Movatterモバイル変換

[0]ホーム
URL:

Skip to main content

Advertisement

Springer Nature Link
Log in

Species-Spanning Echocardiography: Cardiovascular Insights from Across the Animal Kingdom

  • Echocardiography (JM Gardin and AH Waller, Section Editors)
  • Published:
Current Cardiology Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

The objective of this review is to present comparative echocardiography as a source of insights for human cardiovascular medicine.

Recent Findings

We present echocardiographic examples of high impact human cardiovascular pathologies, including valvular, vascular, conduction, and myocardial disorders, in a wide range of species in varying environments. Unique features associated with comparative echocardiographic assessments are linked to human cardiology, including natural animal models of resistance and vulnerability.

Summary

The cardiovascular vulnerabilities and strengths of other species can be a source of invaluable insights for human healthcare professionals. Echocardiography is playing a key role in bridging human and veterinary cardiology. Consequently, species-spanning echocardiography can deliver novel insights for human medicine.

This is a preview of subscription content,log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from ¥17,985 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price includes VAT (Japan)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Saunders LZ. Virchow’s contributions to veterinary medicine: celebrated then, forgotten now. Vet Pathol. 2000;37:199–207.

    Article CAS PubMed  Google Scholar 

  2. Jensen B, Wang T, Christoffels VM, Moorman AF. Evolution and development of the building plan of the vertebrate heart. Biochim Biophys Acta. 1833;2013:783–94.

    Google Scholar 

  3. Fleming JM, Creevy KE, Promislow DE. Mortality in North American dogs from 1984 to 2004: an investigation into age-, size-, and breed-related causes of death. J Vet Intern Med. 2011;25:187–98.

    Article CAS PubMed  Google Scholar 

  4. Freeman LM, Rush JE, Stern JA, Huggins GS, Maron MS. Feline hypertrophic cardiomyopathy: a spontaneous large animal model of human HCM. Cardiol Res. 2017;8:139–42.

    Article PubMed PubMed Central  Google Scholar 

  5. Ostrander EA. Franklin H. Epstein Lecture. Both ends of the leash--the human links to good dogs with bad genes. N Engl J Med. 2012;367:636–46.

    Article CAS PubMed PubMed Central  Google Scholar 

  6. Borgarelli M, Buchanan JW. Historical review, epidemiology and natural history of degenerative mitral valve disease. J Vet Cardiol. 2012;14:93–101.

    Article PubMed  Google Scholar 

  7. Fox PR. Pathology of myxomatous mitral valve disease in the dog. J Vet Cardiol. 2012;14:103–26.

    Article PubMed  Google Scholar 

  8. Menciotti G, Borgarelli M. Review of diagnostic and therapeutic approach to canine myxomatous mitral valve disease. Vet Sci. 2017;4:47.

  9. Pedersen HD, Häggström J. Mitral valve prolapse in the dog: a model of mitral valve prolapse in man. Cardiovasc Res. 2000;47:234–43.

    Article CAS PubMed  Google Scholar 

  10. Meurs KM, Friedenberg SG, Kolb J, Saripalli C, Tonino P, Woodruff K, et al. A missense variant in the titin gene in Doberman pinscher dogs with familial dilated cardiomyopathy and sudden cardiac death. Hum Genet. 2019;138:515–24.

    Article CAS PubMed  Google Scholar 

  11. • Stern JA, Ueda Y. Inherited cardiomyopathies in veterinary medicine. Pflugers Arch. 2019;471:745–53This review presents insights on naturally-occurring cardiomyopathies in companion animals and primates from a One Health perspective and implications of 'large animal' models for translational research. It emphasizes the reciprocal value of collaborations in human and veterinary cardiology.

    Article CAS PubMed  Google Scholar 

  12. Kittleson MD, Meurs KM, Harris SP. The genetic basis of hypertrophic cardiomyopathy in cats and humans. J Vet Cardiol. 2015;17(Suppl 1):S53–73.

    Article PubMed PubMed Central  Google Scholar 

  13. Detweiler DK, Patterson DF. The prevalence and types of cardiovascular disease in dogs. Ann N Y Acad Sci. 1965;127:481–516.

    Article CAS PubMed  Google Scholar 

  14. Schrope DP. Prevalence of congenital heart disease in 76,301 mixed-breed dogs and 57,025 mixed-breed cats. J Vet Cardiol. 2015;17:192–202.

    Article PubMed  Google Scholar 

  15. Oyama MA, Elliott C, Loughran KA, Kossar AP, Castillero E, Levy RJ, et al. Comparative pathology of human and canine myxomatous mitral valve degeneration: 5HT and TGF-β mechanisms. Cardiovasc Pathol. 2020;46:107196.

