Left Ventricular Adaptations in Herding Dogs

Raimy Costa Martins, João Paulo da Exaltação Pascon, Karen Guzmán Béltran, Maria Ligia de Arruda Mistieri

Abstract


Background: Athlete’s heart syndrome comprises a set of functional and anatomic cardiac changes secondary to intense and prolonged physical exercise in humans and animals. The heart adapts to the type of activity performed, and Doppler echocardiography is the best tool for identifying these changes. Speckle tracking echocardiography (STE) has provided new data on cardiovascular adaptations secondary to physical exercise in humans, information that conventional echocardiography cannot provide. Although physical activity and work in dogs are well documented, there are few studies on cardiovascular adaptations secondary to exercise in dogs, and no studies to date evaluated these adaptations using STE.

Materials, Methods &Results:A total of 31 dogs of the Border Collie and OvelheiroGaúchoBrasileiro breeds were divided into two groups: a herding group (HG, n = 15), which performed herding activity five to six times a week for at least 4 months, and a sedentary group (SG, n = 16), with no history of physical activity in the past twelve months. All dogs were previously subjected to electrocardiography and blood pressure measurement. After that, the animals underwent echocardiographic examination at rest at a single time point. The data were analyzed by two-way multivariate analysis of variance (ANOVA) at a level of significance of 5% (P < 0.05) and a trend at 90% (< 0.1). The dogs of the HG had higher values for left-ventricular end-systolic diameter (LVESD) and systolic volume (SV), and lower values for left-ventricular myocardial performance index (Tei index) and systolic septal movement. STE results indicated that the HG presented lower values for strain and strain rate in some myocardial segments in the radial, circumferential, longitudinal, and transverse directions.

Discussion:The increase in LVESD is justified by the increase in preload (volume) required to meet the increased oxygen demand, whereas SV is directly related to the Frank-Starling mechanism. The lower Tei index in the HG indicates better systolic-diastolic performance, explained by a shorter isovolumetric relaxation time and isovolumetric contraction time and by an increase in left ventricular (LV) ejection time. Similar results were not observed in LV systolic wall motion. Therefore, we believe that the most likely explanation is a higher systolic efficiency, associated with lower energy demand at rest. According to STE criteria, the lower strain and strain rate in the HG in some myocardial segments in all directions suggest less need for myocardial deformation and lower deformation velocity in order to maintain systolic function. In conclusion, conventional echocardiography and STE were complementary and fundamental to understand cardiovascular adaptations in herding dogs.


Full Text:

PDF

References


Amory H., Votion D.M., Fraipont A., Goachet A.G., Robert C., Farnir F.& Van Erck E. 2010. Altered systolic left ventricular function in horses completing a long distance endurance race. Equine Veterinary Journal. 42(38): 216-219.

ArnottE.R., Early J.B., Wade C.M.& McGreevy P.D. 2014. Environmental factors associated with success rates of Australian stock herding dogs. PloSOne. 9(8): 1-13.

Baggish A.L., Wang F., Weiner R.B., Elinoff J.M., Tournoux F., Boland A., Picard M.H., Huuter A.M.& Wood M.J. 2008. Training-specific changes in cardiac structure and function: a prospective and longitudinal assessment of competitive athletes. Journal of Applied Physiology.104(4): 1121-1128.

Barbier J., Ville N., Kervio G., Walther G.&Carré F. 2006. Sports-specific features of athlete’s heart and their relation to echocardiographic parameters. HerzKardiovaskuläreErkrankungen.31(6):531-543.

Barreto E.S.B. 2015. Por dez vacas com cria eu não troco meu cachorro’: as relações entre humanos e cães nas atividades pastoris do pampa brasileiro. 131f. Pelotas, RS. Dissertação (Mestrado em Antropologia) - Programa de Pós Graduação em Antropologia, Universidade Federal de Pelotas.

BoonJ.A. 2011. Evaluation of size, function, and hemodynamics. In: Veterinary Echocardiography. 2ndedn. Hoboken: Wiley-Blackwel, pp.151-260.

