwelling; consumption of food rich in saturated fats (meat and ghee), potassium (fruits), and calcium (dairy products); and a family history of hypertension and heart rate.
Stepwise linear regression analyses were conducted by use of forward selection with an entry criterion of P<0.1 for the primary outcomes of systolic and diastolic blood pressure. All adjusted associated factors of systolic and diastolic blood pressures were retained in the respective final models. In addition, variables significantly associated with the outcome (P<0.05) in the univariate analyses were forced into the multivariate models. Interactions between age, ethnicity, BMI, and sex with each other and with other variables were tested in the final models. SAS version 8.0 software was used for all analyses.
Results
In the NHSP data, a total of 5641 subjects were 5 to 14 years old: 2974 (52.7%) boys and 2667 (47.3%) girls. Two readings of blood pressure were recorded in 5495 subjects (97.4%): 2926 boys and 2569 girls. Out of these, BMIs were measured in 5374 subjects (97.8%): 2866 boys and 2508 girls.
In NHANES III, a total of 4756 white children were 5 to 14 years old: 2343 (49.3%) boys and 2413 (50.7%) girls. Two readings of blood pressure were recorded in 3420 subjects (71.9%): 1662 boys and 1758 girls. Out of these, BMIs were measured in 3389 subjects (99.1%): 1647 boys and 1742 girls.
Comparison of Blood Pressure in Children in South Asia Versus Those in the United States
The Figure illustrates the comparison among BMI-specific systolic and diastolic blood pressure levels in children 5 to 14 years old surveyed in NHSP and children in NHANES III.13 Among these children, the mean BMI-adjusted systolic blood pressures were 10011 versus 9911 mm Hg (P<0.001.), and diastolic blood pressures (SD) were 6310 versus 5212 mm Hg (P<0.001) in NHSP versus NHANES III, respectively.
BMI-specific blood pressure levels in children in Pakistan vs white children in the United States. Data are on 5374 South Asian children aged 5 to 14 years included in the NHSP (1990–1994) and 3389 white children in the United States included in NHANES III (1988–1994). BMI cutoffs are based on 25th, 50th, 75th, and 95th percentiles of values in NHSP data. P values are based on ANOVA among children in NHSP vs NHANES III.
Comparison of the first with the second blood pressure readings in NHSP and NHANES III revealed a mean difference (SEM) of 0.7 (0.1) versus 0.9 (0.1) mm Hg, respectively, in systolic blood pressure and 0.5 (0.1) and 0.5 (0.2) mm Hg, respectively, in diastolic blood pressure. The correlation coefficient between the 2 readings of systolic blood pressure was r=0.92 and r=0.89, (P<0.001 for each), respectively, and those of diastolic blood pressure were r=0.93 and r=0.76 (P<0.001 and P=0.01), respectively.
Factors Associated With Systolic and Diastolic Blood Pressure Levels in South Asian Children
The residuals from the final model were normally distributed, and there were no detectable patterns of distribution of standardized residuals against predicted values of systolic blood pressure or diastolic blood pressure.
Tests for interactions in the final model revealed significant interaction between age and sex for the outcomes of systolic and diastolic blood pressure (P<0.001 and P=0.03, respectively). The interaction terms suggested that the rise in systolic and diastolic blood pressure with each 1-year increase in age were 1.55 (1.43, 1.68) and 1.12 (1.00, 1.24) mm Hg in boys and 2.09 (1.95, 2.23) and 1.32 (1.18, 1.46) mm Hg in girls.
Discussion
This is the first report of the associates of blood pressure in South Asian children of Pakistan based on a sound nationally representative epidemiological survey. Using blood pressure–normative data in children in the United States as reference, the overall prevalence (95% CI) of high blood pressure in Pakistani children 5 to 14 years old was 12.2% (11.3% to 13.1%): 15.8% (14.5% to 17.1%) in boys and 8.7% (7.6% to 9.8%) in girls.8 The BMI-standardized levels of diastolic blood pressure were significantly higher in South Asian children compared with those in the United States.13
An increased prevalence of childhood cardiovascular risk factors is predictive of increased carotid intimal-medial thickness, which is a determinant of cardiovascular events.19,20 Recent data from the population-based Bogalusa Heart Study and the Cardiovascular Risk in Young Finns Study show that systolic blood pressure elevations beginning in childhood are a consistent predictor of arterial stiffness in young adults.6,19 Numerous studies have highlighted the importance of diastolic blood pressure in children, which has been suggested to be a good predictor of adult hypertension and CVD.21,22 Lowering blood pressure in hypertensive adults slows the progression of arterial stiffness and lowers the risk of CVD.23,24 Thus, institution of measures during childhood for prevention of high blood pressure is essential for optimal risk reduction of CVD.
