Proceedings of the Royal Society B: Biological Sciences
Restricted accessResearch articles

Canaries in the coal mine: a cross-species analysis of the plurality of obesity epidemics

Published:https://doi.org/10.1098/rspb.2010.1890

    A dramatic rise in obesity has occurred among humans within the last several decades. Little is known about whether similar increases in obesity have occurred in animals inhabiting human-influenced environments. We examined samples collectively consisting of over 20 000 animals from 24 populations (12 divided separately into males and females) of animals representing eight species living with or around humans in industrialized societies. In all populations, the estimated coefficient for the trend of body weight over time was positive (i.e. increasing). The probability of all trends being in the same direction by chance is 1.2 × 10−7. Surprisingly, we find that over the past several decades, average mid-life body weights have risen among primates and rodents living in research colonies, as well as among feral rodents and domestic dogs and cats. The consistency of these findings among animals living in varying environments, suggests the intriguing possibility that the aetiology of increasing body weight may involve several as-of-yet unidentified and/or poorly understood factors (e.g. viral pathogens, epigenetic factors). This finding may eventually enhance the discovery and fuller elucidation of other factors that have contributed to the recent rise in obesity rates.

    References

    • 1
      Ogden C. L., Carroll M. D., Curtin L. R., McDowell M. A., Tabak C. J.& Flegal K. M.. 2006Prevalence of overweight and obesity in the United States, 1999–2004. J. Am. Med. Assoc. 295, 1549–1555.doi:10.1001/jama.295.13.1549 (doi:10.1001/jama.295.13.1549). Crossref, ISIGoogle Scholar
    • 2
      Helmchen L. A.& Henderson R. M.. 2004Changes in the distribution of body mass index of white US men, 1890–2000. Ann. Hum. Biol. 31, 174–181.doi:10.1080/03014460410001663434 (doi:10.1080/03014460410001663434). Crossref, PubMed, ISIGoogle Scholar
    • 3
      Astrup A. V., Rossner S.& Sorensen T. I.. 2006Alternative causes of obesity. Ugeskr Laeger 168, 135–137. PubMedGoogle Scholar
    • 4
      Bray G. A.& Champagne C. M.. 2005Beyond energy balance: there is more to obesity than kilocalories. J. Am. Diet Assoc. 105((5 Suppl. 1)), S17–S23. Crossref, PubMedGoogle Scholar
    • 5
      Eisenmann J. C.. 2006Insight into the causes of the recent secular trend in pediatric obesity: common sense does not always prevail for complex, multi-factorial phenotypes. Prev. Med. 42, 329–335.doi:10.1016/j.ypmed.2006.02.002 (doi:10.1016/j.ypmed.2006.02.002). Crossref, PubMed, ISIGoogle Scholar
    • 6
      Keith S. W., et al.2006Putative contributors to the secular increase in obesity: exploring the roads less traveled. Int. J. Obes. (Lond.) 30, 1585–1594.doi:10.1038/sj.ijo.0803326 (doi:10.1038/sj.ijo.0803326). Crossref, PubMed, ISIGoogle Scholar
    • 7
      McAllister E. J., et al.2009Ten putative contributors to the obesity epidemic. Crit. Rev. Food Sci. Nutr. 49, 868–913.doi:10.1080/10408390903372599 (doi:10.1080/10408390903372599). Crossref, PubMed, ISIGoogle Scholar
    • 8
      Van der Schalie W. H., et al.1999Animals as sentinels of human health hazards of environmental chemicals. Environ. Health Perspect. 107, 309–315.doi:10.1289/ehp.99107309 (doi:10.1289/ehp.99107309). Crossref, PubMed, ISIGoogle Scholar
    • 9
