Articles | Volume 7, issue 2
https://doi.org/10.5194/pb-7-41-2020
© Author(s) 2020. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/pb-7-41-2020
© Author(s) 2020. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
17 Dec 2020
Research article |
| 17 Dec 2020
| 17 Dec 2020
Testing lipid markers as predictors of all-cause morbidity, cardiac disease, and mortality risk in captive western lowland gorillas (Gorilla gorilla gorilla)
Center for Species Survival, Smithsonian Conservation Biology
Institute, 1500 Remount Rd., Front Royal, VA 22630, USA
currently at: Department of Reproductive and
Behavioral Sciences, Saint Louis Zoo, St. Louis, MO 63110, USA
Janine L. Brown
Center for Species Survival, Smithsonian Conservation Biology
Institute, 1500 Remount Rd., Front Royal, VA 22630, USA
Katie L. Edwards
Center for Species Survival, Smithsonian Conservation Biology
Institute, 1500 Remount Rd., Front Royal, VA 22630, USA
North of England Zoological Society, Chester Zoo, Upton by Chester,
CH2 1LH, UK
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Cited articles
Alberti, K. G. M. M., Zimmet, P. Z., and Shaw, J.: Metabolic syndrome – a new
world-wide definition. A Consensus Statement from the International Diabetes
Federation, Diabet. Med., 23, 469–480, 2006.
Amos, C. I., Elston, R. C., Srinivasan, S. R., Wilson, A. F., Cresanta, J.
L., Ward, L. J., and Berenson, G. S.: Linkage and Segregation Analyses of
Apolipoproteins A1 and B, and Lipoprotein Cholesterol Levels in a Large
Pedigree with Excess Coronary Heart Disease: The Bogalusa Heart Study,
Genet. Epidemiol., 4, 115–128, 1987.
Anestis, S. F.: Urinary cortisol responses to unusual events in captive
chimpanzees (Pan troglodytes), Stress,
12, 49–57, 2009.
Anestis, S. F., Bribiescas, R. G., and Hasselschwert, D. L.: Age, rank, and
personality effects on the cortisol sedation stress response in young
chimpanzees, Physiol. Behav., 89, 287–294, 2006.
Arnold, T. W.: Uninformative Parameters and Model Selection Using Akaike's
Information Criterion, J. Wildl. Manage., 74, 1175–1178, 2010.
Atsalis, S. and Margulis, S. W.: Sexual and Hormonal Cycles in Geriatric
Gorilla gorilla gorilla, Int. J. Primatol., 27, 1663–1687, 2006.
Avogaro, P., Cazzolato, G., Bittolo Bon, G., Quinci, G. B., and Chinello, M.:
HDL-cholesterol, apolipoproteins A1 and B: Age and Index Body Weight,
Atherosclerosis, 31, 85–91, 1978.
Bachen, E. A., Muldoon, M. F., Matthews, K. A., and Manuck, S. B.: Effects of
hemoconcentration and sympathetic activation on serum lipid responses to
brief mental stress, Psychosom. Med., 64, 587–594, 2002.
Baitchman, E. J., Calle, P. P., Clippinger, T. L., Deem, S. L., James, S.
B., Raphael, B. L., and Cook, R. A.: Preliminary evaluation of blood lipid
profiles in captive western lowland gorillas (Gorilla gorilla gorilla), J. Zoo Wildl. Med., 37,
126–129, 2006.
Bartoń, K.: MuMIn: Multi-Model Inference, R package version 1.43.15,
available at: https://CRAN.R-project.org/package=MuMIn (last access: 24 March 2020), 2019.
Bates, D., Maechler, M., Bolker, B., Walker, S., Christensen, R. H. B.,
Singmann, H., Dai, B., Scheipl, F., Grothendieck, G., Green, P., and Fox, J.:
lme4: Linear Mixed-Effects Models using “Eigen” and S4. R package version
1.1-21, available at: https://cran.r-project.org/package=lme4 (last access: 24 March 2020),
2019.