It is interesting to note that prevalence of high blood pressure is greater among children in Pakistan (12%) compared with the 5% predicted for children in the United States.8 This is despite lower BMIs of Pakistani children.13 The reason for this paradox is unclear but could be attributed to ethnic differences between the 2 populations. Ethnic differences in blood pressure have been reported in other populations as well.1,25,26 Prospective studies are needed to explore the potential relationships between ethnicity and blood pressure.
Furthermore, low birth weight has been shown to be associated with chronic diseases, including diabetes and high blood pressure,27–29 though this notion has been challenged by some.30 Adverse outcomes of pregnancy, including maternal morbidity and mortality, intrauterine growth retardation, and low-birth-weight infants, are much more common in developing countries, especially South Asia, compared with the West.31,32 Whether a greater prevalence of high blood pressure in South Asian children despite lower BMIs is a reflection of lower birth weight remains to be determined.29,33
Our findings also raise the important question of the suitability of criteria for diagnosis of high blood pressure in South Asian children. The Fourth Report on the Diagnosis, Evaluation, and Treatment of High Blood Pressure in Children and Adolescents recommends age-, sex-, and height-specific blood pressure values that are above the 95th percentile of normative systolic and diastolic blood pressure values among the US population as diagnostic of high blood pressure in childhood.8 On the basis of this definition, 5% of children in any given population would be classified as having high blood pressure. Using the 95th percentile for blood pressure recorded among children in the United States as reference, the prevalence of high blood pressure in children in Pakistan was 12.2% (11.3% to 13.1%). Clearly, it cannot be assumed that the threshold blood pressure level for end-organ damage would be higher for South Asian children. Therefore, appropriate reference populations and blood pressure cutoff values for the diagnosis of high blood pressure in children of South Asian as well as other ethnic descent need to be determined.
Our analyses revealed that children residing in urban compared with rural parts of Pakistan have an adjusted systolic pressure that was lower by 1.56 (95% CI, 0.95, 2.18) mm Hg. The same trend has been reported from other developing regions of the world.34 The poorer health facilities and lower literacy status of women in rural versus urban areas lead to a greater proportion of adverse outcomes of pregnancy,35,36 one manifestation of which could be elevated blood pressure during childhood.27–29 The reason for higher blood pressure in rural versus urban children in Pakistan deserves further study.
Obesity during childhood has been reported to be strongly associated with systolic blood pressure in children and in adults.37 We also observed significant relationships between blood pressure and BMI in children. This is despite lower BMIs of children in Pakistan compared with those in the West. Recent evidence suggests that because of differences in body stature, an equally high BMI confers more CVD risks in Asian than in white populations.38,39 Therefore, the recent WHO guidelines for defining obesity suggest lower cutoff values of BMI in the Asian population.40 It is therefore important to develop population-based distribution for computing appropriate age-, sex-, and BMI-specific blood pressure levels for children in this population.
Previously, we reported an independent association between high meat intake (as a proxy for animal fat consumption) and hypertension in Pakistani adults.5 We now report the same association with systolic and diastolic blood pressures in children. In addition, ghee consumption was also positively and independently associated with diastolic blood pressure in children. Ghee contains cholesterol oxides that are thought to be related to atherosclerosis.41 Our finding of an independent association between high saturated fat content in diet and blood pressure are consistent with those of the Bogalusa study in children.42,43
We found significant ethnic differences in levels of systolic and diastolic blood pressures, with Pashtuns, Muhajirs, and Baluchis having significantly higher values than the Punjabis. The variations in these 4 ethnic subgroups are consistent with our findings in the adult population of Pakistan.5 This suggests that these differences are likely to be a result of genetic variations in susceptibility or early exposure to environmental causes of high blood pressure.
Systolic blood pressure levels were significantly higher in boys than in girls in both the US and South Asian populations. Multivariate analysis of data on South Asian children revealed that these differences persisted even after adjustment for sociodemographic factors. This is consistent with our findings in adults.5 The mechanisms responsible for the sex differences in blood pressure levels are not clear, although it is speculated that interactions between sex hormones and the kidneys could play a protective role in premenopausal women.44 The potential role of sex hormones on blood pressure in women needs further study.