      Vasselli J. R., Weindruch R., Heymsfield S. B., Pi-Sunyer F. X., Boozer C. N., Yi N., Wang C., Pietrobelli A.& Allison D. B.. 2005Intentional weight loss reduces mortality rate in a rodent model of dietary obesity. Obes. Res. 13, 693–702.doi:10.1038/oby.2005.78 (doi:10.1038/oby.2005.78). Crossref, PubMedGoogle Scholar
    • 10
      Coffey C. S., Gadbury G. L., Fontaine K. R., Wang C., Weindruch R.& Allison D. B.. 2005The effects of intentional weight loss as a latent variable problem. Stat. Med. 24, 941–954.doi:10.1002/sim.1964 (doi:10.1002/sim.1964). Crossref, PubMed, ISIGoogle Scholar
    • 11
      Colman R. J., Beasley T. M., Allison D. B.& Weindruch R.. 2008Attenuation of sarcopenia by dietary restriction in rhesus monkeys. J. Gerontol. A Biol. Sci. Med. Sci. 63, 556–559. Crossref, PubMed, ISIGoogle Scholar
    • 12
      Davis D. E.. 1949A phenotypical difference in growth of wild rats. Growth 13, 1–6. PubMedGoogle Scholar
    • 13
      Glass G. E., Childs J. E., Korch G. W.& LeDuc J. W.. 1989Comparative ecology and social interactions of Norway rats Rattus norvegicus. Occasional Papers of the Museum of Natural History, vol. 130, pp. 1–33. Baltimore, MD: University of Kansas. Google Scholar
    • 14
      Heinze G.. 2006A comparative investigation of methods for logistic regression with separated or nearly separated data. Stat. Med. 25, 4216–4226.doi:10.1002/sim.2687 (doi:10.1002/sim.2687). Crossref, PubMed, ISIGoogle Scholar
    • 15
      Post E., Stenseth N. C., Langvatn R.& Fromentin J. M.. 1997Global climate change and phenotypic variation among red deer cohorts. Proc. R. Soc. Lond. B 264, 1317–1324.doi:10.1098/rspb.1997.0182 (doi:10.1098/rspb.1997.0182). Link, ISIGoogle Scholar
    • 16
      German A. J.. 2006The growing problem of obesity in dogs and cats. J. Nutr. 136((Suppl. 7)), 1940S–1946S. Crossref, PubMed, ISIGoogle Scholar
    • 17
      Thatcher C. D., Pleasant R. S., Geor R. J., Elvinger F., Negrin K. A., Franklin J., Gay L.& Werre S. R.. 2009Prevalence of obesity in mature horses: an equine body condition study. J. Anim. Physiol. Anim. Nutr. 92, 222.doi:10.1111/j.1439-0396.2007.00789_8.x (doi:10.1111/j.1439-0396.2007.00789_8.x). CrossrefGoogle Scholar
    • 18
      Nohynek G. J., Longeart L., Geffray B., Provost J. P.& Lodola A.. 1993Fat, frail and dying young: survival, body weight and pathology of the Charles River Sprague–Dawley-derived rat prior to and since the introduction of the VAFR variant in 1988. Hum. Exp. Toxicol. 12, 87–98.doi:10.1177/096032719301200201 (doi:10.1177/096032719301200201). Crossref, PubMed, ISIGoogle Scholar
    • 19
      Ley R. E., Turnbaugh P. J., Klein S.& Gordon J. I.. 2006Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023.doi:10.1038/4441022a (doi:10.1038/4441022a). Crossref, PubMed, ISIGoogle Scholar
    • 20
      Vijay-Kumar M., et al.2010Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science 328, 228–231.doi:10.1126/science.1179721 (doi:10.1126/science.1179721). Crossref, PubMed, ISIGoogle Scholar
    • 21
      Kim J., Peterson K. E., Scanlon K. S., Fitzmaurice G. M., Must A., Oken E., Rifas-Shiman S. L., Rich-Edwards J. W.& Gillman M. W.. 2006Trends in overweight from 1980 through 2001 among preschool-aged children enrolled in a health maintenance organization. Obesity (Silver Spring) 14, 1107–1112.doi:10.1038/oby.2006.126 (doi:10.1038/oby.2006.126). Crossref, PubMed, ISIGoogle Scholar
    • 22
      Childs J. E.. 1986Size-dependent predation on rats (Rattus norvegicus) by house cats (Felis catus) in an urban setting. J. Mammal. 67, 196–199.doi:10.2307/1381025 (doi:10.2307/1381025). Crossref, ISIGoogle Scholar
