The role of gut microbiota in the development of obesity in dogs

María del Carmen Camacho-Rea; Diego Alfredo Cardoso Carmona

doi:10.22201/fmvz.24486760e.2023.1205

María del Carmen Camacho-Rea

Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Departamento de Nutrición Animal “Fernando Pérez-Gil Romo”, CDMX, Mexico

https://orcid.org/0000-0002-1858-8071

Diego Alfredo Cardoso Carmona

Universidad Nacional Autónoma de México, Facultad de Estudios Superiores Cuautitlán, Posgrado en Ciencias de la Producción y la Salud Animal, Cuautitlán, México

https://orcid.org/0009-0003-7475-3654

Abstract

The gut microbiota has become the subject of extensive research in the last decades. Intensive research has revealed its role in several functions related to energy metabolism as well as its importance in both health and illness. An imbalance in gut microbiota composition results in dysbiosis, which has been associated with metabolic disorders such as obesity. In the latter context, the gut microbiota appears to mediate the impact of diet on the host body weight. There are many studies in rodents that show profound changes in the composition and metabolic function of the gut microbiota in subjects with obesity, indicating its influence on the development of the problem. Usually, the microbiota of obese dogs has a modified Firmicutes:Bacteroidetes ratio, which returns to normal values after dietary intervention with diet-induced weight loss. The role of the gut microbiota on the development of dog obesity is a recent topic of research, which has been complex due to most of the studies being carried out using commercial extruded diets, which differ in their nutritional composition, resulting in controversial findings. Nevertheless, it has been shown that macro-nutrients from the diet are the most relevant factors that can modulate the microbiota’s composition in a particular way. Moreover, current studies indicate that a personalized nutritional intervention could modify the composition and function of gut microbiota in a positive manner, reducing the development of pathologies such as obesity.

Keywords:

Obesity, Dogs, Intestinal microbiota, Nutritional disorders, Metabolic disorders, environmental factors

DOI: https://doi.org/10.22201/fmvz.24486760e.2023.1205

References

World Health Organization. Obesity and overweight. 2020. https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight

Thiago HA, Vendramini HT, Macedo RV, Zafalon A, Matheus V, Macegoza V, et al. Serum metabolomics analysis reveals that weight loss in obese dogs results in a similar metabolic profile to dogs in ideal body condition. Metabolomics. 2021;17(3):27. doi: 10.1007/s11306-020-01753-4. DOI: https://doi.org/10.1007/s11306-020-01753-4

Kealy RD, Lawler DF, Ballam JM, Lust G, Biery DN, Smith GK, et al. Evaluation of the effect of limited food consumption on radiographic evidence of osteoarthritis in dogs. Journal of the American Veterinary Medical Association. 2000;217(11):1678-1680. doi: 10.2460/javma.2000.217.1678. DOI: https://doi.org/10.2460/javma.2000.217.1678

Lekcharoensuk C, Lulich JP, Osborne CA, Pusoonthornthum R, Allen TA, Koehler LA, et al. Patient and environmental factors associated with calcium oxalate urolithiasis in dogs. Journal of the American Veterinary Medical Association. 2000;217(4):515–519. doi: 10.2460/javma.2000.217.515. DOI: https://doi.org/10.2460/javma.2000.217.515

Lund EM, Armstrong PJ, Kirk CA, Klausner JS. Prevalence and risk factors for obesity in adult dogs from private US veterinary practices. International Journal of Applied Research in Veterinary Medicine. 2006;4(2):177–186.