Boutcher S.H., McLaren, P.F., Cotton Y.&Boutcher Y. 2003. Stroke volume response to incremental submaximal exercise in aerobically trained, active, and sedentary men. Canadian Journal of Applied Physiology. 28(1): 12-26.

Butz T., Van Buuren F., Mellwig K.P., Langer C., Plehn G., Meissner A.& Faber L.2011. Two-dimensional strain analysis of the global and regional myocardial function for the differentiation of pathologic and physiologic left ventricular hypertrophy: a study in athletes and in patients with hypertrophic cardiomyopathy. The International Journal of Cardiovascular Imaging. 27(1): 91-100.

Carnabuci C., Hanås S., Ljungvall I., Tidholm A., Bussadori C., Häggström J.&Höglund K. 2013. Assessment of cardiac function using global and regional left ventricular endomyocardial and epimyocardial peak systolic strain and strain rate in healthy Labrador retriever dogs. Research in Veterinary Science. 95(1): 241-248.

Chetboul V.2002. Tissue Doppler imaging: a promising technique for quantifying regional myocardial function. Journal of Veterinary Cardiology. 4(2): 7-12.

Chetboul V., Serres F., Gouni V., Tissier R.&Pouchelon J.L. 2008. Noninvasive assessment of systolic left ventricular torsion by 2‐dimensional speckle tracking imaging in the awake dog: Repeatability, reproducibility, and comparison with tissue Doppler imaging variables. Journal of Veterinary Internal Medicine. 22(2): 342-350.

ChetboulV.2010. Advanced techniques in echocardiography in small animals. Veterinary Clinics: Small Animal Practice. 40(4): 529-543.

Chetboul V., Bussadori C.&Madron E.2016. Normal echocardiographic values: TM, 2D, and Doppler spectral modes. In: Chetboul V. (Ed).Clinical Echocardiography of the Dog and the Cat. St. Louis: Elsevier, pp.31-37.

Chetboul V., Escriou C., Tessier D., Richard V., Pouchelon J.L., Thibault H.&Derumeaux G. 2004. Tissue Doppler imaging detects early asymptomatic myocardial abnormalities in a dog model of Duchenne's cardiomyopathy. European Heart Journal. 25(21): 1934-1939.

Chetboul V. &Tissier R. 2012. Echocardiographic assessment of canine degenerative mitral valve disease. Journal of Veterinary Cardiology. 14(1): 127-148.

D'Andrea A., Cocchia R., Riegler L., Scarafile R., Salerno G., Gravino R.&Pacileo G. 2010.Left ventricular myocardial velocities and deformation indexes in top-level athletes. Journal of the American Society of Echocardiography. 23(12): 1281-1288.

D’Ascenzi F., Caselli S., Solari M., Pelliccia A., Cameli M., Focardi M.&Mondillo S. 2016.Novel echocardiographic techniques for the evaluation of athletes’ heart: A focus on speckle-tracking echocardiography. European Journal of Preventive Cardiology. 23(4): 437-446.

Del Castillo J.M., Herszkowicz N., Boschilia T., Capuano R.L.&Cortese M.D. 2009.Deformação miocárdica tangencial (shearstrain) em indivíduos normais: o seu significado. Revista brasileira de ecocardiografia e imagem cardiovascular. 22(4): 20-26.

Demirelli S., Sam C.T., Ermis E., Degirmenci H., Sen I., Arisoy A.&Simsek Z. 2015.Long‐term cardiac remodeling in elite athletes: assessment by tissue Doppler and speckle tracking echocardiography. Echocardiography. 32(9): 1367-1373.

Derumeaux G., Ichinose F., Raher M.J., Morgan J.G., Coman T., LeeC.&Scherrer-Crosbie M. 2008. Myocardial alterations in senescent mice and effect of exercise training: a strain rate imaging study. Circulation: Cardiovascular Imaging. 1(3): 227-234.