Our study has some limitations. First, the differences in protocols and methodologies between the 2 surveys could lead to differences in blood pressure measurements. Still, both the NHANES III and NHSP were designed and conducted under the supervision of NCHS and used similar sampling rationales and techniques for measuring blood pressure and BMI. Second, higher blood pressure levels in NHSP versus NHANES could reflect a "white-coat effect" because of less familiarity of Pakistani children with receiving blood pressure measurement. This is unlikely to explain the entire difference in blood pressure levels between the 2 populations, however, because the white-coat effect tends to affect systolic blood pressure more than diastolic blood pressure, and the differences in the levels of the latter were greater than those in the former. Furthermore, comparison of data after adjustment for pulse rate, which is expected to increase with the white-coat effect, revealed consistent results (data not shown). Third, diastolic blood pressure levels are traditionally more difficult to measure. Therefore, a wider difference in levels of this component of blood pressure between the US and Pakistani children may have several interpretations. These include true findings versus measurement errors. Furthermore, higher correlation between the 2 readings of diastolic blood pressure in NHSP (r=0.93) than in NHANES (r=0.73) could reflect expectation bias on the part of the NHSP research staff, though it is equally likely to be a result of adherence of the latter to the study protocol. Fourth, the blood pressure levels recorded in our study are based on an average of 2 readings at a single visit. A more precise clinical estimate would include measurements from 3 separate occasions. Still, multiple readings of blood pressure from the same day are considered appropriate for epidemiological studies.13 Furthermore, comparative blood pressure levels from the US population reported in this article are also based on an average of 2 readings at a single visit. Moreover, the reproducibility of the second reading of blood pressure compared with the first was good. In addition, our main findings were similar on comparison with data collected on children 8 to 14 years old during NHSP with NHANES 1999 to 2000 (data not shown) and with the average of the last 2 readings of blood pressure obtained during NHANES III. Finally, it is remarkable that despite the lower BMIs of Pakistani children, their blood pressure levels are higher than American children, and even equal levels of blood pressure between the 2 populations would have been noteworthy. Thus, we believe that our findings are robust and alarming.
In the analysis for factors associated with blood pressure in Pakistani children, we did not adjust for all known environmental risk factors for high blood pressure. For instance, information on sodium intake and physical activity was not collected during the NHSP.45 Rural areas of Pakistan have the highest proportion of the labor force employed in the agricultural sector, ie, approximately 63.8%, whereas in the urban areas, it is only 7.6%.46 It is known that child labor in the agricultural sector accounts for >70% of working children globally and in South Asia.47 Hence, physical activity is likely to be greater among rural than urban children. Therefore, it is perhaps surprising that blood pressures were higher among rural children, and an evaluation of causative factors for raised blood pressure in rural areas is required. Finally, the food frequency questionnaire used during NHSP has not been validated. Nevertheless, our findings warrant an in-depth assessment of the potential dietary associations with blood pressure and development of validated dietary questionnaires in the native South Asian population.
In conclusion, this is the first report on levels and associates of blood pressure in a native South Asian sample of nationally representative children of Pakistan. We found that using the blood pressure normograms for children in the United States as reference, the prevalence of high blood pressure in children in Pakistan would be 12.6% (11.5% to 13.7%). This is substantially greater than the 5% predicted prevalence of high blood pressure in children in the United States based on same criteria, despite the lower BMIs of South Asian children.8 The reasons for higher blood pressure levels in South Asian children versus those in the United States need exploration. The adjusted associated factors of high blood pressure in South Asian children identified in our study need immediate attention. Effective ways of identifying South Asian children at high risk of high blood pressure and CVD need to be identified and implemented.
Acknowledgments
This study was supported by grants from Fogarty International Center, National Institutes of Health grant RO3-TWO5657-01A1 (Drs Levey, Jafar, Schmid, and Chaturvedi), and National Institute of Diabetes and Digestive and Kidney Diseases grant RO1-DK53869 (Dr Levey). We thank members of the Pakistan Medical Research Council and the US Department of Health and Human Services for their assistance in acquisition of the NHSP data.
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Mathews R, Reis C, Iacopino V. Child labor: a matter of health and human rights. J Ambul Care Manage. 2003; 26: 181–182(Tazeen H. Jafar, MD, MPH;)
the Section of Nephrology, Department of Medicine (T.H.J.), and the Department of Medicine (M.I.)
Aga Khan University, Karachi, Pakistan; the Division of Nephrology (T.H.J., A.S.L.) and the Division of Clinical Care Research (C.H.S.)
