Arterial Stiffness. Effects of Hunter-Gatherer Subsistence Mode on Arterial Distensibility in Cameroonian Pygmies

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1 Arterial Stiffness Effects of Hunter-Gatherer Subsistence Mode on Arterial Distensibility in Cameroonian Pygmies Daniel Lemogoum, William Ngatchou, Christophe Janssen, Marc Leeman, Luc Van Bortel, Pierre Boutouyrie, Jean Paul Degaute, Philippe Van de Borne See Editorial Commentary, pp 3 5 Abstract We aimed to assess whether arterial distensibility estimated by pulse wave velocity (PWV) and augmentation index (AI) differs between Cameroon traditional pygmies (TPs) on hunter-gather subsistence mode, contemporary pygmies who migrated to semiurban area, and the Bantou farmers (BFs) sharing the same environment. For that purpose, we recorded carotid-femoral PWV (ComplioR) in age and sex carefully matched 20 TPs, 20 contemporary pygmies, and 22 BFs. Aortic AI corrected for heart rate and blood pressures were generated from pressure wave analysis (SphygmoCor). Lipid profile was determined in TP and BF participants. TPs were shorter (P 0.02) with lower body weight (P 0.01) in comparison with contemporary pygmies and BFs. TPs had lower low-density lipoprotein cholesterol but higher high-density lipoprotein cholesterol than BFs (P 0.01). Their PWV ( m/s) was slower (P 0.006) than that of contemporary pygmies ( m/s) or BFs ( m/s); however, after its adjustment for age, mean arterial pressure, and heart rate, the difference was slightly attenuated (P 0.051). PWV adjusted for weight did not differ between groups (P 0.10). In the whole study population but not in TPs taken separately, multivariate regression analysis revealed that PWV was independently associated with mean arterial pressure, age, and TP status (P 0.001), whereas age, mean arterial pressure, and height emerged as independent determinants of aortic AI corrected for heart rate (P 0.001). Aortic AI corrected for heart rate did not differ in the 3 groups. In conclusion, hunter-gather lifestyle is associated with low atherosclerosis risk translated by lower aortic stiffness attributed at least partly to low weight and blunted effects of aging and blood pressures on TP arterial structure and function. (Hypertension. 2012;60: ) Online Data Supplement Key Words: arterial stiffness pulse wave velocity augmentation index atherosclerosis lifestyle pygmies bantou Evidence indicates an increase burden of cardiovascular diseases (CVDs) in Sub-Saharan Africa, especially among black Africans ancestry. 1 3 CVDs have been reported to be more frequent and severe in blacks. 3,4 The underlying mechanisms remain unclear. The contributing role of genetics 4 and lifestyle 3,5 has been evoked. Although the genetic patterns remain poorly explored, available evidence points out the contributing role of changing living conditions and dietary patterns. 5,6 The influence of lifestyle on the global burden of CVD has been well established, 6,7 as well as the impact of dietary intervention on the reduction of cardiovascular (CV) risk. 8 In Sub-Saharan Africa, hunter-gatherers have begun to shift toward an agriculture-based lifestyle over the last 5000 years. Only a few populations still base their mode of subsistence on hunting and gathering. The Pygmies are considered to be the largest group of mobile hunter-gatherers of Africa. They dwell in equatorial forests and are characterized by their short mean stature. However, little is known about their CV status. Few available studies indicated that, in Sub-Saharan Africa, communities like the Kalahari Bushmen and traditional pygmies (TPs) living with ancient lifestyle are relatively free of CVD, 9 11 partly attributed either to low level of blood pressure (BP) 9,10 and to their hunter-gatherer subsistence mode The common characteristics of those populations with low CVD risk are good physical aerobic fitness conditions, which resulted in low body fat and low prevalence of obesity, low cholesterol level, low-salt Received November 14, 2011; first decision December 7, 2011; revision accepted April 12, From the Hypertension Clinic (D.L., W.N., C.J., M.L., L.V.B., P.B., J.P.D., P.V.d.B.), Department of Cardiology, Université Libre de Bruxelles-Erasme Hospital, Brussels, Belgium. Heymans Institute of Pharmacology (L.V.B.), Gend University, Gend, Belgium. Department of Pharmacology (P.B.), Hôpital Européen Georges Pompidou, Paris, France. The online-only Data Supplement is available with this article at /-/DC1. Correspondence to Daniel Lemogoum, Hypertension Clinic, Department of Cardiology, Université Libre de Bruxelles-Erasme Hospital, 808, Lennik Rd 1070, Brussels, Belgium. Daniel.lemogoum@ereasme.ulb.ac.be 2012 American Heart Association, Inc. Hypertension is available at DOI: /HYPERTENSIONAHA