Hansson K., Häggström J., Kvart C.& Lord P. 2002. Left atrial to aortic root indices using two‐dimensional and M‐mode echocardiography in cavalier King Charles spaniels with and without left atrial enlargement. Veterinary Radiology & Ultrasound. 43(6): 568-575.

Helton W.2009. Physiological demands and adaptations of working dogs. In: DavisM.S. (Ed).Canine Ergonomics: The Science of Working Dogs. Boca Raton: CRC Press, pp.245-262.

Kasikcioglu E., Oflaz H., Akhan H., Mercanoglu F.&Kayserilioglu A. 2003.Tei index and aerobic capacity in endurance athletes. European Journal of Echocardiography. (4): 56.

Kovács A., Oláh, A., Lux Á., Mátyás C., Németh B.T., Kellermayer D.&Assabiny A. 2015. Strain and strain rate by speckle-tracking echocardiography correlate with pressure-volume loop-derived contractility indices in a rat model of athlete's heart. American Journal of Physiology-Heart and Circulatory Physiology. 308(7): 743-748.

Lancellotti P., Cosyns B., Zacharakis D., Attena E., Van Camp G., Gach O.Πérard L. A. 2008. Importance of left ventricular longitudinal function and functional reserve in patients with degenerative mitral regurgitation: assessment by two-dimensional speckle tracking. Journal of the American Society of Echocardiography. 21(12): 1331-1336.

Lombard C.W.& Spencer C.P. 1985. Correlation of radiographic, echocardiographic, and electrocardiographic signs of left heart enlargement in dogs with mitral regurgitation. Veterinary Radiology & Ultrasound. 26(3): 89-97.

Lonsdale R.A., Labuc R.H.& Robertson I.D. 1998. Echocardiographic parameters in training compared with non‐training Greyhounds. Veterinary Radiology & Ultrasound. 39(4): 325-330.

Mantovani M.M., Muzzi R. A.L., Pereira G.G., Yamato R.J., Silva A.C., Reis G.F.& Guimarães E.C. 2015.Systolic cardiac function assessment by feature tracking echocardiography in dogs with myxomatous mitral valve disease. Journal of Small Animal Practice. 56(6): 383-392.

Mihl C., Dassen W.R.M.&Kuipers H. 2008. Cardiac remodelling: concentric versus eccentric hypertrophy in strength and endurance athletes. Netherlands Heart Journal. 16(4):129-133.

Monte I.P., Mangiafico S., Buccheri S., Bottari V.E., Lavanco V., Arcidiacono A.A.&Tamburino C. 2015. Myocardial deformational adaptations to different forms of training: a real-time three-dimensional speckle tracking echocardiographic study. Heart and Vessels. 30(3): 386-395.

Morganroth J., Maron B.J., Henry W.L.& Epstein S.E. 1975. Comparative left ventricular dimensions in trained athletes. Annals of Internal Medicine. 82(4): 521-524.

Moro A.S., Okoshi M.P., Padovani C.R.&Okoshi K. 2013. Doppler echocardiography in athletes from different sports. Medical Science Monitor. 19: 187.

Richand V., Lafitte S., Reant P., Serri K., Lafitte M., Brette S.&Roudaut R. 2007. An ultrasound speckle tracking (two-dimensional strain) analysis of myocardial deformation in professional soccer players compared with healthy subjects and hypertrophic cardiomyopathy. American Journal of Cardiology. 100(1): 128-132.

Rovira S., Munoz A.& Benito M. 2007.Hematologic and biochemical changes during canine agility competitions. VeterinaryClinicalPathology. 36(1): 30-35.

Silva A.P. 2011. Deformação miocárdica em atletas de diferentes modalidades–Um estudo por 2D SpeckleTracking. 98p. Lisboa. Dissertação (Mestrado em Ultrassonografia Cardiovascular)–Programa de Pós Graduação em Tecnologia de Diagnóstico e Intervenção Cardiovascular, Escola Superior de Tecnologia da Saúde de Lisboa.