    Article CAS PubMed PubMed Central  Google Scholar 

  16. Markby GR, Summers KM, MacRae VE, Corcoran BM. Comparative transcriptomic profiling and gene expression for myxomatous mitral valve disease in the dog and human. Vet Sci. 2017;4:34.

  17. Pedersen HD, Lorentzen KA, Kristensen BO. Echocardiographic mitral valve prolapse in cavalier King Charles spaniels: epidemiology and prognostic significance for regurgitation. Vet Rec. 1999;144:315–20.

    Article CAS PubMed  Google Scholar 

  18. Menciotti G, Borgarelli M, Aherne M, Camacho P, Häggström J, Ljungvall I, et al. Comparison of the mitral valve morphologies of Cavalier King Charles Spaniels and dogs of other breeds using 3D transthoracic echocardiography. J Vet Intern Med. 2018;32:1564–9.

    Article PubMed PubMed Central  Google Scholar 

  19. Keene BW, Atkins CE, Bonagura JD, Fox PR, Häggström J, Fuentes VL, et al. ACVIM consensus guidelines for the diagnosis and treatment of myxomatous mitral valve disease in dogs. J Vet Intern Med. 2019;33:1127–40.

    Article PubMed PubMed Central  Google Scholar 

  20. Madsen MB, Olsen LH, Häggström J, et al. Identification of 2 loci associated with development of myxomatous mitral valve disease in Cavalier King Charles Spaniels. J Hered. 2011;102(Suppl 1):S62–7.

    Article PubMed  Google Scholar 

  21. Meurs KM, Friedenberg SG, Williams B, Keene BW, Atkins CE, Adin D, et al. Evaluation of genes associated with human myxomatous mitral valve disease in dogs with familial myxomatous mitral valve degeneration. Vet J. 2018;232:16–9.

    Article CAS PubMed  Google Scholar 

  22. Tidholm A, Häggström J, Borgarelli M, Tarducci A. Canine idiopathic dilated cardiomyopathy. Part I: aetiology, clinical characteristics, epidemiology and pathology. Vet J. 2001;162:92–107.

    Article CAS PubMed  Google Scholar 

  23. Sleeper MM, Henthorn PS, Vijayasarathy C, Dambach DM, Bowers T, Tijskens P, et al. Dilated cardiomyopathy in juvenile Portuguese Water Dogs. J Vet Intern Med. 2002;16:52–62.

    Article PubMed  Google Scholar 

  24. Sleeper MM, Bish LT, Sweeney HL. Gene therapy in large animal models of human cardiovascular genetic disease. ILAR J. 2009;50:199–205.

    Article CAS PubMed  Google Scholar 

  25. Freeman LM, Rush JE. Nutrition and cardiomyopathy: lessons from spontaneous animal models. Curr Heart Fail Rep. 2007;4:84–90.

    Article CAS PubMed  Google Scholar 

  26. Freeman LM, Stern JA, Fries R, Adin DB, Rush JE. Diet-associated dilated cardiomyopathy in dogs: what do we know. J Am Vet Med Assoc. 2018;253:1390–4.

    Article PubMed  Google Scholar 

  27. McCauley SR, Clark SD, Quest BW, Streeter RM, Oxford EM. Review of canine dilated cardiomyopathy in the wake of diet-associated concerns. J Anim Sci. 2020;98:skaa155.

  28. Wess G, Schulze A, Butz V, Simak J, Killich M, Keller LJM, et al. Prevalence of dilated cardiomyopathy in Doberman Pinschers in various age groups. J Vet Intern Med. 2010;24:533–8.

    Article CAS PubMed  Google Scholar 

  29. Smucker ML, Kaul S, Woodfield JA, Keith JC, Manning SA, Gascho JA. Naturally occurring cardiomyopathy in the Doberman pinscher: a possible large animal model of human cardiomyopathy. J Am Coll Cardiol. 1990;16:200–6.

    Article CAS PubMed  Google Scholar 

  30. Simpson S, Edwards J, Ferguson-Mignan TF, Cobb M, Mongan NP, Rutland CS. Genetics of human and canine dilated cardiomyopathy. Int J Genomics. 2015;2015:204823.

    Article PubMed PubMed Central CAS  Google Scholar 

  31. Bolfer L, Estrada AH, Larkin C, Conlon TJ, Lourenco F, Taggart K, et al. Functional consequences of PDK4 deficiency in Doberman Pinscher fibroblasts. Sci Rep. 2020;10:3930.