Benirschke, K. and Adams, F. D.: Gorilla diseases and causes of death, J.
Reprod. Fertil., Suppl. 28, 139–148, 1980.
Bittner, V., Johnson, B. D., Zineh, I., Rogers, W. J., Vido, D., Marroquin,
O. C., Bairey-Merz, C. N., and Sopko, G.: The triglyceride/high-density
lipoprotein cholesterol ratio predicts all-cause mortality in women with
suspected myocardial ischemia: A Report From the Women's Ischemia Syndrome
Evaluation (WISE), Am. Heart J., 157, 548–555, 2009.
Castelli, W. P. and Anderson, K.: A Population at Risk: Prevalence of High
Cholesterol Levels in Hypertensive Patients in the Framingham Study, Am. J.
Med., 80, 23–32, 1986.
Chapman, M. J., Ginsberg, H. N., Amarenco, P., Andreotti, F., Borén, J.,
Catapano, A. L., Descamps, O. S., Fisher, E., Kovanen, P. T., Kuivenhoven,
J. A., Lesnik, P., Masana, L., Nordestgaard, B. G., Ray, K. K., Reiner, Z.,
Taskinen, M.-R., Tokgözoglu, L., Tybjærg-Hansen, A., and Watts, G.
F.: Triglyceride-rich lipoproteins and high-density lipoprotein cholesterol
in patients at high risk of cardiovascular disease: evidence and guidance
for management, Eur. Heart J., 32, 1345–1361, 2011.
Chen, Z., Chen, G., Qin, H., Cai, Z., Huang, J., Chen, H., Wu, W., Chen, Z.,
Wu, S., and Chen, Y.: Higher triglyceride to high-density lipoprotein
cholesterol ratio increases cardiovascular risk: 10-year prospective study
in a cohort of Chinese adults, J. Diabetes Investig., 11, 475–481, 2020.
Cordero, A., Andrés, E., Ordoñez, B., León, M., Laclaustra, M.,
Grima, A., Luengo, E., Moreno, J., Bes, M., Pascual, I., Civeira, F.,
Pocoví, M., Alegría, E., and Casasnovas, J. A.: Usefulness of
triglycerides-to-high-density lipoprotein cholesterol ratio for predicting
the first coronary event in men, Am. J. Cardiol., 104, 1393–1397, 2009.
Corti, M.-C., Guralnik, J. M., Salive, M. E., Harris, T., Ferrucci, L.,
Glynn, R. J., and Havlik, R. J.: Clarifying the Direct Relation between Total
Cholesterol Levels and Death from Coronary Heart Disease in Older Persons,
Ann. Intern. Med., 126, 753–760, 1997.
Cousins, D.: Diseases and injuries in wild and captive gorillas (Gorilla gorilla), Int. Zoo
Yearbook, 12, 211–218, 1972.
Crissey, S. D., Barr, J. E., Slifka, K. A., Bowen, P. E.,
Stacewicz-Sapuntzakis, M., Langman, C., Ward, A., and Ange, K.: Serum
Concentrations of Lipids, Vitamins A and E, Vitamin D Metabolites, and
Carotenoids in Nine Primate Species at Four Zoos, Zoo Biology, 18,
551–564, 1999.
da Luz, P. L., Favarato, D., Faria-Neto Jr., J. R., Lemos, P., and Chagas,
A. C. P.: High ratio of triglycerides to HDL-cholesterol predicts extensive
coronary disease, Clinics, 64, 427–432, 2008.
Damsgaard, E. M., Fr øland, A., J ørgensen, O. D., and Mogensen, C. E.:
Microalbuminuria as predictor of increased mortality in elderly people, Br.
Med. J., 300, 297–300, 1990.
