Greater central adiposity resulting from increased market integration is associated with elevated C-reactive protein levels in older women from the Republic of Vanuatu

Hayley Mann; Alysa Pomer; Kathryn Olszowy; Cheng Sun; Harold Silverman; Kelsey Dancause; Chim Chan; Len Tarivonda; George Taleo; Akira Kaneko; Charles Weitz; Ralph Garruto; Jefrey  Lum

doi:10.52905/hbph.v2.20

Authors

Hayley Mann Binghamton University https://orcid.org/0000-0003-0640-1617
Alysa Pomer Department of Chronic Disease Epidemiology, Yale School of Public Health, New Haven, CT https://orcid.org/0000-0003-1267-1189
Kathryn M. Olszowy Department of Anthropology, New Mexico State University, Las Cruces NM https://orcid.org/0000-0003-0843-4519
Cheng Sun Department of Anthropology, Binghamton University, Binghamton, NY; Laboratory of Evolutionary Anthropology and Health, Binghamton University, Binghamton, NY
Harold Silverman Laboratory of Biomedical Science, The Feinstein Institute for Medical Research, Manhasset, NY; Hofstra North Shore-LIJ School of Medicine at Hofstra University, Hempstead, NY
Kelsey N. Dancause Départment des sciences de l’activité physique, Université du Quebec à Montréal, Montréal QC, Canada https://orcid.org/0000-0002-8677-9953
Chim W. Chan Department of Parasitology, Graduate School of Medicine, Osaka City University, Osaka, Japan https://orcid.org/0000-0002-4039-2649
Len Tarivonda Ministry of Health, Port Vila, Vanuatu
George Taleo Ministry of Health, Port Vila, Vanuatu
Akira Kaneko Department of Parasitology, Graduate School of Medicine, Osaka City University, Osaka, Japan; Island Malaria Group, Department of Microbiology, Tumor and Cell Biology (MTC), Karolinska Institutet, Stockholm, Sweden; Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan
Charles A. Weitz Department of Anthropology, Temple University, Philadelphia, PA
Ralph M. Garruto Department of Anthropology, Binghamton University, Binghamton, NY; Laboratory of Biomedical Anthropology and Neurosciences, Binghamton University, Binghamton, NY; Department of Biological Sciences, Binghamton University, Binghamton, NY https://orcid.org/0000-0003-4985-8190
J. Koji Lum Department of Anthropology, Binghamton University, Binghamton, NY; Laboratory of Evolutionary Anthropology and Health, Binghamton University, Binghamton, NY; Department of Biological Sciences, Binghamton University, Binghamton, NY

DOI:

https://doi.org/10.52905/hbph.v2.20

Keywords:

Body Mass Index, central adiposity, Pacific Islands, Melanesians, market integration

Abstract

Objective: We characterized the relationship between circulating C-reactive protein (CRP) levels and nine anthropometric measures of body fat to identify the best anthropometric predictors of CRP in Ni-Vanuatu women.

Sample and Methods: Anthropometric data and blood spot samples were collected from sixty-four Ni-Vanuatu female participants (age 35-78 years) on five islands with varying degrees of market integration, cultural change, and obesity. CRP concentration was determined with a high-sensitivity ELISA (hsCRP) assay and then compared to nine different anthropometric measurements.

Results: BMI was significantly correlated with CRP (p=0.047). Among the eight additional anthropometrics, the suprailiac skinfold (p=0.003) and waist-circumference (p=0.009) were better predictors of CRP than BMI. Moreover, our stepwise selection model indicated that the suprailiac skinfold explained ~14% of CRP level variance.

Conclusions: The BMI-CRP correlation coefficient for Ni-Vanuatu women falls within the range of previously reported values for East Asian populations with whom they share genetic ancestry. However, the best anthropometric predictors of CRP levels were waist circumference and suprailiac skinfold thickness. These measures capture central adiposity and are more closely associated with elevated CRP level and cardiovascular disease risk than fat distributed elsewhere on the body. Ni-Vanuatu in urban settings with high market integration are at greater risk for obesity, which is associated with elevated CRP levels. However, because nearly all Ni-Vanuatu still retain horticultural knowledge and land ownership, consumption of processed, imported foods is largely determined by degree of market integration and personal choice. Therefore, health interventions focusing on sustainable traditional food practices are feasible.