    Article CAS PubMed PubMed Central  Google Scholar 

  32. Meurs KM, Lahmers S, Keene BW, White SN, Oyama MA, Mauceli E, et al. A splice site mutation in a gene encoding for PDK4, a mitochondrial protein, is associated with the development of dilated cardiomyopathy in the Doberman pinscher. Hum Genet. 2012;131:1319–25.

    Article CAS PubMed  Google Scholar 

  33. Posafalvi A, Herkert JC, Sinke RJ, van den Berg MP, Mogensen J, Jongbloed JDH, et al. Clinical utility gene card for: dilated cardiomyopathy (CMD). Eur J Hum Genet. 2013;21:1185.

    Article CAS  Google Scholar 

  34. Wess G, Wallukat G, Fritscher A, Becker NP, Wenzel K, Müller J, et al. Doberman pinschers present autoimmunity associated with functional autoantibodies: a model to study the autoimmune background of human dilated cardiomyopathy. PLoS One. 2019;14:e0214263.

    Article CAS PubMed PubMed Central  Google Scholar 

  35. Wess G, Domenech O, Dukes-McEwan J, Häggström J, Gordon S. European Society of Veterinary Cardiology screening guidelines for dilated cardiomyopathy in Doberman Pinschers. J Vet Cardiol. 2017;19:405–15.

    Article CAS PubMed  Google Scholar 

  36. Luis Fuentes V, Abbott J, Chetboul V, Côté E, Fox PR, Häggström J, et al. ACVIM consensus statement guidelines for the classification, diagnosis, and management of cardiomyopathies in cats. J Vet Intern Med. 2020;34:1062–77.

    Article PubMed PubMed Central  Google Scholar 

  37. Gil-Ortuño C, Sebastián-Marcos P, Sabater-Molina M, Nicolas-Rocamora E, Gimeno-Blanes JR, Fernández Del Palacio MJ. Genetics of feline hypertrophic cardiomyopathy. Clin Genet. 2020;3:203–14.

  38. Tilley LP, Liu SK, Gilbertson SR, Wagner BM, Lord PF. Primary myocardial disease in the cat. A model for human cardiomyopathy. Am J Pathol. 1977;86:493–522.

    CAS PubMed PubMed Central  Google Scholar 

  39. Ueda Y, Stern JA. A one health approach to hypertrophic cardiomyopathy. Yale J Biol Med. 2017;90:433–48.

    CAS PubMed PubMed Central  Google Scholar 

  40. Wallner M, Eaton DM, Berretta RM, Borghetti G, Wu J, Baker ST, et al. A feline HFpEF model with pulmonary hypertension and compromised pulmonary function. Sci Rep. 2017;7:16587.

    Article PubMed PubMed Central CAS  Google Scholar 

  41. • Lowenstine LJ, McManamon R, Terio KA. Comparative pathology of aging great apes: bonobos, chimpanzees, gorillas, and orangutans. Vet Pathol. 2016;53:250–76The study details cardiovascular and other pathologies in context of great ape gerontology. As our closest living relatives, insights on cardiovascular diseases in chimpanzees, bonobos, gorillas and orangutans also cast additional light on these conditions in humans.

    Article CAS PubMed  Google Scholar 

  42. Strong VJ, Grindlay D, Redrobe S, Cobb M, White K. A systematic review of the literature relating to captive great ape morbidity and mortality. J Zoo Wildl Med. 2016;47:697–710.

    Article PubMed  Google Scholar 

  43. Varki N, Anderson D, Herndon JG, Pham T, Gregg CJ, Cheriyan M, et al. Heart disease is common in humans and chimpanzees, but is caused by different pathological processes. Evol Appl. 2009;2:101–12.

    Article PubMed PubMed Central  Google Scholar 

  44. Schulman FY, Farb A, Virmani R, Montali RJ. Fibrosing cardiomyopathy in captive western lowland gorillas (Gorilla gorilla gorilla) in the United States: a retrospective study. J Zoo Wildl Med. 1995;26:43–51.

    Google Scholar 

  45. Seward JB, Casaclang-Verzosa G. Infiltrative cardiovascular diseases: cardiomyopathies that look alike. J Am Coll Cardiol. 2010;55:1769–79.

    Article PubMed  Google Scholar 

  46. Sleeper MM, Drobatz K, Lee DR, Lammey ML. Echocardiography parameters of clinically normal adult captive chimpanzees (Pan troglodytes). J Am Vet Med Assoc. 2014;244:956–60.

    Article PubMed  Google Scholar 

  47. Celestino-Soper PBS, Lynnes TC, Zhang L, Ouyang K, Wann S, Clyde VL, et al. Genetic analyses in a bonobo (Pan paniscus) with arrhythmogenic right ventricular cardiomyopathy. Sci Rep. 2018;8:4350.