Bach JF, Rozanski EA, Bedenice D, Chan DL, Freeman LM, Lofgren JLS, et al. Association of expiratory airway dysfunction with marked obesity in healthy adult dogs. American Journal of Veterinary Research. 2007;68(6):670–675. doi: 10.2460/ajvr.68.6.670. DOI: https://doi.org/10.2460/ajvr.68.6.670

Sandøe P, Palmer C, Corr S, Astrup A, Bjørnvad CR. Canine and feline obesity: A one health perspective. Veterinary Record. 2014;175(24):610–616. doi: 10.1136/vr.g7521. DOI: https://doi.org/10.1136/vr.g7521

Salt C, Morris PJ, Wilson D, Lund EM, German AJ. Association between life span and body condition in neutered client owned dogs. Journal of Veterinary Internal Medicine. 2019;33(1):89-99. doi: 10.1111/jvim.15367. DOI: https://doi.org/10.1111/jvim.15367

Rafan E, Dennis RJ, O'Donovan CJ, Becker JM, Scott RA, Smith SP, et al. A deletion in the canine POMC gene is associated with weight and appetite in obesity-prone Labrador retriever dogs. Cell Metabolism. 2016;23(5):893–900. doi: 10.1016/j.cmet.2016.04.012. DOI: https://doi.org/10.1016/j.cmet.2016.04.012

Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the National Academy of Sciences. 2004;101(44):15718–15723. doi: 10.1073/pnas.0407076101. DOI: https://doi.org/10.1073/pnas.0407076101

Rosenbaum M, Knight R, Leibel RL. The gut microbiota in human energy homeostasis and obesity. Trends in Endocrinology and Metabolism. 2015;26(9):493–501. doi: 10.1016/j.tem.2015.07.002. DOI: https://doi.org/10.1016/j.tem.2015.07.002

Ghazalpour A, Cespedes I, Bennett BJ, Allayee H. Expanding role of gut microbiota in lipid metabolism. Current Opinions on Lipidology. 2016;27(2):141-147. doi: 10.1097/MOL.0000000000000278. DOI: https://doi.org/10.1097/MOL.0000000000000278

Boulangé L, Neves AL, Chilloux J, Nicholson JK, Dumas ME. Impact of the gut microbiota on inﬂammation, obesity, and metabolic disease. Genome Medicine. 2016;8(42):1–12. DOI: https://doi.org/10.1186/s13073-016-0303-2

Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI. The Human Microbiome Project. Nature. 2007;449(7164):804–810. doi: 10.1038/nature06244. DOI: https://doi.org/10.1038/nature06244

Honneffer JB, Minamoto Y, Suchodolski JS. Microbiota alterations in acute and chronic gastrointestinal inflammation of cats and dogs. World Journal of Gastroenterology. 2014;20(44):16489–16497. doi: 10.3748/wjg.v20.i44.16489. DOI: https://doi.org/10.3748/wjg.v20.i44.16489

Abenavoli L, Scarpellini E, Colica C, Boccuto L, Salehi B, Sharifi-Rad J, et al. Gut microbiota and obesity: a role for probiotics. Nutrients. 2019;11(11):2690. doi: 10.3390/nu11112690. DOI: https://doi.org/10.3390/nu11112690

Gao R, Zhu C, Li H, Yin M, Pan C, Huang L, et al. Dysbiosis signatures of gut microbiota along the sequence from healthy, young patients to those with overweight and obesity. Obesity. 2018;26(2):351–361. doi: 10.1002/oby.22088. DOI: https://doi.org/10.1002/oby.22088

Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell. 2012;148(6):1258–1270. doi: 10.1016/j.cell.2012.01.035. DOI: https://doi.org/10.1016/j.cell.2012.01.035

Hand D, Wallis C, Colyer A, Penn CW. Pyrosequencing the canine faecal microbiota: breadth and depth of biodiversity. PLoS One. 2013;8(1):e53115. doi: 10.1371/journal.pone.0053115. DOI: https://doi.org/10.1371/journal.pone.0053115

Middelbos IS, Vester Boler BM, Qu A, White BA, Swanson KS, Fahey GC Jr. Phylogenetic characterization of fecal microbial communities of dogs fed diets with or without supplemental dietary ﬁber using 454 pyrosequencing. PLoS One. 2010;5(3):e9768. doi: 10.1371/journal.pone.0009768. DOI: https://doi.org/10.1371/journal.pone.0009768