Dennis, P. M., Raghanti, M. A., Meindl, R. S., Less, E., Henthorn, E.,
Devlin, W., Murray, S., Meehan, T., Kutinsky, I., and Murphy, H.: Cardiac
disease is linked to adiposity in male gorillas (Gorilla gorilla gorilla), PLoS One, 14,
e0218763, https://doi.org/10.1371/journal.pone.0218763, 2019.
Dimsdale, J. E. and Herd, J. A.: Variability of plasma lipids in response to
emotional arousal, Psychosom. Med., 44, 413–430, 1982.
Edes, A. N. and Brand, C. M.: Age, sex, and individual inflammatory markers
predict chronic conditions, cardiovascular disease, and mortality among
captive western lowland gorillas (Gorilla gorilla gorilla), Am. J. Primatol., in review, 2020.
Emerging Risk Factors Collaboration: Major Lipids, Apolipoproteins, and Risk
of Vascular Disease, J. Am. Med. Assoc., 302, 1993–2000, 2009.
Everly, G. S. and Lating, J. M.: The Anatomy and Physiology of the Human
Stress Response, in A clinical guide to the treatment of the human stress
response, pp. 17–51, Springer, New York, 2013.
Fan, X., Liu, E. Y., Hoffman, V. P., Potts, A. J., Sharma, B., and
Henderson, D. C.: Triglyceride/high-density lipoprotein cholesterol ratio: a
surrogate to predict insulin resistance and low-density lipoprotein
cholesterol particle size in nondiabetic patients with schizophrenia. J.
Clin. Psychiatry, 72, 806–812, 2011.
Florvall, G., Basu, S., and Larsson, A.: Apolipoprotein A1 is a stronger
prognostic marker than are HDL and LDL cholesterol for cardiovascular
disease and mortality in elderly men, J. Gerontol. A Biol. Sci. Med. Sci.,
61A, 1262–1266, 2006.
Gaziano, J. M., Hennekens, C. H., O'Donnell, C. J., Breslow, J. L., and
Buring, J. E.: Fasting triglycerides, high-density lipoprotein, and risk of
myocardial infarction, Circulation, 96, 2520–2525, 1997.
Glei, D. A., Goldman, N., Rodríguez, G., and Weinstein, M.: Beyond
Self-Reports: Changes in Biomarkers as Predictors of Mortality, Popul. Dev.
Rev., 40, 331–360, 2014.
Greenland, S., Senn, S. J., Rothman, K. J., Carlin, J. B., Poole, C.,
Goodman, S. N., and Altman, D. G.: Statistical tests, P values, confidence
intervals, and power: a guide to misinterpretations, Eur. J. Epidemiol.,
31, 337–350, 2016.
Grueber, C. E., Nakagawa, S., Laws, R. J., and Jamieson, I. G.: Multimodel
inference in ecology and evolution: challenges and solutions, J. Evol.
Biol., 24, 699–711, 2011.
Hadaegh, F., Khalili, D., Ghasemi, A., Tohidi, M., Sheikholeslami, F., and
Azizi, F.: Triglyceride/HDL-cholesterol ratio is an independent predictor
for coronary heart disease in a population of Iranian men, Nutr Metab
Cardiovasc Dis., 19, 401–408, 2009.
Harrison, X. A., Donaldson, L., Correa-Cano, M. E., Evans, J., Fisher, D.
N., Goodwin, C. E. D., Robinson, B. S., Hodgson, D. J., and Inger, R.: A
brief introduction to mixed effects modelling and multi-model inference in
ecology, PeerJ, 6, e4794, https://doi.org/10.7717/peerj.4794, 2018.
Hindy, G., Åkesson, K. E., Melander, O., Aragam, K. G., Haas, M. E.,
Nilsson, P. M., Kadam, U. T., and Orho-Melander, M.: Cardiometabolic
Polygenic Risk Scores and Osteoarthritis Outcomes: A Mendelian Randomization
Study Using Data From the Malmö Diet and Cancer Study and the UK
Biobank, Arthritis Rheumatol, 71, 925–934, 2019.
