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Micronutrient Deficiencies as Predisposing Factors for Hypertension in Lacto-Vegetarian Indian Adults

Agharkar Research Institute (S.A.C., V.V.A., K.V.T., K.M.P.), H.C., Pune, INDIA
Jehangir Medical Research Institute (U.P.D.), Pune, INDIA

Address reprint requests to: Dr. Shashi A. Chiplonkar, Biometry & Nutrition Group, Agharkar Research Institute, G. G. Agarkar Road, Pune, 411 004, INDIA. E-mail: shashi49{at}indiainfo.com

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Objective: With the increasing knowledge about the antioxidant potential of many micronutrients such as zinc and vitamin C, their roles in oxidative stress related health disorders have been postulated. This study therefore investigated low micronutrient status as a predisposing factor for hypertension in a traditionally lacto-vegetarian population like Indians.

Methods: Micronutrient profile was assessed in 109 hypertensives with age-gender-socio-economic status matched 115 healthy normotensives (30–58 years of age). Food intakes were estimated through a semi-quantitative food frequency questionnaire. Nutrient intakes were then evaluated by previous estimates of cooked foods from our laboratory. Systolic and diastolic blood pressure (SBP, DBP), age, weight, height, waist and hip circumference, occupation, physical activity, smoking habits were recorded. Fasting blood samples were analyzed for hemoglobin, serum level of glucose, triglycerides, total cholesterol, HDL, ceruloplasmin, plasma level of ascorbic acid, folic acid, retinol, erythrocyte glutathione reductase activity coefficient (EGRAC) and erythrocyte membrane zinc.

Results: There were no significant differences between protein, fat intakes of normal and hypertensive individuals, though intakes of men were higher than those of women (p < 0.05). Intakes of omega-6 fatty acids were higher (p = 0.08) and omega-3 fatty acids were lower in hypertensive men than normotensive men (p = 0.04). Gender differences were also significant for micronutrient intakes except vitamin C and ß-carotene. Intakes of potassium, copper, folic acid and vitamin C were significantly lower in hypertensive individuals than in normotenisves. No significant association was found between occupation or activity level and hypertension (p > 0.2) in these subjects. Conditional logistic regression analysis indicated that intakes of vitamin C, folic acid and zinc were associated with 18% (OR = 1.18, 95% CI:1.08, 1.26), 51% (OR = 1.51, 95% CI 0.94, 2.1) higher odds for hypertension, and 3% lower odds for hypertension (OR = 0.97, 95% CI 0.92, 1.01), respectively. Mean plasma vitamin C and folic acid were significantly higher (p < 0.01), and serum ceruloplasmin and erythrocyte membrane zinc were marginally higher (p = 0.07) in normal than hypertensive subjects. In multivariate linear regression analyses, plasma vitamin C, serum ceruloplasmin and erythrocyte membrane zinc were negatively associated with SBP (p = 0.00001) and plasma vitamin C was negatively associated with DBP (p = 0.0001).

Conclusion: Low dietary intakes of vitamin C, folic acid and zinc emerged as the possible risk factors for hypertension. Further, lower levels of plasma vitamin C, erythrocyte membrane zinc and ceruloplasmin were found to be the putative intermediary biomarkers in pathogenesis of hypertension.

Key words: hypertension, micronutrients, zinc, copper, vitamin C, systolic blood pressure, diastolic blood pressure

	INTRODUCTION

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Innate factors of lacto vegetarian diets, viz. high levels of fiber and minerals and reduced fat content, are considered beneficial in maintaining normal blood pressure. The recent trend in India has however been a reverse in dietary habits. Due to increased consumption of fat and reduced intakes of complex carbohydrates and fiber, the risk for non-communicable diseases such as hypertension has increased in these populations [1,2] Increasing intake of fruits, vegetables and cereals in the diet is currently advocated as a measure to control hypertension [3,4]. The DASH (Dietary Approaches to Stop Hypertension) diet, which is rich in vegetables, fruits and low-fat dairy products and reduced sodium intake (below the current recommendation of 100 mmol per day) has been found to lower blood pressure substantially [5]. Most of these studies have been conducted in populations not habituated to eating vegetables as a part of their daily diet. In the vegetarian population of India, daily consumption of vegetables has been a traditional practice. Still the prevalence of hypertension in Indians is increasing [6,7], indicating the existence of different risk factors. Several studies on risk factors of hypertension in Indians have reported demographic, anthropometric, lifestyle factors, blood lipid profile or glucose [8,9]. Linkages of nutritional factors with hypertension have not been well documented. Therefore it remains to be seen which nutrient deficiencies are prevalent in hypertensive lacto-vegetarian Indians. Secondly, the favorable effect of fruits and vegetables on hypertension suggests a possible role of micronutrients and antioxidants available from fruits and vegetables in reducing high blood pressure. It is therefore necessary to study impact of micronutrient status on the risk of high blood pressure in lacto-vegetarians.