Author Biography

Hayley Mann, Binghamton University

PhD candidate in Molecular Anthropology at Binghamton University, New York. Genomics Variation Scientist in human clinical genetics at Sema4 in Stamford, CT.

References

Allen, M. R. (1968). The establishment of Christianity and cash‐cropping in a New Hebridean community. The Journal of Pacific History 3 (1), 25–46. https://doi.org/10.1080/00223346808572123.

An, Y./Yi, S./Fitzpatrick, A./Gupta, V./Prak, P. R./Oum, S./LoGerfo, J. P. (2013). Appropriate body mass index and waist circumference cutoff for overweight and central obesity among adults in Cambodia. PloS One 8 (10), e77897. https://doi.org/10.1371/journal.pone.0077897.

Brooks, G. C./Blaha, M. J./Blumenthal, R. S./Brooks, Gabriel C./Blaha, Michael J./Blumenthal, Roger S. (2010). Relation of C-reactive protein to abdominal adiposity. The American Journal of Cardiology 106 (1), 56–61. https://doi.org/10.1016/j.amjcard.2010.02.017.

Central Intelligence Agency (2021). Obesity – adult prevalence rate. The World Factbook, Langley (VA).

Choi, J./Joseph, L./Pilote, L. (2012). Obesity and C‐reactive protein in various populations: a systematic review and meta‐analysis. Obesity Reviews 14 (3), 232–244. https://doi.org/10.1111/obr.12003.

Dancause, K. N./DeHuff, C./Soloway, L. E./Vilar, M./Chan, C./Wilson, M./Tarivonda, L./Regenvanu, R./Kaneko, A./Garruto, R. M./Lum, J. K. (2011). Behavioral changes associated with economic development in the South Pacific: health transition in Vanuatu. American Journal of Human Biology 23 (3), 366–376. https://doi.org/10.1002/ajhb.21146.

Dancause, K. N./Vilar, M./DeHuff, C./Wilson, M./Soloway, L. E./Chan, C./Lum, J. K./Garruto, R. M. (2010). Relationships between body size and percent body fat among Melanesians in Vanuatu. Asia Pacific Journal of Clinical Nutrition 19 (3), 425–431.

Dancause, K. N./Vilar, M./Wilson, M./Soloway, L. E./DeHuff, C./Chan, C./Tarivonda, L./Regenvanu, R./Kaneko, A./Lum, J. K./Garruto, R. M. (2013). Behavioral risk factors for obesity during health transition in Vanuatu, South Pacific. Obesity 21 (1), E98‐E104. https://doi.org/10.1002/oby.20082.

Danesh, J./Whincup, P./Walker, M./Lennon, L./Thomson, A./Appleby, P./Gallimore, J. R./Pepys, M. B. (2000). Low grade inflammation and coronary heart disease: prospective study and updated meta-analyses. BMJ 321 (7255), 199–204. https://doi.org/10.1136/bmj.321.7255.199.

DeLoach, S./Falkner, B./Keith, S. W./Gidding, S. S. (2014). Obesity associated inflammation in African American adolescents and adults. The American Journal of the Medical Sciences 347 (5), 357–363. https://doi.org/10.1097/MAJ.0b013e31829555f0.

Ding, D./Wang, M./Su, D./Hong, C./Li, X./Yang, Y./Zhang, Y./Hu, G./Ling, W. (2015). Body mass index, high-sensitivity C-reactive protein and mortality in Chinese with coronary artery disease. PloS One 10 (8), e0135713. https://doi.org/10.1371/journal.pone.0135713.