Tufts-New England Medical Center, Department of Medicine, Tufts University School of Medicine School, Boston, Mass
the National Heart and Lung Institute, Imperial College London, UK (N.P., N.C.).
Abstract
Background— Blood pressure during childhood is an established predictor of adult blood pressure, which in turn increases mortality as a result of cardiovascular disease. Adult South Asian populations are particularly predisposed to cardiovascular disease compared with whites, but the prevalence of high blood pressure and determinants of blood pressure in South Asian children have not been explored or compared with those of white children.
Methods and Results— Analyses were performed on 5641 South Asian children 5 to 14 years old included in the nationally representative National Health Survey of Pakistan (NHSP) (1990–1994) and on 4756 white children 5 to 14 years old included in Third National Health and Nutrition Examination Survey (NHANES III) (1988–1994). Anthropometric measurements were obtained. Blood pressure was measured twice in the seated position with a mercury sphygmomanometer and an appropriate-size cuff. High blood pressure was defined as a systolic or diastolic blood pressure level that was 95th percentile of age-, sex-, and height-percentile–specific reference level for the US population. Mean body mass index (BMI)–adjusted blood pressure values were compared among children in 2 data sets by use of linear regression analysis. The overall prevalence (95% CI) of high blood pressure in South Asian children 5 to 14 years old was 12.2% (11.3% to 13.1%): 15.8% (14.5% to 17.1%) in boys and 8.7% (7.6% to 9.8%) in girls. This is in sharp contrast with the predicted 5% prevalence of high blood pressure in children in the United States (P<0.001). The mean BMI-adjusted systolic blood pressure levels (SD) were 100 (11) versus 99 (11) mm Hg (P<0.001), and diastolic blood pressure levels (SD) were 63 (10) versus 52 (12) mm Hg (P<0.001) in NHSP versus NHANES III, respectively.
Conclusions— South Asian children have higher body-mass–adjusted blood pressure levels than white children in the United States. Further studies are needed to determine factors responsible for these differences. Immediate attention is needed to address high blood pressure and its risk factors in native South Asian children.
Key Words: blood pressure ; pediatrics ; epidemiology ; ethnic groups
Introduction
Migrant populations of South Asian origin (India, Pakistan, and Bangladesh) living in the West are at higher risk of cardiovascular disease (CVD) compared with whites,1–3 but the problems of noncommunicable diseases are not limited only to South Asian populations residing in the West. South Asian countries, home to approximately one quarter of the world’s population, are major contributors to the global burden of CVD at present, and this contribution is projected to grow, given their consistent population growth rates.4 Hypertension, the most common risk factor for CVD, has now become a major health problem in Pakistan, affecting 17.9% of all adults 15 years old and 1 in 3 adults 45 years old.5 Thus, prevention of high blood pressure and CVD needs urgent attention in South Asia.
The knowledge that blood pressure during childhood is an established predictor of adult blood pressure, which in turn increases mortality from CVD, clearly underscores the importance of studying childhood blood pressure and the need for establishing preventive measures in early life.6,7 The Fourth Report on the Diagnosis, Evaluation, and Treatment of High Blood Pressure in Children and Adolescents recommends age-, sex-, and height-specific values that are at >95th percentile of normative systolic and diastolic blood pressure values as diagnostic of high blood pressure in childhood.8 Unfortunately, data on age-specific blood pressure levels in children of South Asian origin are scarce. To date, studies of blood pressure in South Asian children have suffered from inadequate sample size or have been restricted to distinct communities.9–12
We therefore used data in South Asian children 5 to 14 years old included in the nationally representative National Health Survey of Pakistan (NHSP) (1990–1994) to determine the prevalence of high blood pressure in children in Pakistan. We also compared blood pressure levels among children 5 to 14 years old included in the NHSP with those surveyed in the United States during the Third National Health and Nutrition Examination Survey (NHANES III), 1988 to 1994.13 In addition, we studied the correlates of systolic and diastolic blood pressure in South Asian children.
Methods
NHSP (1990–1994)
Cross-sectional data were collected during the NHSP over a period of 4 years (1990–1994) by the Pakistan Medical Research Council, under the technical guidance and support of the US National Center for Health Statistics (NCHS).14 The overall design of NHSP was a modification of NHANES III conducted by the NCHS, tailored to the needs of Pakistan. The details of sampling, design, components, survey instrument, and quality control have been reported previously.5,15 Briefly, the survey was conducted on a nationally representative sample of 18 135 individuals 6 months to 110 years old from 2400 urban and rural households after informed consent had been obtained. A 2-stage stratified design was used. The urban and rural areas of each of the 4 provinces of Pakistan were taken as strata. There were 80 urban or rural primary sampling units. A total of 30 households were drawn into the sample from each unit, and all residents of the household were included in the study. The overall individual response rate was 92.6%. The total number of individuals 5 years old was 15 083. Out of these, 5641 subjects were between 5 and 14 years old.