Hokanson, J. E. and Austin, M. A.: Plasma triglyceride level is a risk
factor for cardiovascular disease independent of high-density lipoprotein
cholesterol level: a meta-analysis of population-based prospective studies,
J. Cardiovasc. Risk, 3, 213–219, 1996.
Horwich, T. B., Hamilton, M. A., MacLellan, W. R., and Fonarow, G. C.: Low
Serum Total Cholesterol is Associated With Marked Increase in Mortality in
Advanced Heart Failure, J. Card. Fail., 8, 216–224, 2002.
Hruban, Z., Meehan, T., Wolff, P., Wollmann, R. L., and Glagov, S.: Aortic
Dissection in a Gorilla, J. Med. Primatol., 15, 287–293, 1986.
Isles, C. G., Hole, D. J., Gillis, C. R., Hawthorne, V. M., and Lever, A. F.:
Plasma Cholesterol, Coronary Heart Disease, and Cancer in the Renfrew and
Paisley Survey, BMJ: British Medical J., 298, 920–924, 1989.
Iso, H., Jacobs, D. R., Jr, Wentworth, D., Neaton, J. D., and Cohen, J. D.:
Serum Cholesterol Levels and Six-Year Mortality From Stroke in 350,977 Men
Screened for the Multiple Risk Factor Intervention Trial, N. Engl. J. Med.,
320, 904–910, 1989.
Jacobs, R. M., Ross, S. R., Wagner, K. E., Leahy, M., Meiers, S. T., and
Santymire, R. M.: Evaluating the Physiological and Behavioral Response of a
Male and Female Gorilla (Gorilla gorilla gorilla) During an Introduction, Zoo Biol., 33,
394–402, 2014.
Janssen, D. L. and Bush, R. M.: Review of Medical Literature of Great Apes
in the 1980s, Zoo Biol., 9, 123–134, 1990.
Junge, R. E., Mezei, L. E., Muhlbauer, M., and Weber, M.: Cardiovascular
evaluation of lowland gorillas, J. Am. Vet. Med. Assoc., 212, 413–415,
1998.
Kang, H.-T., Shim, J.-Y., Lee, Y.-J., Lee, J.-E., Linton, J. A., Kim, J.-K.,
and Lee, H.-R.: Association between the ratio of triglycerides to
high-density lipoprotein cholesterol and chronic kidney disease in Korean
adults: the 2005 Korean National Health and Nutrition Examination Survey,
Kidney Blood Press. Res., 34, 173–179, 2011.
Kannel, W. B., Castelli, W. P., Gordon, T., and McNamara, P. M.: Serum
Cholesterol, Lipoproteins, and the Risk of Coronary Heart Disease, Ann.
Intern. Med., 74, 1–12, 1971.
Karlamangla, A. S., Singer, B. H., McEwen, B. S., Rowe, J. W., and Seeman, T.
E.: Allostatic load as a predictor of functional decline: MacArthur studies
of successful aging, J. Clin. Epidemiol., 55, 696–710, 2002.
Kenny, D. E., Cambre, R. C., Alvarado, T. P., Prowten, A. W., Allchurch, A.
F., Marks, S. K., and Zuba, J. R.: Aortic Dissection: An Important
Cardiovascular Disease in Captive Gorillas (Gorilla gorilla gorilla), J. Zoo Wildl. Med., 25,
561–568, 1994.
Koba, S., Hirano, T., Kondo, T., Shibata, M., Suzuki, H., Murakami, M.,
Geshi, E., and Katagiri, T.: Significance of small dense low-density
lipoproteins and other risk factors in patients with various types of
coronary heart disease, Am. Heart J., 144, 1026–1035, 2002.