2 124 Hypertension July 2012 Table 1. Comparison of Demographic and Cardiovascular Variables Between the Groups Variables BF (N 22) CP (N 20) TP (N 20) P Values Age, y Sex male /female 8/14 7/5 10/ Height, cm * Weight, kg * BMI, kg/m * Brachial SBP, mm Hg Brachial DBP, mm Hg MAP, mm Hg HR, bpm AIx,% AP, mm Hg Aortic transit time, ms Aortic SBP, mm Hg Aortic DBP, mm Hg Aortic PP, mm Hg PWV, m/s * PWV corrected for MAP, age and HR, m/s Total cholesterol, mg/dl LDL cholesterol, mg/dl * HDL cholesterol, mg/dl * Triglycerides, mg/dl Data are mean SEM. BF indicates Bantou farmer; CP, contemporary pygmies; TP, traditional pygmies; BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; MAP, mean arterial pressure; PP, pulse pressure; HR, heart rate; AP, augmentation pressure corrected for HR; AIx, augmentation index corrected for HR; PWV, pulse wave velocity; LDL, low-density lipoprotein; HDL, high-density lipoprotein. *P 0.05 vs the Bantou farmers. P 0.05 as compared with CP. diet, high fruit and vegetable consumption, less stress, and the absence of a rise in BP with aging Whether the relative low CVD risk in hunting-gathering TPs is accompanied by preserved arterial distensibility has not yet been explored. Arterial stiffness is an important index of arterial distensibility and is increased when elastic properties of the arterial wall are reduced. 13,14 Increased arterial stiffness is associated with atherosclerosis. 14,15 Aortic pulse wave velocity (PWV) is a direct measure of arterial stiffness and is an independent determinant of CV morbidity and mortality. 14,15 Aortic augmentation index (AI), derived from aortic pressure waveforms, provides additional information concerning wave reflections. AI 16,17 is a predictor of CV outcomes. Arterial stiffness indices are BP dependent, 18 and a BP decrease could be followed by a parallel decrease of stiffness. 17 Because BP is a major determinant of arterial stiffness and lifestyle may also be associated with elasticity, we tested the hypothesis that environmental factors could overcome genetic factors with a direct influence on arterial distensibility that will be translated by more distensible arteries in TPs living in forest environment as compared with that of Bantou farmers (BFs) and of their contemporary pygmy (CP) neighbors, both living in a semiurban environment. Moreover, and because AI is influenced by stature, 19 we anticipated that TP short stature is accompanied by early wave reflections, which will be comparable with those of BFs and CPs. Materials and Methods Population Characteristics The present study took place in Socapalm (Cameroon industrial plantation of palm grove) medical center in Kienke located 15 km from the city of Kribi, situated in the equatorial rainforest of southern Cameroon. A total of 62 subjects aged 20 years were enrolled in the study composed of 20 TPs carefully matched for age and sex to 20 CPs and 22 BFs (Table 1). The study protocol was approved by the Erasme Hospital and the Cameroonian national ethic committees. Participation in the study was voluntary, and informed consent was obtained from each participant. All of the examinations were performed in the morning between 8:30 AM and 12:00 AM to limit daily variability in CV parameters. For more details of study operational procedure, please see the online-only Data Supplement. Study Populations and Their Ecological Setting Traditional Pygmies These populations are still classic hunter-gatherers living in the forest of south Cameroon. Their traditional lifestyle is to move frequently through dense forests, living in huts built temporarily with structures of bamboo sticks thatched with banana leaves and moving regularly from one camp to another. Their physical activity is considerable. Their basic nutrition consists of complex carbohydrates, plantain, and cassava; fruits, especially bananas and bush mangos, used in varying proportions; and vegetables and bushmeat. River and well water, used for drinking, is of moderate quality. They drink palm wine and have limited contact with the Bantou population. Nevertheless, whenever possible, they exchange part of their hunt for some salt, palm oil, knives, weapons, and bullets.