Data on demographic, lifestyle, socioeconomic, and health-related variables were collected by use of a questionnaire validated in local languages. Physicians at mobile examination centers performed a standardized physical examination. Mothers were proxy respondents for children <12 years old. Trained technicians performed anthropometric examinations. Blood pressure was measured by certified physicians in a standardized manner. Blood pressure certification consisted of measurement performance on live volunteers. As in NHANES III, the physician selected one of 5 (infant, child, adult, large adult, and thigh) cuff sizes for blood pressure measurement on the basis of the size of the participant’s arm. Blood pressure was measured in the seated position by use of a mercury sphygmomanometer with the right forearm horizontal on a table. After the appropriate-size cuff for children had been applied (covering approximately two thirds of the upper arm), the cuff was gradually inflated to approximately 20 mm Hg above the point at which the radial pulse disappeared. The pressure within the cuff was then released at a rate of approximately 2 mm Hg/s while auscultating with a stethoscope over the brachial artery. The onset of sound (Korotkoff phase I) was indicative of systolic blood pressure, and the disappearance of the sound (Korotkoff phase V) was taken as indicative of diastolic blood pressure.16 Two readings were recorded at an interval of 1 to 2 minutes, and the cuff was completely deflated between the readings. The mean of 2 readings was calculated for final analysis.
Weight and height were recorded for each individual in light clothing without shoes. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared. Pulse rate was measured by noting pulsations of the radial artery at the right wrist in the sitting position. Quality control for the survey and blood pressure measurements included a visit to the field by expert consultants, duplicate examination by field supervisors, calibration protocols, and retraining exercises.15
Urban and rural areas were classified according to the definition used by the Federal Bureau of Statistics, according to which thinly populated, largely agricultural areas (<5000 people) with poor availability of basic amenities (eg, electricity) are considered rural.14 Ethnicity was reported as "mother tongue," which is specific for each of the 5 major ethnic subgroups of Pakistan: Muhajir, Punjabi, Sindhi, Pashtun, and Baluchi. Levels of socioeconomic status were defined through a count of the number of items owned. An index of household item (eg, television, refrigerator, automobile) ownership was constructed by summing up items owned by the household. This methodology has been shown to be particularly useful for measuring health inequalities that result from the direct effects of material conditions and has been validated previously.17,18 Two components of saturated fat intake were defined: (1) intake of ghee (hydrogenated oil/clarified butter), depending on whether or not these were consumed daily, and (2) meat (animal fat) intake, depending on whether or not the meat was consumed at least every other day. High intakes of calcium and potassium were defined as daily consumption of dairy products and fruits, respectively.
High blood pressure in children was defined as systolic or diastolic blood pressure of 95 percentile of age-, sex-, and height-specific levels of blood pressure of the reference US population.8
A family history of hypertension was defined by the presence of hypertension (systolic blood pressure 140 mm Hg or diastolic blood pressure 90 mm Hg based on the mean of 2 readings, or current therapy with antihypertensive medications) in any adult member (15 years old) of the household.
NHANES III (1988–1994)
NHANES III is a nationally representative cross-sectional survey of the population in the United States. Details of its design and conduct have been published previously.13 As in NHSP, blood pressure measurements were obtained in the seated position for children 5 years old or older in a standardized manner with a mercury sphygmomanometer.13 Although 3 readings of blood pressure were recorded, to be consistent with NHSP, a mean of the first 2 readings was calculated for our analysis (http://www.cdc.gov/nchs/about/major/nhanes/nh3data.htm; accessed December 2004). A total of 6980 children 5 to 14 years old were included in NHANES III. Of these, 2224 belonged to the black race and were excluded from this analysis.
Statistical Analysis
Age- and height-percentile–specific systolic and diastolic blood pressure values for South Asian children 5 to 14 years old from NHSP data were plotted on normograms derived for the US population.8 The overall and age-specific prevalence of high blood pressure was computed for South Asian children and compared with the overall prevalence of the same in children in the United States by use of 2 test.
Linear regression analyses were used for the outcomes of systolic and diastolic blood pressure levels to determine the association of ethnicity (United States versus Pakistan) after adjustment for BMI.