Doumatey, A. P./Lashley, K. S./Huang, H./Zhou, J./Chen, G./Amoah, A./Agyenim‐Boateng, K./Oli, J./Fasanmade, O./Adebamowo, C. A./Adeyemo, A. A./Rotimi, C. N. (2010). Relationships among obesity, inflammation, and insulin resistance in African Americans and West Africans. Obesity 18 (3), 598–603. https://doi.org/10.1038/oby.2009.322.

Ford, E. S./Giles, W. H./Mokdad, A. H./Myers, G. L. (2004). Distribution and correlates of C-reactive protein concentrations among adult US women. Clinical Chemistry 50 (3), 574–581. https://doi.org/10.1373/clinchem.2003.027359.

Forouhi, N. G./Sattar, N./McKeigue, P. M. (2001). Relation of C-reactive protein to body fat distribution and features of the metabolic syndrome in Europeans and South Asians. International Journal of Obesity 25 (9), 1327–1331. https://doi.org/10.1038/sj.ijo.0801723.

Ghaffari, M. A./Sede, S. A./Rashtchizadeh, N./Mohammadzadeh, G./Majidi, S. (2014). Association of CRP gene polymorphism with CRP levels and Coronary Artery Disease in Type 2 Diabetes in Ahvaz, southwest of Iran. Bioimpacts 4 (3), 133. https://doi.org/10.15171/bi.2014.006.

Ghosh, C. (2003). Healthy people 2010 and Asian Americans/Pacific islanders: defining a baseline of information. American Journal of Public Health 93 (12), 2093–2098. https://doi.org/10.2105/ajph.93.12.2093.

Gill, T. (2006). Epidemiology and health impact of obesity: an Asia Pacific perspective. Asia Pacific Journal of Clinical Nutrition 15, Suppl:3–14.

Huang, C.‐C./Chung, C.‐M./Leu, H.‐B./Lin, T.‐H./Hung, S.‐l./Wu, T.‐C./Huang, P.‐H./Lin, S.‐J./Pan, W.‐H./Chen, J.‐W. (2013). Genetic variation in C-reactive protein in ethnic Chinese population in Taiwan. European Journal of Clinical Investigation 43 (5), 449–456. https://doi.org/10.1111/eci.12067.

Jeemon, P./Prabhakaran, D./Ramakrishnan, L./Gupta, R./Ahmed, F./Thankappan, K. R./Kartha, C. C./Chaturvedi, V./Reddy, K. S. (2011). Association of high sensitive C-reactive protein (hsCRP) with established cardiovascular risk factors in the Indian population. Nutrition & Metabolism 8 (1), 1–8. https://doi.org/10.1186/1743-7075-8-19.

Jitnarin, N./Kosulwat, V./Rojroongwasinkul, N./Boonpraderm, A./Haddock, C. K./Poston, W. S.C./Jitnarin, N./Poston, W. S. C. (2011). Prevalence of overweight and obesity in Thai population: results of the National Thai Food Consumption Survey. Eating and Weight Disorders 16 (4), e242–e249. https://doi.org/10.1007/BF03327467.

Kaneko, A./Taleo, G./Kalkoa, M./Yamar, S./Kobayakawa, T./Björkman, A. (2000). Malaria eradication on islands. Lancet 356 (9241), 1560–1564. https://doi.org/10.1016/S0140-6736(00)03127-5.

Kathiresan, S./Larson, M. G./Vasan, R. S./Guo, C.-Y./Gona, P./Keaney Jr, J. F./Wilson, P. W. F./Newton-Cheh, C./Musone, S. L./Camargo, A. L./Keaney, J. F./Drake, J. A./Levy, D./O'Donnell, C. J./Hirschhorn, J. N./Benjamin, E. J. (2006). Contribution of clinical correlates and 13 C-reactive protein gene polymorphisms to interindividual variability in serum C-reactive protein level. Circulation 113 (11), 1415–1423. https://doi.org/10.1161/CIRCULATIONAHA.105.591271.

Kayser, M. (2010). The human genetic history of Oceania: near and remote views of dispersal. Current Biology 20 (4), R194–R201. https://doi.org/10.1016/j.cub.2009.12.004.