3 Lemogoum et al Lifestyle and Arterial Stiffness in Pygmies 125 Contemporary Pygmies The CPs involved in the present study live in community of 70 to 100 individuals in Kienke. They were the second generation of migrated pygmies and have long history of exchange bushmeat with their farming Bantou neighbors for staple foods and manufactured goods. Beyond their traditional nutrition habits that are comparable to those of TPs, they also regularly consume salt obtained from Bantus. They frequently smoke cigarettes and drink heavy alcohol named kitoko (with alcohol content of 40% volume) and palm wine. They have access to modern health care, education, and markets. They remain more sedentary because of socioeconomic dependence on neighboring farmers and are less physically active. Some of them are still hunting, others began agriculture, and a marginal part of them are working as seasonal farmers in industrial oil palm plantations. For the BF ecological setting, please see the online-only Data Supplement. Experimental Measurements Anthropometric Measurements and Biochemical Samples All of the participants underwent clinical examination and bioclinic measurements, including BP, heart rate (HR), weight, and height. The weight was measured with electronic medical scales (Seca). Height was measured with fixed stadiometers (Seca). The body mass index (BMI) was calculated as weight in kilograms divided by height squared in meters (kilograms per meter squared). Only people aged 20 years were included in the study. Pygmies and Bantou ages were recorded and double checked using their national identity cards and birth registry provided by local municipal and health authorities. Determination of Serum Lipid Levels Fasting serum lipid levels were determined in the TP and BF study participants and were obtained within 2 hours after blood withdrawal and immediately frozen at 20 C. Because of local ritual constraints, we could not collect blood in the CP group. The determination of lipid profile was performed at the Erasme Hospital Central Laboratory. Hemodynamic Measurements All of the hemodynamic measurements were performed after 15 minutes of supine rest in a quiet room and in the standardized conditions, as described previously. 20 All of the measurements were performed by the same investigator (D.L.) in triplicate and averaged for analysis. Brachial BPs and HR Brachial systolic and diastolic BPs and HR were recorded in the supine position at the right arm using an automated sphygmomanometer (HEM-705 CP, Omron Corporation, Tokyo, Japan). Pulse pressure (PP) was calculated as systolic minus diastolic BP and mean arterial pressure (MAP) as diastolic plus one-third of PP. Carotid-Femoral PWV PWV was generated by a validated 21 noninvasive device (ComplioR, Artech Medical), which performs pressure wave recordings and calculates automatically the PWV as described previously. 20 In our hands (D.L.), the mean SD intraobserver repeatability of aortic PWV measurements with ComplioR device expressed as coefficient of variation was % (n 30). Aortic Augmentation Index Corrected for HR and BP Aortic augmentation index corrected for HR (AIx), BP, and transit time were obtained from noninvasive pulse wave analysis by the means of radial applanation tonometry calibrated by the brachial BP (SphygmoCor version 6.1 software, Atcor Medical Pty Ltd, West Ryde, New South Wales, Australia), as described previously. 20 The reproducibility of derived AIx has been validated previously. 22,23 In our hands (D.L.), the mean SD intraobserver within session coefficient of variation for derived AI measures using SphygmoCor was % (n 30). Statistical Analysis Results are expressed as mean SEM. Statistical analysis was performed with the program SPSS version The comparison among the 3 groups (BF, CP, and TP) was made using 1-way ANOVA except for the lipid profile, for which a paired Student t test was performed. Post hoc tests were performed using a Bonferroni correction for multiple comparisons when 1-way ANOVA was significant. Correlations were made among the PWV, AIx, and the different variables using the Pearson correlation coefficient. All of the correlations were bilateral tests. A multiple regression analysis was performed to assess the independent determinant of the PWV and AIx. All of the relevant variables that correlated with PWV and AIx (P 0.01) were included in that model. Significance was assumed for P Results Comparison of Anthropometric, Hemodynamic, and Biological Variables Between the 3 Study Populations TPs were shorter (P 0.02) and had lower