Fruits and vegetables are rich sources of antioxidants such as vitamin C and ß-carotene. Several studies have reported the role of vitamin C in reducing high blood pressure [10–12]. Intake of ß-carotene along with intake of total fiber, vitamin A, vitamin C, iron and magnesium has been reported to have an inverse relation with diastolic blood pressure [13]. Short-term oral high-doses of zinc, vitamin C, ß-carotene and alpha-tocopherol have lowered the blood pressure, possibly via increased availability of nitric oxide [14]. Chen et al. examined the relation between serum vitamins A, C and E, -carotene and ß-carotene levels and blood pressure among men and women (20 years of age) in the US population indicating that antioxidant vitamins may be important in the underlying cause and prevention of hypertension. However, further studies in establishing linkages of antioxidant vitamins and minerals with hypertension are warranted [15]. The role of antioxidant vitamins as preventive measures in reducing risk of cardiovascular disease is still an unproven hypothesis [16]. Levels of vitamin B12 and folic acid are also likely to influence blood pressure indirectly through involvement of homocysteine [17]. Linkages of B12 and folic acid deficiencies also need to be examined in relation to hypertension in lacto-vegetarians.

Antioxidant minerals like zinc and selenium have been studied for their role in hypertension. It was shown that high dietary intakes of Ca or Zn were related to a higher rate of hypertension, and at a low level of dietary intake of magnesium or copper the prevalence of hypertension was seen 1.8 to 2 times more often than at a high level of intake of these micronutrients [18]. Altered plasma status of copper, zinc, magnesium and calcium in hypertension has also been reported [19,20]. Yet major research is directed towards effects of electrolytes such as sodium, magnesium and potassium on blood pressure regulation. Non-electrolytic minerals such as zinc, copper, along with vitamins and their interactive effects need further studies to understand their importance in hypertension.

Multivariate analysis is the best approach to understand the role of several micronutrients simultaneously. However, dietary intakes of nutrients are highly correlated with each other resulting in collinearity of variables under consideration [21]. To assess their relative contribution along with the extent of their positive/negative impact on blood pressure demands special statistical considerations in data analysis. With this view the present study reports data on 109 hypertensive subjects with 115 age-gender matched normotensive individuals from a cross sectional survey with an aim to analyze the influence of 1) dietary intakes and 2) biochemical indices of vitamin C, folic acid, retinol, riboflavin, copper, zinc, glucose, triglycerides, total and HDL cholesterol on blood pressure.

	METHODS

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Subjects
This cross-sectional study was conducted in a traditionally vegetarian population but one consuming milk and milk products. The situation in many parts of India is that the majority of individuals are vegetarians or lacto-vegetarians consuming cereals, legumes, vegetables and milk or milk products in their daily diets. Health surveys on this free-living population were undertaken through private hospitals, clinics and health camps in rural and urban communities in and around Pune city, Maharashtra, India. A total of 614 individuals (263 women and 351 men) participated in the study voluntarily and gave informed written consent. Of these, 122 subjects (89 men and 33 women, 30–58 years of age) were reported to have high blood pressure (diastolic blood pressure of 90 mmHg or higher or systolic blood pressure of 140 mmHg or higher), while 350 were found to have normal blood pressure and no health complaints. From these apparently healthy subjects, a random sample of 122 age-gender matched subjects was selected from the same socioeconomic group from the rural and urban communities. The overall percentage of smokers in the study population was around 6%, with a higher number of smokers in the hypertensive group. The intensity of smoking was ranging from occasional to two cigarettes per day. The sample size of smokers was not sufficient to perform separate analysis. Alcohol consumption was rare in the study population. However, to avoid confounding effects, if any, all these subjects were omitted from the final analysis. The characteristics of the remaining 115 normal and 109 hypertensive subjects have been given in Table 1.