To assess the reproducibility of blood pressure readings in the 2 surveys, the mean difference (SEM) between the first and the second readings and the correlation between the 2 were computed.
The associations of systolic and diastolic blood pressure with sociodemographic and clinical characteristics were studied by use of univariate and multivariate analyses in children 5 to 14 years old in the NHSP data. The candidate predictor list included ethnicity; age; sex; BMI; low versus high socioeconomic status; urban versus rural dwelling; consumption of food rich in saturated fats (meat and ghee), potassium (fruits), and calcium (dairy products); and a family history of hypertension and heart rate.
Stepwise linear regression analyses were conducted by use of forward selection with an entry criterion of P<0.1 for the primary outcomes of systolic and diastolic blood pressure. All adjusted associated factors of systolic and diastolic blood pressures were retained in the respective final models. In addition, variables significantly associated with the outcome (P<0.05) in the univariate analyses were forced into the multivariate models. Interactions between age, ethnicity, BMI, and sex with each other and with other variables were tested in the final models. SAS version 8.0 software was used for all analyses.
Results
In the NHSP data, a total of 5641 subjects were 5 to 14 years old: 2974 (52.7%) boys and 2667 (47.3%) girls. Two readings of blood pressure were recorded in 5495 subjects (97.4%): 2926 boys and 2569 girls. Out of these, BMIs were measured in 5374 subjects (97.8%): 2866 boys and 2508 girls.
In NHANES III, a total of 4756 white children were 5 to 14 years old: 2343 (49.3%) boys and 2413 (50.7%) girls. Two readings of blood pressure were recorded in 3420 subjects (71.9%): 1662 boys and 1758 girls. Out of these, BMIs were measured in 3389 subjects (99.1%): 1647 boys and 1742 girls.
Comparison of Blood Pressure in Children in South Asia Versus Those in the United States
The Figure illustrates the comparison among BMI-specific systolic and diastolic blood pressure levels in children 5 to 14 years old surveyed in NHSP and children in NHANES III.13 Among these children, the mean BMI-adjusted systolic blood pressures were 10011 versus 9911 mm Hg (P<0.001.), and diastolic blood pressures (SD) were 6310 versus 5212 mm Hg (P<0.001) in NHSP versus NHANES III, respectively.
BMI-specific blood pressure levels in children in Pakistan vs white children in the United States. Data are on 5374 South Asian children aged 5 to 14 years included in the NHSP (1990–1994) and 3389 white children in the United States included in NHANES III (1988–1994). BMI cutoffs are based on 25th, 50th, 75th, and 95th percentiles of values in NHSP data. P values are based on ANOVA among children in NHSP vs NHANES III.
Comparison of the first with the second blood pressure readings in NHSP and NHANES III revealed a mean difference (SEM) of 0.7 (0.1) versus 0.9 (0.1) mm Hg, respectively, in systolic blood pressure and 0.5 (0.1) and 0.5 (0.2) mm Hg, respectively, in diastolic blood pressure. The correlation coefficient between the 2 readings of systolic blood pressure was r=0.92 and r=0.89, (P<0.001 for each), respectively, and those of diastolic blood pressure were r=0.93 and r=0.76 (P<0.001 and P=0.01), respectively.
Factors Associated With Systolic and Diastolic Blood Pressure Levels in South Asian Children
The residuals from the final model were normally distributed, and there were no detectable patterns of distribution of standardized residuals against predicted values of systolic blood pressure or diastolic blood pressure.
Tests for interactions in the final model revealed significant interaction between age and sex for the outcomes of systolic and diastolic blood pressure (P<0.001 and P=0.03, respectively). The interaction terms suggested that the rise in systolic and diastolic blood pressure with each 1-year increase in age were 1.55 (1.43, 1.68) and 1.12 (1.00, 1.24) mm Hg in boys and 2.09 (1.95, 2.23) and 1.32 (1.18, 1.46) mm Hg in girls.