weight and BMI as compared with CPs and BFs (P 0.01; Table 1). Brachial systolic BP (SBP), MAP, diastolic BP (DBP), and HR, as well as aortic SBP, DBP, and PP, were comparable between the 3 groups (all P 0.05). AIx did not differ in the 3 groups. TPs exhibited markedly slower aortic PWV as compared with CPs and BFs (P 0.006); however, after adjustment of PWV for age, MAP, and heart rate, the difference was slightly attenuated and just failed to achieve formal statistic significance (0.051). PWV adjusted for weight did not differ among the 3 groups (P 0.10). Low-density lipoprotein cholesterol was lower and high-density lipoprotein cholesterol higher in TPs as compared with BFs (P 0.01), suggesting a low risk for atherosclerosis in the TP group. Relation Between PWV and AIx and CV Variables in the Different Study Groups In the whole study population (Table S1, available in the online-only Data Supplement), we observed a positive relation between PWV and age, weight, BMI, MAP, aortic SBP, and PP, as well as with AIx. The TP status was negatively correlated with PWV. AIx was linked with age, height, weight, brachial DBP, and MAP, as well as aortic SBP and DBP. In the TP group (Table S2), PWV was not correlated with any of the measured variables. However, AIx was negatively correlated with weight and transit time. In the CPs (Table S3) and BFs (Table S4), PWV was related to age, brachial SBP, MAP, aortic PP, and AP. In the BF group, a correlation between PWV and DBP, AIx, and high-density lipoprotein cholesterol was also found. Moreover, AIx was also linked with height, weight, brachial SBP and DBP, and PWV in the BF group. AIx was correlated with age and MAP in both CP and BF groups. Determinants of the PWV Multiple regression analysis in the whole study population revealed MAP, age, and TP status as independent determinants of the PWV, accounting for 38% of variability of the PWV in our study population (Table 2). In the BF group, age and MAP emerged as independent predictors of PWV, accounting for 47% of its variability; whereas in the CP

4 PWV (m/s) 126 Hypertension July 2012 Table 2. Determinants of Aortic PWV in Multiple Regression Models PWV P Value Whole study cohort Constant MAP, mm Hg Age, y Pygmies status (yes 1, no 0) Bantou farmer group Constant Age, y MAP, mm Hg Contemporary pygmies group Constant MAP, mm Hg PWV indicates pulse wave velocity; MAP, mean arterial pressure. The whole study cohort included variables are weight, MAP, age. and pygmies status (R ; P 0.001). Bantou farmer group included variables are aortic augmentation index corrected for heart rate, MAP, aortic pulse pressure, and age (R ; P 0.001). Contemporary pygmies group included variables are MAP, aortic pulse pressure, and age (R ; P 0.007). group, only MAP appeared as independent determinant of PWV, explaining 58% of its variability. Determinants of the AIx Multiple regression analysis showed that height, MAP, and age are independent predictors of the AIx in the whole study population, accounting for 50% of the changes in AIx (Table 3). In the TP group, transit time was negatively and independently associated with AIx, explaining 81% of its variability, whereas in CPs, MAP appeared as an independent determinant of AIx (P 0.01). Age, MAP, weight, and heart rate emerged as independent determinants of AIx in BF (P 0.001). Effects of Aging on the PWV, BP, and AIx Aging is accompanied by a rise in brachial and aortic SBP, brachial DBP, AIx, and PWV in the BF and CP groups. However, aging had no effect on these parameters in the TP group (Figure and Figure S1, S2, S3, S4, and S5). Discussion This study illustrates for the first time a lower aortic stiffness in pygmies living in the Cameroon forest, as well as a negative association between PWV and TP status. Furthermore, and despite a slower PWV, wave reflections determined by aortic AIx are similar in TPs, CPs, and BFs. Globally, CPs seem to be phenotypically much more close to BFs than to TPs despite similar genetic background with the latter. We are not aware of another study exploring aortic stiffness and pressure wave reflections in pygmy communities in Africa. PWV in Pygmies Increased arterial stiffness has been reported in both normotensive and hypertensive blacks. 