Biochemical Analyses
Fasting venous blood (10 mL) was collected for each subject (not more than 12 hours fasting). Laboratory estimations of plasma retinol, ascorbic acid, folic acid, erythrocyte glutathione reductase activity coefficient (EGRAC), serum ceruloplasmin were done as per NIN manual [24] and erythrocyte membrane zinc as per Ruz et al. [25].

Blood Pressure and Body Measurement
Blood pressure was recorded by a medical doctor at the time of clinical examination in the morning in supine position. Weight, height, waist and hip circumferences were also recorded.

Physical Activity and Occupation
Occupation of each individual was recorded along with the pattern of habitual physical activity through a structured questionnaire. Information about duration in minutes of major daily activities like sleep, sitting, standing, walking, exercise, recreation and occupational activity were used to classify an individual into activity groups: sedentary, light, moderate and heavy.

Statistical Methods
All statistical analyses were performed using SPSS Version 10.0.1 for Windows. Descriptive statistics were computed to characterize the men and women in the normal and hypertensive groups. Gender differences were tested using ANOVA. The characteristics of the subjects were analyzed for main effects of hypertension and gender and any interactions using a two-way ANOVA (blood pressure at two levels by gender at two levels). Association of occupation and physical activity level were tested by chi square test and found to be non significant (p = 0.215 and p = 0.412 respectively). The distributions of nutrient intakes and biochemical indicators were normalized by suitable transformations. For vitamin C, ß-carotene and iron intake, natural logarithmic transformation was done. Correlations between age and both SBP as well as DBP were statistically significant (r = 0.47, r = 0.40, p < 0.01 respectively). So also were the correlations of SBP and DBP with weight of the order of 0.42 (p < 0.01) and with BMI 0.32 (p < 0.01). It was found that adjusting for weight or BMI produced similar results, but correlation of weight was higher than BMI. Hence all the statistical analyses were performed after controlling for age and weight. Partial correlations were computed to examine associations between various micronutrient status variables and blood pressure. Differences between nutrient intakes amongst normal and hypertensive groups were tested using generalized linear models (GLM) univariate procedure with gender and hypertension as factors. The sources of various nutrients are the same foods; hence, bivariate correlation analysis has a limited use in understanding the relative importance of nutrients in hypertension. Therefore forward conditional logistic regression analysis was performed using all the nutrients’ intake simultaneously to estimate odds ratios for nutrient intakes and predict the risk of hypertension.

The natural logarithmic transformation for serum vitamin C, square root transformation for ceruloplasmin, folic acid, riboflavin (EGRAC), and exponential transformation for erythrocyte membrane zinc were performed to make the variables normal to enter regression analysis. Multivariate linear regression model and conditional logistic regression analyses were used to examine simultaneously the effect of blood levels of copper, zinc, riboflavin, folic acid, retinol, and ascorbic acid on the blood pressure after adjusting for age and weight. Multiple regression model giving adjusted R², the coefficient of multiple determination adjusted by dividing the error sum of squares and total sums of square by their respective degrees of freedom, has been used.

	RESULTS

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Percent prevalence of hypertension was higher in the men (25.4%) than in women (12.5%) in the study population. Weight and BMI showed significant differences between normal and hypertensive groups and weight showed significant gender difference (Table 1, p < 0.01). There were no significant differences between macronutrients intakes or dietary fiber and phytate intakes amongst normal and hypertensive groups, though intakes of men were higher than those of women (p < 0.05). Intakes of PUFA, MUFA, -6 and -3 fatty acids differed significantly only between hypertensive and normal men. However, gender differences were significant for all these parameters.

Occupation of the majority of the subjects was office work, while 12.5% to 18% subjects were laborers. Around 70% of the subjects had a sedentary level of physical activity while 8% to 12.9% were agricultural laborers (Table 2). Although the percent of subjects under sedentary and light activity was higher in the hypertensive groups than normal, no significant association was found between occupation or activity level and hypertension (p = 0.2).

with adjusted R² = 0.64, and level of significance p = 0.00001

with adjusted R² = 0.32 and the level of significance, p = 0.0001.