Handl S, Dowd SE, Garcia-Mazcorro JF, Steiner JM, Suchodolski JS. Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiological Ecology. 2011;76(2):301–310. doi: 10.1111/j.1574-6941.2011.01058.x. DOI: https://doi.org/10.1111/j.1574-6941.2011.01058.x

Vazquez-Baeza Y, Hyde ER, Suchodolski JS, Knight R. Dog and human inflammatory bowel disease rely on overlapping yet distinct dysbiosis networks. Nature Microbiology. 2016;1:16177. doi: 10.1038/nmicrobiol.2016.177. DOI: https://doi.org/10.1038/nmicrobiol.2016.177

Garcia-Mazcorro JF, Dowd SE, Poulsen J, Steiner JM, Suchodolski JS. Abundance and short-term temporal variability of fecal microbiota in healthy dogs. Microbiology Open. 2012;1(3):340–347. doi: 10.1002/mbo3.36. DOI: https://doi.org/10.1002/mbo3.36

Switonski M, Mankowska M. Dog obesity–The need for identifying predisposing genetic markers. Research in Veterinary Science. 2013;95(3):831–836. doi: 10.1016/j.rvsc.2013.08.015. DOI: https://doi.org/10.1016/j.rvsc.2013.08.015

Bäckhed F, Fraser CM, Ringel Y, Sanders ME, Sartor RB, Sherman PM, et al. Deﬁning a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host and Microbe. 2012;12(5):611–622. doi: 10.1016/j.chom.2012.10.012. DOI: https://doi.org/10.1016/j.chom.2012.10.012

Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–1031. doi: 10.1038/nature05414. DOI: https://doi.org/10.1038/nature05414

David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563. doi: 10.1038/nature12820. DOI: https://doi.org/10.1038/nature12820

Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–1023. doi: 10.1038/4441022a. DOI: https://doi.org/10.1038/4441022a

Duan M, Wang Y, Zhang Q, Zou R, Guo M, Zheng H. Characteristics of gut microbiota in people with obesity. PLoS One. 2021;16(8). eNumber: e0255446. doi: 10.1371/journal.pone.0255446. DOI: https://doi.org/10.1371/journal.pone.0255446

Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI et al. Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences. 2005;102(31):11070–11075. doi: 10.1073/pnas.0504978102. DOI: https://doi.org/10.1073/pnas.0504978102

Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host and Microbe. 2008;3(4):213–223. doi: 10.1016/ j.chom.2008.02.015. DOI: https://doi.org/10.1016/j.chom.2008.02.015

Rizzatti G, Lopetuso LR, Gibiino G, Binda C, Gasbarrini A. Proteobacteria: a common factor in human diseases. BioMed Research International 2017;2017:9351507. doi: 10.1155/2017/9351507. DOI: https://doi.org/10.1155/2017/9351507

Cani PD, Osto M, Geurts L, Everard A. Involvement of gut microbiota in the development of low-grade inflammation and type 2 diabetes associated with obesity. Gut Microbes. 2012;3(4):279-288. doi: 10.4161/gmic.19625. DOI: https://doi.org/10.4161/gmic.19625

Handl S, German AJ, Holden SL, Dowd SE, et al. Faecal microbiota in lean and obese dogs. FEMS Microbiology Ecology. 2013;84(2):332−343. doi: 10.1111/1574-6941.12067. DOI: https://doi.org/10.1111/1574-6941.12067

Benson AK, Kelly SA, Legge R, Ma F, Low SJ, Kim J, Zhang M, et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Sciences. 2010;107(44):18933–18938. doi: 10.1073/pnas.1007028107. DOI: https://doi.org/10.1073/pnas.1007028107

Xu Z, Knight R. Dietary effects on human gut microbiome diversity. British Journal of Nutrition. 2015;113(Suppl 1):S1–S5. doi: 10.1017/S0007114514004127. DOI: https://doi.org/10.1017/S0007114514004127

