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Transthoracic Echocardiography and Cardiac Locquet et al. BMC Veterinary Research (2020) 16:217 https://doi.org/10.1186/s12917-020-02406-3 RESEARCH ARTICLE Open Access Transthoracic echocardiography and cardiac biomarkers in healthy captive male and female squirrel monkeys (Saimiri spp.) Laurent Locquet1*†, Blandine Houdellier2†, Bart J. G. Broeckx3, Tim Bouts4, Veronique Liekens1, Jimmy H. Saunders2† and Pascale Smets1† Abstract Background: Echocardiography is the most frequently used non -invasive diagnostic tool to evaluate cardiac anatomy and function in domestic species but increasingly also in non -domestic species, especially since cardiac disease is being recognized as an important cause of death in captive primates. The purpose of this cross -sectional study was to investigate the feasibility of transthoracic echocardiography in healthy squirrel monkeys as well as to provide species specific normal values for standard echocardiographic measurements. A secondary aim was to determine plasma and serum levels of the cardiac biomarkers, N -terminal pro -brain natriuretic peptide (NT -proBNP) and cardiac troponin T (cTnT). Furthermore, a commercial, non -invasive, smartphone -based ECG (AliveCor Vet TM) monitoring device was used to evaluate the heart rate and rhythm and to diagnose possible arrhythmias. Results: In this study, transthoracic echocardiography of 14 squirrel monkeys was performed in right and left lateral recumbency. Similar standard right parasternal and left apical images were obtained as in dogs and cats and normal values for routine two -dimensional, time motion mode and Doppler mode measurements were generated. Thirteen animals were considered healthy and one squirrel monkey was identified with significant aortic dilation and regurgitation and consequently values obtained from this animal were not used when species specific normal values were calculated. NT -ProBNP and cTnT concentrations were available for 7 of the 13 healthy monkeys with NT -proBNP concentrations below detection limit in all animals and a mean cTnT concentration of 0.049 ng/mL. Electrocardiography was performed in all squirrel monkeys. The mean heart rate was 172 bpm. Frequent supraventricular premature beats were diagnosed in the squirrel monkey suffering from significant aortic dilation and regurgitation. Conclusion: This study presents echocardiographic normal values and additional cardiovascular data in anaesthetised Saimiri monkeys, fundamental from both the perspective of zoo animal health care as well as scientific research, since the squirrel monkey is often used as an animal model for human disease. Keywords: Squirrel monkey, Saimiri, Echocardiography, Cardiac troponin T, NT-proBNP * Correspondence: [email protected] †Laurent Locquet, Blandine Houdellier, Jimmy H. Saunders and Pascale Smets contributed equally to this work. 1Small Animal Department, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Locquet et al. BMC Veterinary Research (2020) 16:217 Page 2 of 13 Background in the squirrel monkey [34–38]. The general protocol Squirrel monkeys (family Cebidae, subfamily Saimirinae) applied in great apes is comparable to echocardiog- are among the most commonly studied animal models raphy performed in humans, as the anatomy and in biomedical research, both in veterinary and human morphology of the thorax is similar. Given a similar medicine, the latter due to their phylogenetic similarities thoracic morphology compared to cats and dogs, it [1]. These arboreal neotropical nonhuman primates have was decided to follow the protocol for feline and ca- been subdivided into divergent taxa on which numerous nine echocardiographic examinations, which has been biological, biogeographical, morphological and behav- thoroughly described [39, 40]. ioural studies have been published in the past [2–11]. The primary aims of this study were to test the feasi- Despite these earlier studies, vital information for both bility of transthoracic echocardiography (TTE), following wildlife conservation, zoological management and future a protocol similar to canine and feline echocardiography, biomedical research is still lacking, indicating the im- in healthy squirrel monkeys as