24 This was the case for CP and BF study participant groups, contrasting with TP participants in whom PWV was markedly slower, suggesting less stiffness along their arterial tree. Table 3. Determinants of AIx in Multiple Regression Model AIx P Value Whole study cohort Constant Height, cm MAP, mm Hg Age, y Bantou farmer group Constant Weight, kg MAP, mm Hg Age, y HR, bpm Contemporary pygmies groups Constant MAP, mm Hg Age, y Traditional pygmies Constant Central transit time AIx indicates augmentation index corrected for heart rate; MAP, mean arterial pressure; HR, heart rate. Whole study cohort included variables are height, weight, MAP, and age (R ; P 0.001). Bantou farmer group included variables are height, weight, MAP, heart rate, and age (R ; P 0.001). Contemporary pygmies groups included variables are MAP and age (R ; P 0.01). Traditional pygmies included variables are height, weight, central transit time, and age (R ; P 0.001). It seems likely that hunter-gatherer subsistence mode illustrated by low weight, low BMI, low low-density lipoprotein cholesterol, and high level of high-density lipoprotein cholesterol, together with previously reported low-salt diet, 9 11 have contributed to improve aortic elasticity in TPs. In keeping with our observation, weight appeared in this study as a major confounder of lower PWV in TPs. Beyond the impact of low weight and BMI on aortic PWV in TPs, high high-density lipoprotein cholesterol and low low-density lipoprotein cholesterol that they exhibited could partly explain their more distensible aorta and, subsequently, their low atherosclerosis risk BF: R²=0.5, p< Age (years) Contemporary pygmies (CP) Bantou Farmers (BF) CP: R²=0.25, p=0.03 TP: R²=0.085, p=0.212 Traditional pygmies (TP) Figure. Effects of aging on pulse wave velocity (PWV) in the 3 study groups.

5 Lemogoum et al Lifestyle and Arterial Stiffness in Pygmies 127 An unexpected finding in this study is the blunted effect of aging on the increase of PWV. Arterial stiffening is an inevitable part of the aging process. 25,26 Indeed, with advancing age, the aorta and large arteries become progressively less distensible, and the ability to absorb pulsations from the ejecting ventricle is reduced. 25 Our observation is in keeping with the Chinese community study 26 that reported lower aortic PWV in rural Guangzhou subjects and that increased to a lesser degree with age as compared with urban Beijing subjects with the same BP. That blunted effect of aging on PWV was attributed to low-salt intake diet. 26 Our finding could be also attributed at least to TP low-sodium diet and high fruit and vegetable consumption, which constitute a major component of their subsistence mode. Interestingly, in this study, TP status emerged as an independent determinant of the reduction in arterial stiffness in the whole study population, indicating a possible intrinsic vascular protective mechanism probably linked to their hunter-gathering subsistence mode and/or to their genetic constitution. Some genetic predisposition of increase arterial stiffness has been reported. 14,24,27 Further studies are needed to elucidate the underlying mechanism explaining slower PWV in TPs, taking into account genetic aspects of their aorta. BP is a major determinant of PWV. 14,19 Indeed, aortic stiffening can be functional, resulting from high BP without structural changes of the artery. However, the BP cannot solely explain the observed difference in PWV among TPs and CPs and BFs, because it remained lower in TPs than in CPs and BFs, even after adjustment for MAP. The increase of BP with age is well established in the Bantou population. 24 This was the case for BF and CP participants but not for TPs in whom, as reported previously, 9,11 BP does not increase with age, probably partly because of their low body weight. Wave Reflections in Pygmies AIx is a marker of aortic wave reflections. In our study, no differences in AIx were observed among TPs, CPs, and BFs. Multivariate analysis revealed that AIx increased with short stature, age, and MAP. Our observations are in keeping with previous studies, which observed strong association between AIx and height, 19,28 MAP, 22,28 and age. 28 Sex is known to influence AIx independent of changes in stiffness 29 ; however, this was not the case in our study; probably because sex did not differ among the 3 groups. AIx depends also on transit time and site of arterial wave reflections. 22,23 Transit time was shorter and an independent determinant of AIx in TPs, thus, early wave reflections observed in the TP group was probably attributed to their short stature that was accompanied by a shorter aorta, resulting in sites of the reflected waves closer to their heart. The short stature of adult pygmies has been attributed to various factors related to individuals, such as a failure of growth to accelerate during puberty, 30,31 metabolic adaptation to low food availability and ambient temperature, and increased mobility in the forest. 