Khoo, C. M./Sairazi, S./Taslim, S./Gardner, D./Wu, Y./Lee, J./van Dam, R. M./Tai, E. S. (2011). Ethnicity modifies the relationships of insulin resistance, inflammation, and adiponectin with obesity in a multiethnic Asian population. Diabetes Care 34 (5), 1120–1126. https://doi.org/10.2337/dc10-2097.

Klein, S./Allison, D. B./Heymsfield, S. B./Kelley, D. E./Leibel, R. L./Nonas, C./Kahn, R. (2007). Waist circumference and cardiometabolic risk: a consensus statement from shaping America’s health: Association for Weight Management and Obesity Prevention; NAASO, the Obesity Society; the American Society for Nutrition; and the American Diabetes Association. The American Journal of Clinical Nutrition 85 (5), 1197–1202. https://doi.org/10.1093/ajcn/85.5.1197.

Lim, S./Jang, H. C./Lee, H. K./Kimm, K. C./Park, C./Cho, N. H. (2006). The relationship between body fat and C-reactive protein in middle-aged Korean population. Atherosclerosis 184 (1), 171–177. https://doi.org/10.1016/j.atherosclerosis.2005.04.003.

Lipson, M./Skoglund, P./Spriggs, M./Valentin, F./Bedford, S./Shing, R./Buckley, H./Phillip, I./Ward, G. K./Mallick, S./Rohland, N./Broomandkhoshbacht, N./Cheronet, O./Ferry, M./Harper, T. K./Michel, M./Oppenheimer, J./Sirak, K./Stewardson, K./Auckland, K./Hill, A. V. S./Maitland, K./Oppenheimer, S. J./Parks, T./Robson, K./Williams, T. N./Kennett, D. J./Mentzer, A. J./Pinhasi, R./Reich, D. (2018). Population turnover in remote Oceania shortly after initial settlement. Current Biology 28 (7), 1157–1165. https://doi.org/10.1016/j.cub.2018.02.051.

Lohman, T. G./Roche, A. F./Martorell, R. (Eds.) (1988). Anthropometric standardization reference manual. Champaign, Ill., Human Kinetics Books.

Lum, J. K./Cann, R. L. (1998). mtDNA and language support a common origin of Micronesians and Polynesians in Island Southeast Asia. American Journal of Physical Anthropology 105 (2), 109–119. https://doi.org/10.1002/(SICI)1096-8644(199802)105:2<109::AID-AJPA1>3.3.CO;2-M.

MacClancy, J. (1981). To kill a bird with two stones. A short history of Vanuatu. Port Vila, Vanuatu Cultural Centre.

McDade, T. W./Hawkley, L. C./Cacioppo, J. T. (2006). Psychosocial and behavioral predictors of inflammation in middle-aged and older adults: the Chicago health, aging, and social relations study. Psychosomatic Medicine 68 (3), 376–381. https://doi.org/10.1097/01.psy.0000221371.43607.64.

McDade, T. W./Rutherford, J. N./Adair, L./Kuzawa, C. (2009). Population differences in associations between C-reactive protein concentration and adiposity: comparison of young adults in the Philippines and the United States. The American Journal of Clinical Nutrition 89 (4), 1237–1245. https://doi.org/10.3945/ajcn.2008.27080.

McKeigue, P. M./Shah, B./Marmot, M. G. (1991). Relation of central obesity and insulin resistance with high diabetes prevalence and cardiovascular risk in South Asians. Lancet 337 (8738), 382–386. https://doi.org/10.1016/0140-6736(91)91164-P.

McLennan, A. K./Ulijaszek, S. J. (2015). Obesity emergence in the Pacific islands: why understanding colonial history and social change is important. Public Health Nutrition 18 (8), 1499–1505. https://doi.org/10.1017/S136898001400175X.

NCD Risk Factor Collaboration (2019). Rising rural body-mass index is the main driver of the global obesity epidemic in adults. Nature 569 (7755), 260. https://doi.org/10.1038/s41586-019-1171-x.