Kronmal, R. A., Cain, K. C., Ye, Z., and Omenn, G. S.: Total Serum
Cholesterol Levels and Mortality Risk as a Function of Age: A Report Based
on the Framingham Data, Arch. Intern. Med., 153, 1065–1073, 1993.
Lambeth, S. P., Hau, J., Perlman, J. E., Martino, M., and Schapiro, S. J.:
Positive Reinforcement Training Affects Hematologic and Serum Chemistry
Values in Captive Chimpanzees (Pan troglodytes), Am. J. Primatol., 68, 245–256, 2006.
Langsted, A., Freiberg, J. J., Tybjærg-Hansen, A., Schnohr, P., Jensen,
G. B., and Nordestgaard, B. G.: Nonfasting cholesterol and triglycerides and
association with risk of myocardial infarction and total mortality: the
Copenhagen City Heart Study with 31 years of follow-up, J. Intern. Med.,
270, 65–75, 2011.
Lemieux, I., Lamarche, B., Couillard, C., Pascot, A., Cantin, B., Bergeron,
J., Dagenais, G. R., and Després, J. P.: Total cholesterol/HDL
cholesterol ratio vs LDL cholesterol/HDL cholesterol ratio as indices of
ischemic heart disease risk in men: the Quebec Cardiovascular Study, Arch.
Intern. Med., 161, 2685–2692, 2001.
Liao, K. P., Diogo, D., Cui, J., Cai, T., Okada, Y., Gainer, V. S., Murphy,
S. N., Gupta, N., Mirel, D., Ananthakrishnan, A. N., Szolovits, P., Shaw, S.
Y., Raychaudhuri, S., Churchill, S., Kohane, I., Karlson, E. W., and Plenge,
R. M.: Association between low density lipoprotein and rheumatoid arthritis
genetic factors with low density lipoprotein levels in rheumatoid arthritis
and non-rheumatoid arthritis controls, Ann. Rheum. Dis., 73, 1170–1175,
2014.
Libby, P.: Inflammation in atherosclerosis, Nature, 420, 868–874, 2002.
Lowenstine, L. J., McManamon, R., and Terio, K. A.: Comparative Pathology of
Aging Great Apes: Bonobos, Chimpanzees, Gorillas, and Orangutans, Vet.
Pathol., 53, 250–276, 2016.
Maestripieri, D. and Hoffman, C. L.: Chronic stress, allostatic load, and
aging in nonhuman primates, Dev. Psychopathol., 23, 1187–1195, 2011.
Mangiafico, S.: Functions to Support Extension Education Program Evaluation
[R package rcompanion version 2.3.25], available at:
https://CRAN.R-project.org/package=rcompanion (last access: 23 July 2020), 2020.
Manninen, V., Tenkanen, L., Koskinen, P., Huttunen, J. K., Mänttäri,
M., Heinonen, O. P., and Heikki Frick, M.: Joint Effects of Serum Triglyceride
and LDL Cholesterol and HDL Cholesterol Concentrations on Coronary Heart
Disease Risk in the Helsinki Heart Study: Implications for Treatment,
Circulation, 85, 37–45, 1992.
Marcovina, S. and Packard, C. J.: Measurement and meaning of apolipoprotein
AI and apolipoprotein B plasma levels, J. Intern. Med., 259, 437–446,
2006.
Margulis, S. W., Atsalis, S., Bellem, A., and Wielebnowski, N.: Assessment of
Reproductive Behavior and Hormonal Cycles in Geriatric Western Lowland
Gorillas, Zoo Biol., 26, 117–139, 2007.
McClure, H. M., Keeling, M. E., and Guilloud, N. B.: Hematologic and Blood
Chemistry Data for the Gorilla (Gorilla gorilla), Folia Primatol., 18, 300–316, 1972.
McGuire, J. T., Dierenfeld, E. S., Poppenga, R. H., and Brazelton, W. E.:
Plasma Alpha-Tocopherol, Retinol, Cholesterol, and Mineral Concentrations in
Captive Gorillas, J. Med. Primatol., 18, 155–161, 1989.