In the conditional logistic regression model, ln(plasma vitamin C) remains as the only risk predictor with 1.56 times higher odds against having hypertension (OR = 1.56, 95% CI: 1.02, 2.11).

	DISCUSSION

 
Prevalence of hypertension in Indians is showing alarmingly steep rise due to rapid changes in diet and lifestyle [1,2]. Differences in dietary exposures may be the result of traditional diets or the modern food industry, which heavily influences the food supply of urban populations. For example, trans fatty acids compose over 50% of the partially hydrogenated "vegetable ghee" widely used in Asian countries, which generally exceeds levels in current western foods [26]. Moreover, lower prevalence of CHD in Indian men consuming higher amounts of ghee (clarified butter) has been reported [27]. With changing life patterns, it is necessary to examine causes of hypertension so as to suggest strategies for prevention and control of high blood pressure.

Considerable evidence is available from epidemiological observations, intervention trials and studies on experimental animals showing the influence of various dietary components on blood pressure. Most of these studies have been carried out on non-vegetarian populations. There are some studies dealing with vegans or lacto-ovo-vegetarians [28] or meat eaters, fish eaters, vegetarians and vegans [29] reporting lower prevalence of hypertension in vegetarians than non-vegetarians. However, vegetarianism in India is different from that reported in these studies. Vegetables are consumed by Indians as an essential part of daily meals with whole unprocessed cereals as staples. The majority of vegetables are used in cooked form and not as raw salads, thus causing vitamin loss. Secondly, consumption of sweets and fried foods is frequent due to the number of festive and cultural events. The effect of BMI, central obesity and dietary fat intake on high blood pressure in Indians has been discussed [6–9]. However, information on nutritional biomarkers in hypertension is scanty. Therefore, in a traditionally lacto-vegetarian population like Indians, it was important to explore and identify specific nutritional factors posing risk for development of hypertension.

BMI to be greater than 25 kg/m² is considered as the cut off for risk of health problems and recent studies also stress the need to lower this cutoff to 23 kg/m² in the case of Indians [30,31]. There were 59.3% hypertensives in our data with BMI <25 indicating a lower threshold for this index. The % prevalence of hypertension was seen to be two times higher in men (25.4%) than in women (12.5%). Further, considering cut-off values of WHR for Indian men (0.88) and women (0.81) [31] prevalences in our data were 62% and 89% in hypertensive group indicating central obesity as the determinant rather than BMI for women.

Though lower protein intakes have been associated with low DBP [32], our data did not support this finding. Vegetable proteins are reported to reduce serum lipids [33]. Absence of association between protein intake and hypertension in our data may be due to the fact that major source of protein was from cereals and legumes.

As compared to the omnivorous diet, the vegetarian diet contains less cholesterol, less saturated fatty acids, more monounsaturated fatty acids and polyunsaturated fatty acids, with a high ratio of polyunsaturated to saturated fatty acids. In general, fat intakes of our subjects were high, higher than the RDA for Indians [23]. However the source of fat was not meat or fish but vegetable oil or milk. Fat intake per se did not show significant impact on hypertension. Further analysis suggested lower intakes of 3 fatty acids but higher intakes of 6 fatty acids in hypertensive subjects, highlighting their differential roles.

Dietary intakes of potassium and magnesium [34] have been reported to have favorable effects on blood pressure in Indians. Our hypertensive subjects showed lower potassium intakes, though it did not enter the regression model. High salt intake is known to be a major risk factor in hypertension. Elliott et al. have reported strong, positive association of urinary sodium with systolic pressure of individuals [35]. Our data did not show a significant difference between salt intakes of normal and hypertensive subjects. This may be because of the reduced salt in the diet strictly followed by the hypertensives. Secondly, food habits of Indians are such that processed and salted food items are rarely consumed even by normotensives.

Our results of conditional logistic regression analysis indicated that dietary intakes of vitamin C, folic acid and zinc were associated with risk of hypertension. Mean plasma levels of vitamin C, folic acid, serum ceruloplasmin and erythrocyte membrane zinc were significantly lower in hypertensive group than normal groups. Further multiple regression analysis of our biochemical data supports the view that vitamin C is involved in the control of both systolic and diastolic blood pressure but adds zinc and copper as important factors in control of systolic blood pressure.