Neuhouser, M. L./Schwarz, Y./Wang, C./Breymeyer, K./Coronado, G./Wang, C. Y./Noar, K./Song, X./Lampe, J. W. (2012). A low-glycemic load diet reduces serum C-reactive protein and modestly increases adiponectin in overweight and obese adults. Journal of Nutrition 142 (2), 369-374. https://doi.org/10.3945/jn.111.149807.

Neovius, M./Hemmingsson, E./Freyschuss, B./Uddén, J. (2006). Bioelectrical impedance underestimates total and truncal fatness in abdominally obese women. Obesity 14 (10), 1731–1738. https://doi.org/10.1038/oby.2006.199.

Olszowy, K. M./Pomer, A./Dancause, K. N./Sun, C./Silverman, H./Lee, G./Chan, C. W./Tarivonda, L./Regenvanu, R./Kaneko, A./Weitz, C. A./Lum, J. K./Garruto, R. M. (2015). Impact of modernization on adult body composition on five islands of varying economic development in Vanuatu. American Journal of Human Biology 27 (6), 832–844. https://doi.org/10.1002/ajhb.22734.

Pan, W.-H./Yeh, W.-T. (2008). How to define obesity? Evidence-based multiple action points for public awareness, screening, and treatment: an extension of Asian-Pacific recommendations. Asia Pacific Journal of Clinical Nutrition 17 (3), 370.

Pankow, J. S./Folsom, A. R./Cushman, M./Borecki, I. B./Hopkins, P. N./Eckfeldt, J. H./Tracy, R. P. (2001). Familial and genetic determinants of systemic markers of inflammation: the NHLBI family heart study. Atherosclerosis 154 (3), 681–689. https://doi.org/10.1016/S0021-9150(00)00586-4.

Park, H. S./Park, J. Y./Yu, R. (2005). Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-α and IL-6. Diabetes Research and Clinical Practice 69 (1), 29–35. https://doi.org/10.1016/j.diabres.2004.11.007.

Pearson, T. A./Mensah, G. A./Alexander, R. W./Anderson, J. L./Cannon III, R. O./Criqui, M./Fadl, Y. Y./Fortmann, S. P./Hong, Y./Myers, G. L./Cannon, R. O./Rifai, N./Smith, S. C./Taubert, K./Tracy, R. P./Vinicor, F. (2003). Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 107 (3), 499–511. https://doi.org/10.1161/01.CIR.0000052939.59093.45.

Peters, S. A. E./Bots, S. H./Woodward, M. (2018). Sex differences in the association between measures of general and central adiposity and the risk of myocardial infarction: results from the UK Biobank. Journal of the American Heart Association 7 (5), e008507. https://doi.org/10.1161/JAHA.117.008507.

Popkin, B. M. (2004). The nutrition transition: an overview of world patterns of change. Nutrition Reviews 62 (7, Suppl. Pt 2), S140–S143. https://doi.org/10.1111/j.1753-4887.2004.tb00084.x.

Popkin, B. M./Adair, L. S./Ng, S. W. (2012). Global nutrition transition and the pandemic of obesity in developing countries. Nutrition Reviews 70 (1), 3–21. https://doi.org/10.1111/j.1753-4887.2011.00456.x.

Saito, M./Ishimitsu, T./Minami, J./Ono, H./Ohrui, M./Matsuoka, H. (2003). Relations of plasma high-sensitivity C-reactive protein to traditional cardiovascular risk factors. Atherosclerosis 167 (1), 73–79. https://doi.org/10.1016/S0021-9150(02)00380-5.

Schafer, M. H./Ferraro, K. F./Williams, S. R. (2011). Low socioeconomic status and body mass index as risk factors for inflammation in older adults: conjoint influence on C-reactive protein? Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences 66 (6), 667–673. https://doi.org/10.1093/gerona/glr009.

Sergi, G./Rui, M. de/Stubbs, B./Veronese, N./Manzato, E. (2017). Measurement of lean body mass using bioelectrical impedance analysis: a consideration of the pros and cons. Aging Clinical and Experimental Research 29 (4), 591–597. https://doi.org/10.1007/s40520-016-0622-6.