McManamon, R. and Lowenstine, L.: Cardiovascular Disease in Great Apes, in:
Fowler's Zoo and Wild Animal Medicine, edited by: Miller, R. E. and Fowler, M.,
pp. 408–415, W.B. Saunders, Saint Louis, 2012.
Millán, J., Pintó, X., Muñoz, A., Zúñiga, M.,
Rubiés-Prat, J., Pallardo, L. F., Masana, L., Mangas, A.,
Hernández-Mijares, A., González-Santos, P., Ascaso, J. F., and
Pedro-Botet, J.: Lipoprotein ratios: Physiological significance and clinical
usefulness in cardiovascular prevention, Vasc. Health Risk Manag., 5,
757–765, 2009.
Murphy, H. W., Dennis, P., Devlin, W., Meehan, T., and Kutinsky, I.:
Echocardiographic parameters of captive western lowland gorillas (Gorilla gorilla gorilla), J. Zoo
Wildl. Med., 42, 572–579, 2011.
Murphy, H. W., Danforth, M. D., and Clyde, V. L.: The Great Ape Heart
Project, Int. Zoo Yb., 52, 103–112, 2018.
Murray, S., Kishbaugh, J. C., Hayek, L.-A. C., Kutinsky, I., Dennis, P. M.,
Devlin, W., Hope, K. L., Danforth, M. D., and Murphy, H. W.: Diagnosing
cardiovascular disease in western lowland gorillas (Gorilla gorilla gorilla) with brain natriuretic
peptide, PLoS One, 14, e0214101, https://doi.org/10.1371/journal.pone.0214101, 2019.
Myasoedova, E., Crowson, C. S., Kremers, H. M., Fitz-Gibbon, P. D.,
Therneau, T. M., and Gabriel, S. E.: Total cholesterol and LDL levels
decrease before rheumatoid arthritis, Ann. Rheum. Dis., 69, 1310–1314,
2010.
Nakagawa, S. and Cuthill, I. C.: Effect size, confidence interval and
statistical significance: a practical guide for biologists, Biol. Rev. Camb.
Philos. Soc., 82, 591–605, 2007.
Niaura, R., Stoney, C. M., and Herbert, P. N.: Lipids in psychological
research: the last decade, Biol. Psychol., 34, 1–43, 1992.
Nordestgaard, B. G., Benn, M., Schnohr, P., and Tybjærg-Hansen, A.:
Nonfasting Triglycerides and Risk of Myocardial Infarction, Ischemic Heart
Disease, and Death in Men and Women, JAMA, 298, 299–308, 2007.
Olsson, A. G.: Is high HDL cholesterol always good?, Ann. Med., 41,
11–18, 2009.
Popovich, D. G., Jenkins, D. J. A., Kendall, C. W. C., Dierenfeld, E. S.,
Carroll, R. W., Tariq, N., and Vidgen, E.: The Western Lowland Gorilla Diet
Has Implications for the Health of Humans and Other Hominoids, J. Nutr.,
127, 2000–2005, 1997.
R Core Team: R: A language and environment for statistical computing, R
Foundation for Statistical Computing, Vienna, Austria, 2018.
Richards, S. A.: Testing Ecological Theory Using the Information-Theoretic
Approach: Examples and Cautionary Results, Ecology, 86, 2805–2814,
2005.
Richards, S. A.: Dealing with overdispersed count data in applied ecology,
J. Appl. Ecol., 45, 218–227, 2008.
Richards, S. A., Whittingham, M. J., and Stephens, P. A.: Model selection and
model averaging in behavioural ecology: the utility of the IT-AIC framework,
Behav. Ecol. Sociobiol., 65, 77–89, 2011.