    Article PubMed PubMed Central CAS  Google Scholar 

  48. Kenny DE, Cambre RC, Alvarado TP, et al. Aortic dissection: an important cardiovascular disease in captive gorillas (Gorilla gorilla gorilla). J Zoo Wildl Med. 1994;25:561–8.

    Google Scholar 

  49. Stenvinkel P, Painer J, Johnson RJ, Natterson-Horowitz B. Biomimetics - Nature’s roadmap to insights and solutions for burden of lifestyle diseases. J Intern Med. 2020;287:238–51.

    Article CAS PubMed  Google Scholar 

  50. Drew KL, Rice ME, Kuhn TB, Smith MA. Neuroprotective adaptations in hibernation: therapeutic implications for ischemia-reperfusion, traumatic brain injury and neurodegenerative diseases. Free Radic Biol Med. 2001;31:563–73.

    Article CAS PubMed  Google Scholar 

  51. Jansen HT, Trojahn S, Saxton MW, Quackenbush CR, Evans Hutzenbiler BD, Nelson OL, et al. Hibernation induces widespread transcriptional remodeling in metabolic tissues of the grizzly bear. Commun Biol. 2019;2:336.

    Article PubMed PubMed Central CAS  Google Scholar 

  52. Friedrich AU, Kakuturu J, Schnorr PJ, et al. Comparative coagulation studies in hibernating and summer-active black bears (Ursus americanus). Thromb Res. 2017;158:16–8.

    Article CAS PubMed  Google Scholar 

  53. Albuquerque TAF, Drummond do Val L, Doherty A, de Magalhães JP. From humans to hydra: patterns of cancer across the tree of life. Biol Rev Camb Philos Soc. 2018;93:1715–34.

    Article PubMed PubMed Central  Google Scholar 

  54. Blumstein DT, Rangchi TN, Briggs T, De Andrade FS, Natterson-Horowitz B. A systematic review of carrion eaters’ adaptations to avoid sickness. J Wildl Dis. 2017;53:577–81.

    Article CAS PubMed  Google Scholar 

  55. Currie SE, Stawski C, Geiser F. Cold-hearted bats: uncoupling of heart rate and metabolism during torpor at sub-zero temperatures. J Exp Biol. 2018;221:jeb170894.

    PubMed  Google Scholar 

  56. O’Rourke MF, Avolio AP, Nichols WW. The kangaroo as a model for the study of hypertrophic cardiomyopathy in man. Cardiovasc Res. 1986;20:398–402.

    Article PubMed  Google Scholar 

  57. Oren O, Goldberg S. Heart failure with preserved ejection fraction: diagnosis and management. Am J Med. 2017;130:510–6.

    Article PubMed  Google Scholar 

  58. Zile MR, Baicu CF, Ikonomidis JS, et al. Myocardial stiffness in patients with heart failure and a preserved ejection fraction: contributions of collagen and titin. Circulation. 2015;131:1247–59.

    Article CAS PubMed PubMed Central  Google Scholar 

  59. Bertelsen MF, Grøndahl C, Stegmann GF, Sauer C, Secher NH, Hasenkam JM, et al. Accuracy of noninvasive anesthetic monitoring in the anesthetized giraffe (Giraffa camelopardalis). J Zoo Wildl Med. 2017;48:609–15.

    Article PubMed  Google Scholar 

  60. Brøndum E, Hasenkam JM, Secher NH, Bertelsen MF, Grøndahl C, Petersen KK, et al. Jugular venous pooling during lowering of the head affects blood pressure of the anesthetized giraffe. Am J Phys Regul Integr Comp Phys. 2009;297:R1058–65.

    Google Scholar 

  61. Damkjaer M, Wang T, Brøndum E, Østergaard KH, Baandrup U, Hørlyck A, et al. The giraffe kidney tolerates high arterial blood pressure by high renal interstitial pressure and low glomerular filtration rate. Acta Physiol (Oxford). 2015;214:497–510.

    Article CAS  Google Scholar 

  62. • Smerup M, Damkjær M, Brøndum E, et al. The thick left ventricular wall of the giraffe heart normalises wall tension, but limits stroke volume and cardiac output. J Exp Biol. 2016;219:457–63Findings from this study suggest that while many characteristics of modern giraffe myocardium align with what is found in other mammals, unique adaptations involving wall thickness, LV cavity size and cardiac output have evolved in association with its high systemic arterial pressure.