In the randomized double-blind crossover design placebo-controlled study on 21 hypertensives and 17 normotensives, a high dose supplementation of zinc and vitamin C along with alpha-tocopherol and beta-carotene for eight weeks resulted in a fall of SBP in both hypertensives as well as normotensives [14]. Negative correlation of plasma vitamin C and SBP and DBP has been well-documented [10–12]. Vitamin C may be an important component of the effectiveness of fruits and vegetables in the reduction in blood pressure, and tissue ascorbic acid levels may be important in the maintenance of low blood pressure. Long-term intervention studies are warranted to support this hypothesis [36].

Main food items contributing to vitamin C intake are citrus fruits and vegetables. Higher intakes of non-sweet fruits have been found to increase levels of plasma vitamin C in healthy adults of Indian vegetarian origin [22]. The present data also indicated higher consumption of sweet fruits like banana by the hypertensive group. This might be one of the reasons for the lower plasma vitamin C levels of hypertensives. Our results, though based on cross sectional data, suggest that lower dietary intake of this antioxidant micronutrient might be accelerating the genesis of hypertension. Our findings on plasma vitamin C further emphasize the role of vitamin C as a protective agent against high blood pressure in lacto-vegetarian populations. Further prospective studies are essential to establish the risk of long-term vitamin C deficiency on blood pressure.

Hypertensive men and women in our study had lower folic acid intakes than their normal counterparts. Dietary folic acid intake was found to be negatively associated with risk of hypertension. A similar observation was reported in a study on adolescents at risk for high blood pressure [17] wherein mean DBP was found to be significantly higher in the low folate vs. the high folate group (p = 0.008). Serum concentrations of folate and vitamin B-12 were associated with reduced serum homocysteine in persons at high risk of cardiovascular disease in a study on 491 adults from 10 medical research centers in the United States and Canada with hypertension, dyslipidemia, type 2 diabetes, or a combination thereof [37]. This suggests a possible role for folic acid in lowering blood pressure. Direct evidence of low plasma folic acid concentrations in our data has implications for undertaking supplementation trials of micronutrients including folic acid as an adjunct to anti-hypertensive therapy.

Zinc intakes of the study group were lower than the RDA for Indians. Further the average zinc intakes were lower in the hypertensive group than in normal individuals. Erythrocyte membrane zinc has been considered a more sensitive parameter of zinc status than the erythrocyte zinc [25]. Moreover plasma zinc gets affected by factors not related to zinc metabolism. Erythrocyte membrane zinc was found to be associated with hypertension in our data. Zinc, as assessed by serum or erythrocyte or urinary zinc levels, was reported to play a role in pathogenesis of essential hypertension [20,38]. Zinc may also act as an important antioxidant defense factor. A zinc deficiency state may deteriorate taste function leading to an unwitting increase in the salt intake. This might aggravate the situation in turn predisposing the individual to hypertension. Serum ceruloplasmin has emerged as a significant factor negatively associated with hypertension in our data. Negative association of serum ceruloplasmin with hypertension was also stated by Engstrom et al. about healthy men followed 15 years for hypertension [39]. These findings highlight the importance of zinc and copper as the non-electrolyte micronutrients in control of hypertension.

	CONCLUSION

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Major findings of our study are the emergence of micronutrients and antioxidants, viz., vitamin C, zinc, copper and folic acid, as important nutritional factors in the pathogenesis of hypertension in lacto-vegetarians. Further clinical trials can be formulated in view of these results. Prospective clinical trials on vitamin C supplementation have been done [3,4] as also on supplementation with zinc [14]. However, trials of vitamin C, zinc along with copper and folic acid may be worthwhile in lacto-vegetarians.

	ACKNOWLEDGMENTS

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The major part of the work was funded by Department of Science and Technology, New Delhi, India (Project No: SP/SO/B39/94). Part of the data were collected under a project funded by Indian Council of Medical Research, New Delhi. The authors also thank Director, Agharkar Research Institute, for extending necessary facilities to carry out the work.

Received March 1, 2003. Accepted September 16, 2003.

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TOP ABSTRACT INTRODUCTION METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 

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