Ridker, P. M., Hennekens, C. H., Buring, J. E., and Rifai, N.: C-Reactive
Protein and Other Markers of Inflammation in the Prediction of
Cardiovascular Disease in Women, N. Engl. J. Med., 342, 836–843, 2000.
Ridker, P. M., Stampfer, M. J., and Rifai, N.: Novel Risk Factors for
Systemic Atherosclerosis: A Comparison of C-Reactive Protein, Fibrinogen,
Homocysteine, Lipoprotein(a), and Standard Cholesterol Screening as
Predictors of Peripheral Arterial Disease, J. Am. Med. Assoc., 285,
2481–2485, 2001.
Russo, G., Pintaudi, B., Giorda, C., Lucisano, G., Nicolucci, A.,
Cristofaro, M. R., Suraci, C., Mulas, M. F., Napoli, A., Rossi, M. C., and
Manicardi, V.: Age- and Gender-Related Differences in LDL-Cholesterol
Management in Outpatients with Type 2 Diabetes Mellitus, Int. J.
Endocrinol., 2015, 957105, https://doi.org/10.1155/2015/957105, 2015.
Sapolsky, R. M.: The Endocrine Stress-Response and Social Status in the Wild
Baboon, Horm. Behav., 16, 279–292, 1982.
Sarwar, N., Danesh, J., Eiriksdottir, G., Sigurdsson, G., Wareham, N.,
Sheila, B., Boekholdt, M., Khaw, K.-T., and Gudnason, V.: Triglycerides and
the Risk of Coronary Heart Disease: 10 158 Incident Cases Among 262 525
Participants in 29 Western Prospective Studies, Circulation, 115, 450–458,
2007.
Schatz, I. J., Masaki, K., Yano, K., Chen, R., Rodriguez, B. L., and Curb, J.
D.: Cholesterol and all-cause mortality in elderly people from the Honolulu
Heart Program: a cohort study, Lancet, 358, 351–355, 2001.
Schmidt, D. A., Ellersieck, M. R., Cranfield, M. R., and Karesh, W. B.:
Cholesterol values in free-ranging gorillas (Gorilla gorilla gorilla and Gorilla beringei) and Bornean orangutans
(Pongo pygmaeus), J. Zoo Wildl. Med., 37, 292–300, 2006.
Seidell, J. C., Cigolini, M., Charzewska, J., Ellsinger, B. M.,
Björntorp, P., Hautvast, J. G., and Szostak, W.: Fat distribution and
gender differences in serum lipids in men and women from four European
communities, Atherosclerosis, 87, 203–210, 1991.
Smith, R. J.: The continuing misuse of null hypothesis significance testing
in biological anthropology, Am. J. Phys. Anthropol., 166, 236–245, 2018.
Species360: Species360, available at: https://www.species360.org/ (last access: 14 October 2020),
2020.
Steptoe, A. and Brydon, L.: Associations between acute lipid stress
responses and fasting lipid levels 3 years later, Health Psychol., 24,
601–607, 2005.
Stoney, C. M., Matthews, K. A., McDonald, R. H., and Johnson, C. A.: Sex
differences in lipid, lipoprotein, cardiovascular, and neuroendocrine
responses to acute stress, Psychophysiology, 25, 645–656, 1988.
Strong, V., Baiker, K., Brennan, M. L., Redrobe, S., Rietkerk, F., Cobb, M.,
and White, K.: A retrospective review of western lowland gorilla (Gorilla gorilla gorilla)
mortality in European zoologic collections between 2004 and 2014, J. Zoo
Wildl. Med., 48, 277–286, 2017.
Strong, V. J., Grindlay, D., Redrobe, S., Cobb, M., and White, K.: A
systematic review of the literature relating to captive great ape morbidity
and mortality, J. Zoo Wildl. Med., 47, 697–710, 2016.
Strong, V. J., Martin, M., Redrobe, S., White, K., and Baiker, K.: A
retrospective review of great ape cardiovascular disease epidemiology and
pathology, Int. Zoo Yb., 52, 113–125, 2018.