    PubMed  Google Scholar 

  63. Wolf CM. Hypertrophic cardiomyopathy: genetics and clinical perspectives. Cardiovasc Diagn Ther. 2019;9:S388–415.

    Article PubMed PubMed Central  Google Scholar 

  64. Campbell TJ. Characteristics of cardiac action potentials in marsupials. J Comp Physiol B. 1989;158:759–62.

    Article CAS PubMed  Google Scholar 

  65. Hing S, Narayan E, Thompson RC, Godfrey S. A review of factors influencing the stress response in Australian marsupials. Conserv Physiol. 2014;2:cou027.

    Article PubMed PubMed Central CAS  Google Scholar 

  66. Fredholm DV, Jones AE, Hall NH, Russell K, Heard DJ. Successful management of hypertrophic cardiomyopathy in a Matschie’s tree kangaroo (Dendrolagus matschiei). J Zoo Wildl Med. 2015;46:95–9.

    Article PubMed  Google Scholar 

  67. Stern AW, Smith S, Snider TA. Hypertrophic cardiomyopathy in two captive Bennett’s wallabies (Macropus rufogriseus rufogriseus). J Vet Diagn Investig. 2009;21:889–92.

    Article  Google Scholar 

  68. Arany Z, Elkayam U. Peripartum cardiomyopathy. Circulation. 2016;133:1397–409.

    Article CAS PubMed  Google Scholar 

  69. Isogai T, Kamiya CA. Worldwide incidence of peripartum cardiomyopathy and overall maternal mortality. Int Heart J. 2019;60:503–11.

    Article PubMed  Google Scholar 

  70. Warren JD, Aitken-Palmer C, Weldon AD, Flanagan JP, Howard LL, Garner MM, et al. Congestive heart failure associated with pregnancy in okapi (Okapia johnstoni). J Zoo Wildl Med. 2017;48:179–88.

    Article PubMed  Google Scholar 

  71. Letunic I, Bork P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256–9.

    Article CAS PubMed PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors wish to acknowledge the following investigators for granting permission to use echocardiographic images from non-domestic animal species: Dr. Scott Citino, University of Florida and White Oak Conservation Center, Florida, USA and Dr. Alan D. Weldon, Jacksonville Equine Associates, Florida, USA (okapi); Dr. Darryl Heard, University of Florida, USA (tree kangaroo); Dr. Tobias Wang, Århus University, Denmark (giraffe). We are furthermore grateful to everyone who facilitated the search for echocardiographic images, including Dr. Kirk Sudemeyer, Kansas City Zoo, USA; Dr. Suzan Murray, Smithsonian Conservation Biology Institute, Washington DC, USA; Dr. Michael Garner, Northwest ZooPath, Washington, USA; Dr. Haley Murphy, Zoo Atlanta, Georgia, USA; Dr. Dominique Keller, Los Angeles Zoo, California, USA. We thank Basil Baccouche and Susan Kwan for technical support with the manuscript preparation.

Author information

Authors and Affiliations

  1. Department of Medicine, Harvard Medical School, Boston, MA, USA

    B. N. Horowitz

  2. Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA

    B. N. Horowitz

  3. David Geffen School of Medicine, University of California, Los Angeles, CA, USA

    B. N. Horowitz

  4. William Beaumont School of Medicine, Oakland University, Rochester, MI, USA

    Ilana B. Kutinsky

  5. College of Veterinary Medicine, Western University of Health Sciences, Pomona, CA, USA

    Annika Linde

Authors
  1. B. N. Horowitz
  2. Ilana B. Kutinsky
  3. Annika Linde

Corresponding author

Correspondence toB. N. Horowitz.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection onEchocardiography

Electronic Supplementary Material

Supplementary Video 1

Giraffe heart imaged using modified intracardiac echo technique. TEE probe inserted into internal jugular vein and passed into right atrium. Equivalent of four chamber view shown. (Video provided and with permission from the authors of Smerup et al. Journal of Experimental Biology (2016) 219, 457–463. doi:https://doi.org/10.1242/jeb.132753) [62•]) (AVI 13732 kb).

Rights and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Horowitz, B.N., Kutinsky, I.B. & Linde, A. Species-Spanning Echocardiography: Cardiovascular Insights from Across the Animal Kingdom.Curr Cardiol Rep22, 165 (2020). https://doi.org/10.1007/s11886-020-01417-8

Download citation

Keywords

Associated Content

Part of a collection:

Topical Collection on Echocardiography

Access this article

Subscribe and save

Springer+
from ¥17,985 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price includes VAT (Japan)

Instant access to the full article PDF.

Advertisement

[8]ページ先頭
©2009-2025 Movatter.jp