Discussion
This is the first report of the associates of blood pressure in South Asian children of Pakistan based on a sound nationally representative epidemiological survey. Using blood pressure–normative data in children in the United States as reference, the overall prevalence (95% CI) of high blood pressure in Pakistani children 5 to 14 years old was 12.2% (11.3% to 13.1%): 15.8% (14.5% to 17.1%) in boys and 8.7% (7.6% to 9.8%) in girls.8 The BMI-standardized levels of diastolic blood pressure were significantly higher in South Asian children compared with those in the United States.13
An increased prevalence of childhood cardiovascular risk factors is predictive of increased carotid intimal-medial thickness, which is a determinant of cardiovascular events.19,20 Recent data from the population-based Bogalusa Heart Study and the Cardiovascular Risk in Young Finns Study show that systolic blood pressure elevations beginning in childhood are a consistent predictor of arterial stiffness in young adults.6,19 Numerous studies have highlighted the importance of diastolic blood pressure in children, which has been suggested to be a good predictor of adult hypertension and CVD.21,22 Lowering blood pressure in hypertensive adults slows the progression of arterial stiffness and lowers the risk of CVD.23,24 Thus, institution of measures during childhood for prevention of high blood pressure is essential for optimal risk reduction of CVD.
It is interesting to note that prevalence of high blood pressure is greater among children in Pakistan (12%) compared with the 5% predicted for children in the United States.8 This is despite lower BMIs of Pakistani children.13 The reason for this paradox is unclear but could be attributed to ethnic differences between the 2 populations. Ethnic differences in blood pressure have been reported in other populations as well.1,25,26 Prospective studies are needed to explore the potential relationships between ethnicity and blood pressure.
Furthermore, low birth weight has been shown to be associated with chronic diseases, including diabetes and high blood pressure,27–29 though this notion has been challenged by some.30 Adverse outcomes of pregnancy, including maternal morbidity and mortality, intrauterine growth retardation, and low-birth-weight infants, are much more common in developing countries, especially South Asia, compared with the West.31,32 Whether a greater prevalence of high blood pressure in South Asian children despite lower BMIs is a reflection of lower birth weight remains to be determined.29,33
Our findings also raise the important question of the suitability of criteria for diagnosis of high blood pressure in South Asian children. The Fourth Report on the Diagnosis, Evaluation, and Treatment of High Blood Pressure in Children and Adolescents recommends age-, sex-, and height-specific blood pressure values that are above the 95th percentile of normative systolic and diastolic blood pressure values among the US population as diagnostic of high blood pressure in childhood.8 On the basis of this definition, 5% of children in any given population would be classified as having high blood pressure. Using the 95th percentile for blood pressure recorded among children in the United States as reference, the prevalence of high blood pressure in children in Pakistan was 12.2% (11.3% to 13.1%). Clearly, it cannot be assumed that the threshold blood pressure level for end-organ damage would be higher for South Asian children. Therefore, appropriate reference populations and blood pressure cutoff values for the diagnosis of high blood pressure in children of South Asian as well as other ethnic descent need to be determined.
Our analyses revealed that children residing in urban compared with rural parts of Pakistan have an adjusted systolic pressure that was lower by 1.56 (95% CI, 0.95, 2.18) mm Hg. The same trend has been reported from other developing regions of the world.34 The poorer health facilities and lower literacy status of women in rural versus urban areas lead to a greater proportion of adverse outcomes of pregnancy,35,36 one manifestation of which could be elevated blood pressure during childhood.27–29 The reason for higher blood pressure in rural versus urban children in Pakistan deserves further study.
Obesity during childhood has been reported to be strongly associated with systolic blood pressure in children and in adults.37 We also observed significant relationships between blood pressure and BMI in children. This is despite lower BMIs of children in Pakistan compared with those in the West. Recent evidence suggests that because of differences in body stature, an equally high BMI confers more CVD risks in Asian than in white populations.38,39 Therefore, the recent WHO guidelines for defining obesity suggest lower cutoff values of BMI in the Asian population.40 It is therefore important to develop population-based distribution for computing appropriate age-, sex-, and BMI-specific blood pressure levels for children in this population.
Previously, we reported an independent association between high meat intake (as a proxy for animal fat consumption) and hypertension in Pakistani adults.5 We now report the same association with systolic and diastolic blood pressures in children. In addition, ghee consumption was also positively and independently associated with diastolic blood pressure in children. Ghee contains cholesterol oxides that are thought to be related to atherosclerosis.41 Our finding of an independent association between high saturated fat content in diet and blood pressure are consistent with those of the Bogalusa study in children.42,43
We found significant ethnic differences in levels of systolic and diastolic blood pressures, with Pashtuns, Muhajirs, and Baluchis having significantly higher values than the Punjabis. The variations in these 4 ethnic subgroups are consistent with our findings in the adult population of Pakistan.5 This suggests that these differences are likely to be a result of genetic variations in susceptibility or early exposure to environmental causes of high blood pressure.