Suchodolski JS, Ruaux CG, Steiner JM, Fetz K, Williams DA. Assessment of the qualitative variation in bacterial microflora among compartments of the intestinal tract of dogs by use of a molecular fingerprinting technique. American Journal of Veterinary Research. 2005;66(9):1556−1562. doi: 10.2460/ajvr.2005.66.1556. DOI: https://doi.org/10.2460/ajvr.2005.66.1556

Alexander C, Cross TL, Devendran S, Neumer F, Theis S, Ridlon JM, et al. Eﬀects of prebiotic inulin-type fructans on blood metabolite and hormone concentrations and faecal microbiota and metabolites in overweight dogs. British Journal of Nutrition. 2018;120(6):711–720. doi: 10.1017/S00071145180 01952. DOI: https://doi.org/10.1017/S0007114518001952

Bermingham EN, Maclean P, Thomas DG, Cave NJ, Young W. Key bacterial families (Clostridiaceae, Erysipelotrichaceae and Bacteroidaceae) are related to the digestion of protein and energy in dogs. PeerJ. 2017;5:e3019. doi: 10.7717/peerj.3019. DOI: https://doi.org/10.7717/peerj.3019

Bresciani F, Minamoto Y, Suchodolski JS, Galiazzo G, Vecchiato CG, Pinna C, et al. Eﬀect of an extruded animal protein-free diet on fecal microbiota of dogs with food-responsive enteropathy. Journal Veterinary Internal Medicine. 2018;32(6):1903–1190. doi: 10.1111/jvim.15227. DOI: https://doi.org/10.1111/jvim.15227

Schauf S, de la Fuente G, Newbold CJ, Salas-Mani A, Torre C, Abecia L, et al. Eﬀect of dietary fat to starch content on fecal microbiota composition and activity in dogs. Journal of Animal Science. 2018;96(9):3684–3698. doi: 10.1093/jas/sky264. DOI: https://doi.org/10.1093/jas/sky264

Herstad KMV, Gajardo K, Bakke AM, Moe L, Ludvigsen J, Rudi K, et al. A diet change from dry food to beef induces reversible changes on the faecal microbiota in healthy, adult client-owned dogs. BMC Veterinary Research. 2017;13(147):1-13. doi: 10.1186/s12917-017-1073-9. DOI: https://doi.org/10.1186/s12917-017-1073-9

Marchesi JR, Adams DH, Fava F, Hermes GDA, Hirschfield GM, Hold G, et al. The gut microbiota and host health: a new clinical frontier. Gut. 2016;65(2):330−339. doi: 10.1136/gutjnl-2015-309990. DOI: https://doi.org/10.1136/gutjnl-2015-309990

Schmitz S, Suchodolski J. Understanding the canine intestinal microbiota and its modiﬁcation by pro-, pre- and synbiotics- what is the evidence? Veterinary Medicine and Science. 2016;2(2):71–94. doi: 10.1002/vms3.17. DOI: https://doi.org/10.1002/vms3.17

Gagné JW, Wakshlag JJ, Simpson KW, Dowd SE, Latchman S, Brown DA, et al. Eﬀects of a synbiotic on fecal quality, short-chain fatty acid concentrations, and the microbiome of healthy sled dogs [PDF]. BMC Veterinary Research. 2013;9(246):1–10. doi: 10.1186/1746-6148-9-246. DOI: https://doi.org/10.1186/1746-6148-9-246

Maynard C, Weinkove D. The gut microbiota and ageing. In: J Harris, V Korolchuk, editors. Biochemistry and Cell Biology of Ageing: Part I Biomedical Science. Subcellular Biochemistry. Vol. 90. Singapore: Springer; 2018. pp. 351-371. doi: 10.1007/978-981-13-2835-0_12. DOI: https://doi.org/10.1007/978-981-13-2835-0_12