well as to provide species portance of additional studies in order to better under- specific normal values for standard echocardiographic stand the biology and morphology of the squirrel measurements. A secondary aim was to determine blood monkey. concentrations of two cardiac biomarkers, NT -proBNP Several studies in both human and nonhuman pri- and cTnT, and to evaluate heart rate and rhythm using a mates have identified cardiovascular disease as a major non -invasive, smartphone based ECG (AliveCor Vet cause of death with mortality rates ranging from 41% in TM) monitoring device. gorillas to approximately 81% in chimpanzees (Meehan and Lowenstine, 1994 [12–15];). Earlier studies and case reports have described one or multiple cases of dilated, Results hypertrophic (-like) and fibrosing cardiomyopathy in One Saimiri boliviensis peruviensis presented with a sig- several monkey species, including the Rhesus macaque nificant abnormality (severe dilation of the ascending (Macaca mulatta), owl monkey (Aotus sp.) and squirrel aorta with aortic regurgitation) on echocardiography and monkey [12, 13, 15–24]. arrhythmia (frequent supraventricular beats) on electro- Given the significant mortality secondary to cardiovas- cardiography and was excluded from the study. The age cular disease, previous research has concentrated on of the 13 remaining animals ranged from 2.25 to 21.3 thoracic radiographic, electrocardiographic and echocar- years (mean age = 9.12 years ± SD of 6.95 years). The diographic characteristics of squirrel monkeys [25, 26]. minimum and maximum weights of the animals were However, only few echocardiographic parameters have 467 g and 756 g respectively (mean weight = 615 g ± SD been described earlier and an echocardiographic proto- of 92 g). There were 11 females and 2 males. col is currently lacking in the squirrel monkey. Good quality echocardiographic examinations were Echocardiography is the most commonly used diag- obtained in all 13 healthy animals and 25 variables were nostic tool for non -invasive assessment of cardiac struc- measured (Table 1). Eleven squirrel monkeys (Saimiri tures and function. Elevated blood concentrations of spp.) showed signs of trace valvular insufficiency without cardiac biomarkers such as N -terminal pro -brain natri- clinical relevance, namely of the mitral valve (n = 2), uretic peptide (NT -proBNP), cardiac troponin I (cTnI) tricuspid valve (n = 6), aortic valve (n = 2) and pulmonic and T (cTnT) are associated with several types of cardiac valve (n = 7). Furthermore, one mild mitral valve insuffi- disease in human and veterinary medicine [27–30]. Car- ciency was diagnosed without signs of cardiac diac troponin T is an intracellular protein, bound to the remodelling. actin backbone within cardiomyocytes. Elevated cTnT High sensitivity cTnT concentrations were measured values, indicating recent damage of cardiomyocytes, can in seven squirrel monkeys with a mean ± SD of 0.049 ng/ be a useful diagnostic piece of a puzzle in cardiac disease m ± 0.043 ng/mL and a range of 0.005 -0.129 ng/L. NT in both domestic and non domestic mammals [27]. -proBNP concentrations in these seven squirrel monkeys Given the fact that cardiac troponin is encoded in higher were all below the detection limit of 0.5912 pmol/L. A vertebrates by orthologous genes, this biomarker appears summary of the characteristics of the included squirrel to be highly conserved across species [31, 32]. Increased monkeys and adjacent cTnT values and echocardio- NT -proBNP concentrations are associated with myocar- graphic findings can be found in Table 2. dial stretch, as described in many human and veterinary Electrocardiographic examination was performed in all studies [33]. but one Saimiri boliviensis, due to technical difficulties. Although an echocardiographic protocol in great apes The mean heart rate ± SD in these 12 squirrel monkeys has been described and is currently being applied in a (Saimiri spp.) during the echocardiographic examination large international study in chimpanzees, gorillas, bono- was 172 ± 40 bpm (121 -236 bpm). No cardiac arrhyth- bos and orangutans, no such protocol has been defined mias were detected (Fig. 1). Locquet et al. BMC
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