Symonds, M. R. E. and Moussalli, A.: A brief guide to model selection,
multimodel inference and model averaging in behavioural ecology using
Akaike's information criterion, Behav. Ecol. Sociobiol., 65, 13–21,
2011.
Treímollières, F. A., Pouilles, J.-M., Cauneille, C., and Ribot, C.:
Coronary heart disease risk factors and menopause: a study in 1684 French
women, Atherosclerosis, 142, 415–423, 1999.
Ulrich-Lai, Y. M. and Herman, J. P.: Neural regulation of endocrine and
autonomic stress responses, Nat. Rev. Neurosci., 10, 397–409, 2009.
van Doornen, L. J., Snieder, H., and Boomsma, D. I.: Serum lipids and
cardiovascular reactivity to stress, Biol. Psychol., 47, 279–297, 1998.
Varki, N., Anderson, D., Herndon, J. G., Pham, T., Gregg, C. J., Cheriyan,
M., Murphy, J., Strobert, E., Fritz, J., Else, J. G., and Varki, A.: Heart
disease is common in humans and chimpanzees, but is caused by different
pathological processes, Evol. Appl., 2, 101–112, 2009.
Videan, E. N., Heward, C. B., Chowdhury, K., Plummer, J., Su, Y., and Cutler,
R. G.: Comparison of biomarkers of oxidative stress and cardiovascular
disease in humans and chimpanzees (Pan troglodytes), Comp. Med., 59, 287–296, 2009.
Wang, X., Magkos, F., and Mittendorfer, B.: Sex differences in lipid and
lipoprotein metabolism: it's not just about sex hormones, J. Clin.
Endocrinol. Metab., 96, 885–893, 2011.
Wasserman, M. D., Chapman, C. A., Milton, K., Goldberg, T. L., and Ziegler,
T. E.: Physiological and Behavioral Effects of Capture Darting on Red
Colobus Monkeys (Procolobus rufomitratus) with a Comparison to Chimpanzee (Pan troglodytes) Predation, Int. J.
Primatol., 34, 1020–1031, 2013.
Weverling-Rijnsburger, A. W. E., Blauw, G. J., Lagaay, A. M., Knook, D. L.,
Meinders, A. E., and Westendorp, R. G. J.: Total cholesterol and risk of
mortality in the oldest old, Lancet, 350, 1119–1123, 1997.
Whitten, P. L., Stavisky, R., Aureli, F., and Russell, E.: Response of Fecal
Cortisol to Stress in Captive Chimpanzees (Pan troglodytes), Am. J. Primatol., 44,
57–69, 1998.
Wickham, H., Chang, W., Henry, L., Pedersen, T. L., Takahashi, K., Wilke, C.,
and Woo, K.: ggplot2: Create Elegant Data Visualisations Using the Grammar
of Graphics. R package version 3.3.0, available at:
https://cran.r-project.org/package=ggplot2, last access: 24 March 2020.
Yunke, Z., Guoping, L., and Zhenyue, C.: Triglyceride-to-HDL cholesterol
ratio. Predictive value for CHD severity and new-onset heart failure, Herz.,
39, 105–110, 2014.
ZIMS: Expected Test Results for western lowland gorillas. Species360
Zoological Information Management System, available at: http://zims.Species360.org, last access: 2 May 2019.
Short summary
Great apes and humans can develop similar health conditions, including heart disease. As lipids predict health risk in humans, we explored whether they do so in gorillas and also examined relationships with age and sex. Multiple sex and age differences were observed. Age, sex, and lower LDL / HDL ratio best predicted morbidity risk, which may be related to arthritis. Unlike humans, in gorillas age and sex alone best predicted cardiac disease, and mortality risk was best predicted only by age.
Great apes and humans can develop similar health conditions, including heart disease. As lipids...