Simsek Z., Gundogdu F., Alpaydin S., Gerek, Z., Ercis S., Sen I.&Karakelleoglu S. 2011. Analysis of athletes’ heart by tissue Doppler and strain/strain rate imaging. The International Journal of Cardiovascular Imaging. 27(1): 105-111.

Simsek Z., HakanTas M., Degirmenci H., GokhanYazıcı A., Ipek E., Duman H.&Senocak H. 2013. Speckle tracking echocardiographic analysis of left ventricular systolic and diastolic functions of young elite athletes with eccentric and concentric type of cardiac remodeling. Echocardiography. 30(10): 1202-1208.

Smith D.N., Bonagura J.D., Culwell N.M.&Schober K.E. 2012. Left ventricular function quantified by myocardial strain imaging in small-breed dogs with chronic mitral regurgitation. Journal of Veterinary Cardiology. 14(1): 231-242.

Starling E.H.&Visscher M.B. 1927. The regulation of the energy output of the heart. The Journal of Physiology. 62(3): 243-261.

Stepien R.L., Hinchcliff K.W., Constable P.D.& Olson J. 1998. Effect of endurance training on cardiac morphology in Alaskan sled dogs. Journal of Applied Physiology. 85(4): 1368-1375.

Storteig Horn S., Steinheim G., Fjerdingby O.H., Gjerjordet H.F. &Klemetsdal G. 2017. Genetic analyses of herding traits in the Border Collie using sheepdog trial data. Journal of Animal Breeding and Genetics. 134(2): 144-151.

Szauder I., Kovács A.&Pavlik G. 2015.Comparison of left ventricular mechanics in runners versus bodybuilders using speckle tracking echocardiography. Cardiovascular Ultrasound. 13(1): 7.

Takano H., Fujii Y., Yugeta N., Takeda S.&Wakao Y. 2011.Assessment of left ventricular regional function in affected and carrier dogs with Duchenne muscular dystrophy using speckle tracking echocardiography. BMC Cardiovascular Disorders. 11(1): 23.

Tei C. 1995. New noninvasive index for combined systolic and diastolic ventricular function. Journalof Cardiology. 26:135-136.

Teichholz L.E., Kreulen T., Herman M.V.&Gorlin R. 1976. Problems in echocardiographic volume determinations: echocardiographic-angiographic correlations in the presence or absence of asynergy. American Journal of Cardiology. 37(1): 7-11.

Troy B.L., Pombo J.&Rackley C.E. 1972. Measurement of left ventricular wall thickness and mass by echocardiography. Circulation. 45(3): 602-611.

Tüzün N., Ergün M., Alioğlu E., Edem E., Tengiz I., Aytemiz F.&İşleğen Ç. 2015. TEI Index in elite sprinters and endurance athletes. The Journal of Sports Medicine and Physical Fitness. 55(9): 988-994.

Utomi V., Oxborough D., Ashley E., Lord R., Fletcher S., StembridgeM.& Sharma S. 2014. Predominance of normal left ventricular geometry in the male ‘athlete's heart’. Heart. 100(16):1264-1271.

Wang Y., Wisloff U.& Kemi O.J. 2010. Animal models in the study of exercise-induced cardiac hypertrophy. Physiological Research. 59(5): 633.

Wess G., Keller L.J., Klausnitzer M., Killich M.& Hartmann K. 2011. Comparison of longitudinal myocardial tissue velocity, strain, and strain rate measured by two-dimensional speckle tracking and by color tissue Doppler imaging in healthy dogs. Journal of Veterinary Cardiology. 13(1): 31-43.

WilliamsT. 2007. Natural ability and selection. In: Working Sheep Dogs: A Practical Guide to Breeding, Training and Handling. Melbourne:Landlinks Press, pp.7-63.




DOI: https://doi.org/10.22456/1679-9216.90864

Copyright (c) 2019 Raimy Costa Martins, João Paulo da Exaltação Pascon, Karen Guzmán Béltran, Maria Ligia de Arruda Mistieri

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.