Shin, H.-R./Varghese, C. (2014). WHO Western Pacific regional action plan for the prevention and control of NCDs (2014-2020). Epidemiology and Health 36, e2014007. https://doi.org/10.4178/epih/e2014007.

Sites, C. K./Toth, M. J./Cushman, M./L’Hommedieu, G. D./Tchernof, A./Tracy, R. P./Poehlman, E. T. (2002). Menopause-related differences in inflammation markers and their relationship to body fat distribution and insulin-stimulated glucose disposal. Fertility and Sterility 77 (1), 128–135. https://doi.org/10.1016/S0015-0282(01)02934-X.

Skoglund, P./Posth, C./Sirak, K./Spriggs, M./Valentin, F./Bedford, S./Clark, G. R./Reepmeyer, C./Petchey, F./Fernandes, D./Fu, Q./Harney, E./Lipson, M./Mallick, S./Novak, M./Rohland, N./Stewardson, K./Abdullah, S./Cox, M. P./Friedlaender, F. R./Friedlaender, J. S./Kivisild, T./Koki, G./Kusuma, P./Merriwether, D. A./Ricaut, F./Wee, J. T. S./Patterson, N./Krause, J./Pinhasi, R./Reich, D. (2016). Genomic insights into the peopling of the Southwest Pacific. Nature 538 (7626), 510–513. https://doi.org/10.1038/nature19844.

Steptoe, A./Hamer, M./Chida, Y. (2007). The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain, Behavior, and Immunity 21 (7), 901-912. https://doi.org/10.1016/j.bbi.2007.03.011.

Sung, K.-C./Ryu, S./Chang, Y./Byrne, C. D./Kim, S. H. (2014). C-reactive protein and risk of cardiovascular and all-cause mortality in 268 803 East Asians. European Heart Journal 35 (27), 1809–1816. https://doi.org/10.1093/eurheartj/ehu059.

Swinburn, B. A./Sacks, G./Hall, K. D./McPherson, K./Finegood, D. T./Moodie, M. L./Gortmaker, S. L. (2011). The global obesity pandemic: shaped by global drivers and local environments. Lancet 378 (9793), 804–814. https://doi.org/10.1016/S0140-6736(11)60813-1.

Trinh, O. T. H./Nguyen, N. D./Phongsavan, P./Dibley, M. J./Bauman, A. E. (2009). Prevalence and risk factors with overweight and obesity among Vietnamese adults: Caucasian and Asian cut-offs. Asia Pacific Journal of Clinical Nutrition 18 (2), 226–233. Available online at https://search.informit.org/doi/10.3316/informit.683855345951353 (accessed 11/19/2021).

Vilar, M. G. (2010). Origins and post-settlement gene flow among culturally and linguistically distinct Pacific populations. Doctoral dissertation. [New York], Binghamton University.

Visser, M./Bouter, L. M./McQuillan, G. M./Wener, M. H./Harris, T. B. (1999). Elevated C-reactive protein levels in overweight and obese adults. JAMA 282 (22), 2131–2135. https://doi.org/10.1001/jama.282.22.2131.

WHO Expert Consultation (2004). Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 363 (9403), 157–163. https://doi.org/10.1016/S0140-6736(03)15268-3.

World Health Organization (2000a). Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organization technical report series 894, 1–253. PMID: 11234459.

World Health Organization. Regional Office for the Western Pacific (2000b). The Asia-Pacific perspective: redefining obesity and its treatment. Sydney : Health Communications Australia. https://apps.who.int/iris/handle/10665/206936 (accessed 12/22/2021).

Zacho, J./Tybjærg-Hansen, A./Nordestgaard, B. G./Tybjaerg-Hansen, A. (2010). C-reactive protein and all-cause mortality: the Copenhagen City Heart Study. European Heart Journal 31 (13), 1624–1632. https://doi.org/10.1093/eurheartj/ehq103.