Guard BC, Suchodolski JS. Horse Species Symposium: Canine intestinal microbiology and metagenomics: from phylogeny to function. Journal of Animal Science. 2016;94(6):2247–2261. doi: 10.2527/jas.2015-0029. DOI: https://doi.org/10.2527/jas.2015-0029

Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56(7):1761-1772. doi: 10.2337/db06-1491. DOI: https://doi.org/10.2337/db06-1491

Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GG, Neyrinck AM, et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes. 2011;60(11):2775-2786. doi: 10.2337/db11-0227. DOI: https://doi.org/10.2337/db11-0227

Murphy EF, Cotter PD, Hogan A, O'Sullivan O, Joyce A, Fouhy F, et al. Divergent metabolic outcomes arising from targeted manipulation of the gut microbiota in diet-induced obesity. Gut. 2013;62(2):220-226. doi: 10.1136/gutjnl-2011-300705. DOI: https://doi.org/10.1136/gutjnl-2011-300705

Fildes A, Charlton J, Rudisill C, Littlejohns P, Prevost AT, Gulliford MC. Probability of an obese person attaining normal body weight: cohort study using electronic health records. American Journal of Public Health. 2015;105(9):e54-e59. doi: 10.2105/AJPH.2015.302773. DOI: https://doi.org/10.2105/AJPH.2015.302773

German AJ, Titcomb JM, Holden SL, Queau Y, Morris PJ, Biourge V. Cohort study of the success of controlled weight loss programs for obese dogs. Journal of Veterinary Internal Medicine. 2015;29(6):1547–1555. doi: 10.1111/jvim.13629. DOI: https://doi.org/10.1111/jvim.13629

Duncan S, Lobley G, Holtrop G. Ince J, Johnstone AM, Louis P, et al. Human colonic microbiota associated with diet, obesity and weight loss. International Journal of Obesity. 2008;32(11):1720–1724. doi: 10.1038/ijo.2008.155. DOI: https://doi.org/10.1038/ijo.2008.155

Cotillard A, Kennedy S, Kong L, Prifti E, Pons N, Le Chatelier E, et al. Dietary intervention impact on gut microbial gene richness. Nature. 2013;500:585–588. doi: 10.1038/nature12480. DOI: https://doi.org/10.1038/nature12480

Mori A, Goto A, Kibe R, Oda H, Kataoka Y, Sako T. Comparison of the effects of four commercially available prescription diet regimens on the fecal microbiome in healthy dogs. Journal of Veterinary Medical Science. 2019;81(12):1783-1790. doi: 10.1292/jvms.19-0055. DOI: https://doi.org/10.1292/jvms.19-0055

Kieler IN, Kamal S, Vitger AD, Nielsen DS, Lauridsen C, Bjornvad CR. Gut microbiota composition may relate to weight loss rate in obese pet dogs. Veterinary Medicine and Science. 2017;3(4):252-262. doi: 10.1002/vms3.80. DOI: https://doi.org/10.1002/vms3.80

Santacruz A, Marcos A, Wärnberg J, Martí A, Martin-Matillas M, Campoy C, et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity. 2009;17(10):1906-1915. doi: 10.1038/oby.2009.112. DOI: https://doi.org/10.1038/oby.2009.112

License

Veterinaria México OA by Facultad de Medicina Veterinaria y Zootecnia - Universidad Nacional Autónoma de México is licensed under a Creative Commons Attribution 4.0 International Licence.
Based on a work at http://www.revistas.unam.mx

All articles in Veterinaria México OA re published under the Creative Commons Attribution 4.0 Unported (CC-BY 4.0). With this license, authors retain copyright but allow any user to share, copy, distribute, transmit, adapt and make commercial use of the work, without needing to provide additional permission as long as appropriate attribution is made to the original author or source.

By using this license, all Veterinaria México OAarticles meet or exceed all funder and institutional requirements for being considered Open Access.

Authors cannot use copyrighted material within their article unless that material has also been made available under a similarly liberal license.

Article Sidebar

Main Article Content

Abstract

Article Details

References

License