Systolic blood pressure levels were significantly higher in boys than in girls in both the US and South Asian populations. Multivariate analysis of data on South Asian children revealed that these differences persisted even after adjustment for sociodemographic factors. This is consistent with our findings in adults.5 The mechanisms responsible for the sex differences in blood pressure levels are not clear, although it is speculated that interactions between sex hormones and the kidneys could play a protective role in premenopausal women.44 The potential role of sex hormones on blood pressure in women needs further study.
Our study has some limitations. First, the differences in protocols and methodologies between the 2 surveys could lead to differences in blood pressure measurements. Still, both the NHANES III and NHSP were designed and conducted under the supervision of NCHS and used similar sampling rationales and techniques for measuring blood pressure and BMI. Second, higher blood pressure levels in NHSP versus NHANES could reflect a "white-coat effect" because of less familiarity of Pakistani children with receiving blood pressure measurement. This is unlikely to explain the entire difference in blood pressure levels between the 2 populations, however, because the white-coat effect tends to affect systolic blood pressure more than diastolic blood pressure, and the differences in the levels of the latter were greater than those in the former. Furthermore, comparison of data after adjustment for pulse rate, which is expected to increase with the white-coat effect, revealed consistent results (data not shown). Third, diastolic blood pressure levels are traditionally more difficult to measure. Therefore, a wider difference in levels of this component of blood pressure between the US and Pakistani children may have several interpretations. These include true findings versus measurement errors. Furthermore, higher correlation between the 2 readings of diastolic blood pressure in NHSP (r=0.93) than in NHANES (r=0.73) could reflect expectation bias on the part of the NHSP research staff, though it is equally likely to be a result of adherence of the latter to the study protocol. Fourth, the blood pressure levels recorded in our study are based on an average of 2 readings at a single visit. A more precise clinical estimate would include measurements from 3 separate occasions. Still, multiple readings of blood pressure from the same day are considered appropriate for epidemiological studies.13 Furthermore, comparative blood pressure levels from the US population reported in this article are also based on an average of 2 readings at a single visit. Moreover, the reproducibility of the second reading of blood pressure compared with the first was good. In addition, our main findings were similar on comparison with data collected on children 8 to 14 years old during NHSP with NHANES 1999 to 2000 (data not shown) and with the average of the last 2 readings of blood pressure obtained during NHANES III. Finally, it is remarkable that despite the lower BMIs of Pakistani children, their blood pressure levels are higher than American children, and even equal levels of blood pressure between the 2 populations would have been noteworthy. Thus, we believe that our findings are robust and alarming.
In the analysis for factors associated with blood pressure in Pakistani children, we did not adjust for all known environmental risk factors for high blood pressure. For instance, information on sodium intake and physical activity was not collected during the NHSP.45 Rural areas of Pakistan have the highest proportion of the labor force employed in the agricultural sector, ie, approximately 63.8%, whereas in the urban areas, it is only 7.6%.46 It is known that child labor in the agricultural sector accounts for >70% of working children globally and in South Asia.47 Hence, physical activity is likely to be greater among rural than urban children. Therefore, it is perhaps surprising that blood pressures were higher among rural children, and an evaluation of causative factors for raised blood pressure in rural areas is required. Finally, the food frequency questionnaire used during NHSP has not been validated. Nevertheless, our findings warrant an in-depth assessment of the potential dietary associations with blood pressure and development of validated dietary questionnaires in the native South Asian population.
In conclusion, this is the first report on levels and associates of blood pressure in a native South Asian sample of nationally representative children of Pakistan. We found that using the blood pressure normograms for children in the United States as reference, the prevalence of high blood pressure in children in Pakistan would be 12.6% (11.5% to 13.7%). This is substantially greater than the 5% predicted prevalence of high blood pressure in children in the United States based on same criteria, despite the lower BMIs of South Asian children.8 The reasons for higher blood pressure levels in South Asian children versus those in the United States need exploration. The adjusted associated factors of high blood pressure in South Asian children identified in our study need immediate attention. Effective ways of identifying South Asian children at high risk of high blood pressure and CVD need to be identified and implemented.
Acknowledgments
This study was supported by grants from Fogarty International Center, National Institutes of Health grant RO3-TWO5657-01A1 (Drs Levey, Jafar, Schmid, and Chaturvedi), and National Institute of Diabetes and Digestive and Kidney Diseases grant RO1-DK53869 (Dr Levey). We thank members of the Pakistan Medical Research Council and the US Department of Health and Human Services for their assistance in acquisition of the NHSP data.
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