    • 23
      Glass G. E., Gardner-Santana L. C., Holt R. D., Chen J., Shields T. M., Roy M., Schachterle S.& Klein S. L.. 2009Trophic garnishes: cat–rat interactions in an urban environment. PLoS ONE 4, e5794.doi:10.1371/journal.pone.0005794 (doi:10.1371/journal.pone.0005794). Crossref, PubMed, ISIGoogle Scholar
    • 24
      Elobeid M. A.& Allison D. B.. 2008Putative environmental-endocrine disruptors and obesity: a review. Curr. Opin. Endocrinol. Diabetes Obes. 15, 403–408. Crossref, PubMedGoogle Scholar
    • 25
      Dhurandhar N. V., et al.2002Human adenovirus Ad-36 promotes weight gain in male rhesus and marmoset monkeys. J. Nutr. 132, 3155–3160. Crossref, PubMed, ISIGoogle Scholar
    • 26
      Atkinson R. L., Dhurandhar N. V., Allison D. B., Bowen R. L., Israel B. A., Albu J. B.& Augustus A. S.. 2005Human adenovirus-36 is associated with increased body weight and paradoxical reduction of serum lipids. Int. J. Obes. (Lond.) 29, 281–286.doi:10.1038/sj.ijo.0802830 (doi:10.1038/sj.ijo.0802830). Crossref, PubMed, ISIGoogle Scholar
    • 27
      Gluckman P. D.& Hanson M. A.. 2008Developmental and epigenetic pathways to obesity: an evolutionary-developmental perspective. Int. J. Obes. (Lond.) 32((Suppl. 7)), S62–S71. Crossref, PubMed, ISIGoogle Scholar
    • 28
      Waterland R. A.& Michels K. B.. 2007Epigenetic epidemiology of the developmental origins hypothesis. Annu. Rev. Nutr. 27, 363–388.doi:10.1146/annurev.nutr.27.061406.093705 (doi:10.1146/annurev.nutr.27.061406.093705). Crossref, PubMed, ISIGoogle Scholar
    • 29
      Speakman J. R.. 2007A nonadaptive scenario explaining the genetic predisposition to obesity: the ‘predation release’ hypothesis. Cell Metab. 6, 5–12.doi:10.1016/j.cmet.2007.06.004 (doi:10.1016/j.cmet.2007.06.004). Crossref, PubMed, ISIGoogle Scholar
    • 30
      Ozgul A., Tuljapurkar S., Benton T. G., Pemberton J. M., Clutton-Brock T. H.& Coulson T.. 2009The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325, 464–467.doi:10.1126/science.1173668 (doi:10.1126/science.1173668). Crossref, PubMed, ISIGoogle Scholar
    • 31
      Ozgul A., Childs D. Z., Oli M. K., Armitage K. B., Blumstein D. T., Olson L. E., Tuljapurkar S.& Coulson T.. 2010Coupled dynamics of body mass and population growth in response to environmental change. Nature 466, 482–485.doi:10.1038/nature09210 (doi:10.1038/nature09210). Crossref, PubMed, ISIGoogle Scholar
    • 32
      Keenan K. P.. 1996Commentary. The uncontrolled variable in risk assessment: ad libitum overfed rodents–fat, facts and fiction. Toxicol. Pathol. 24, 376–383.doi:10.1177/019262339602400315 (doi:10.1177/019262339602400315). Crossref, PubMed, ISIGoogle Scholar
    • 33
      Keenan K. P., Laroque P., Ballam G. C., Soper K. A., Dixit R., Mattson B. A., Adams S. P.& Coleman J. B.. 1996The effects of diet, ad libitum overfeeding, and moderate dietary restriction on the rodent bioassay: the uncontrolled variable in safety assessment. Toxicol. Pathol. 24, 757–768.doi:10.1177/019262339602400620 (doi:10.1177/019262339602400620). Crossref, PubMed, ISIGoogle Scholar
    • 34
      Turturro A., Leakey J., Allaben W. T.& Hart R. W.. 1997Fat (and thin) rats distort results. Nature 389, 326.doi:10.1038/38590 (doi:10.1038/38590). Crossref, PubMed, ISIGoogle Scholar
    • 35
      Keenan K. P., Laroque P.& Dixit R.. 1998Need for dietary control by caloric restriction in rodent toxicology and carcinogenicity studies. J. Toxicol. Environ. Health B Crit. Rev. 1, 135–148. Crossref, PubMed, ISIGoogle Scholar