12,32 Arterial Stiffness and CV Variables in the Whole Study The present study confirms previous observations reporting increased PWV with aging, 22,26 high BP, 14,22,26 and obesity 33 in the entire study population. No relation was found between PWV and cholesterol in our study and was in keeping with some previous studies 34,35 but not all. 27 Increased AIx with aging and BP is in accordance with previous observations, 16,21 23 as well as its decrease with higher stature. 19,28 Limitations The potential limitation of the present study is small sample size and the lack of screening of serum DNA telomerase length and activities that could be helpful to determine whether the observed difference in PWV between TPs and CPs and BFs are attributed to genetic determinants or only to environmental factors. Therefore, further studies, including a larger-scale sample population coupled with assessment of DNA telomerase activities and length, are needed to confirm our findings. Perspectives Increased atherosclerosis is an established determinant of CV outcomes. 14,15 The present study provides the first evidence that hunter-gatherer lifestyle is associated with low atherosclerosis risk elicited by less stiffening of the aorta of TP. The changes from traditional to transitional and modern lifestyles as indigenous people become victims of Bantous proximity are sensitive indicators of the influence of living environments rather than genetic determinants. Our findings increase knowledge of the health status of pygmies in a country lacking health data and provide strong arguments for improvements needed in the collection of their health data and the provision of health services. Conclusions The present study reveals that hunter-gatherer lifestyle is associated with lower aortic stiffness attributed at least partly to low body weight and blunted effects of aging and BP on TP arterial structure and function. The similarity of AIx in the tree groups could be accounted for by early wave reflections in relation to TP shorter stature. An appreciation of the adaptive history of African populations with different modes of subsistence should improve our understanding of the influence of human lifestyles on CVD. Sources of Funding This study was supported by the French Foundation for Research on Arterial Hypertension (to D.L.) and the Dr. Tagnon Fund (to P.V.d.B.). None. Disclosures References 1. Mensah G. Ischemic heart disease in Africa. Heart. 2008;94: Yusuf S, Reddy S, Ôunpuu S, Anand S. Global burden of cardiovascular diseases: part II variations in cardiovascular disease by specific ethnic groups and geographic regions and prevention strategies. Circulation. 2001;104: Opie L, Seedat YK. Hypertension in Sub-Saharan African populations. Circulation. 2005;112: Cooper RS, Zhu X. Racial differences and genetic of hypertension. 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Influence of sex on arterial hemodynamics and blood pressure: role of body height. Hypertension. 1996;26: What Is New? This is the first study on central hemodynamic properties in traditional pigmies, an indigenous people born and living in Cameroon equatorial forest on hunter-gather subsistence mode compared to pigmies migrated to semiurban area and bantou farmers. Although it has been generally evangelized that pygmies have lower health problem, this study is the first of its kind to draw innovative attention on the atherosclerosis risk in that marginalized and jeopardized population. What Is Relevant? The lower aortic stiffness in traditional pigmies. Novelty and Significance 20. Lemogoum D, Van Bortel L, Najem B, Dzudie A, Teutcha C, Madu E, Leeman M, Degaute JP, Van de Borne P. Arterial stiffness and wave reflections in patients with sickle cell disease. Hypertension. 2004;44: Asmar R, Benetos A, Topouchian J, Laurent P, Pannier B, Brisac AM, Target R, Levi BI. 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Lancet. 1991;338: The blunted effects of aging and BP on the increase of PWV in traditional pygmies suggesting that they may be at low hypertension risk. Pigmies migrated to urban area are taller and have a higher BMI than traditional pigmies. Despite the smaller stature, AIx was not higher in traditional pigmies. Summary Hunter-gather subsistence mode is associated with low atherosclerosis risk in traditional pygmies translated by less stiffer aorta. The unaltered AIx in traditional pigmies may be due to the slower PWV despite reflection points closer to the heart.