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Heart morphology and function evaluation by transthoracic echocardiography in six captive crested gibbons (Nomascus spp.)

Evaluation de la morphologie et de la fonction cardiaque chez six gibbons à crêtes captifs (Nomascus spp.)
Irène Vonfeld, Anaïs Nowakowski, Brice Lefaux and Benoît Quintard

Abstracts

Cardiovascular diseases are one of the leading causes of morbidity and mortality in captive apes. Transthoracic echocardiography is the most comprehensive cardiovascular imaging technique used to diagnose and monitor cardiopathies in mammals. However, there are currently no baseline data of heart morphology and function in hylobatid primates. Conventional transthoracic echocardiograms were performed on six clinically healthy crested gibbons of three species (Nomascus siki, N. leucogenys and N. gabriellae) under general anesthesia using sevoflurane without premedication. Each echocardiogram included the evaluation of 11 variables in bidimensional mode, 8 variables in M-Mode and 6 variables in Doppler mode. Most functional parameters evaluated, like left ventricular ejection fraction (range, 49.3 to 72.4%), shortening fraction (SF; range, 18.9 to 34.5%), left atrium/aorta ratio (range, 0.8 to 1.2), and maximal velocity of aortic, pulmonic, and mitral flows had similar values as those described in gorillas, dogs, and humans. Valvular insufficiencies were detected in two of the six individuals evaluated: one adult female N. siki was diagnosed with a discrete aortic regurgitation and one young male N. leucogenys with a mild mitral valve insufficiency. The mitral valve regurgitation was associated with a low-grade systolic heart murmur, but no further morphological changes of heart chambers were identified in these animals. Finally, a decreased heart contractility (SF = 18.9%) was diagnosed in one female N. gabriellae. This study is the first database transthoracic echocardiography in gibbons undergoing general anesthesia.

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Editor’s notes

Received 25/01/2024, accepted after revisions 06/05/2024, published online 25/06/2024. A translated version, in French, is available online in supplementary materials.
Une version, traduite en français, est disponible en ligne en annexe.

Full text

1 Introduction

1Cardiovascular diseases (CVD) have been identified as a major cause of mortality and morbidity in all great ape taxa, with mortality rates related to CVD ranging from 10% in orangutans (Pongo pygmaeus; Besnard et al., 2021) to 45% in bonobos (Pan paniscus; McManamon & Lowenstine, 2012; Murphy & Danforth, 2019), with up to 80% of geriatric animals dying from CVD or their consequences (Besnard et al., 2021). The most common heart disease in this taxon is known as fibrosing cardiomyopathy, characterized by a scattered pattern of myocardial fibrosis with atrophy and hypertrophy of cardiac myocytes, absent or mild inflammation, and no apparent etiology or associated diseases (Lowenstine et al., 2016; Lowenstine et al., 2018; Murphy & Danforth, 2019). Other diseases reported include congenital heart defects, cardiomyopathies, and viral myocarditis amongst other (McManamon & Lowenstine, 2012; Murphy & Danforth, 2019).

2However, antemortem diagnosis of heart diseases is challenging in non-human primates (NHP), as most animals do not show any cardiovascular clinical signs before dying from sudden death secondary to heart failure, infarction or ventricular arrhythmias (McManamon & Lowenstine, 2012; Murphy & Danforth, 2019). This has led to extensive effort to better understand cardiac function and diseases in great apes, with the development of guidelines for electrocardiographic (Atencia et al., 2015; Cloutier et al., 2020) and echocardiographic assessment (Strong et al., 2015; Boyd et al., 2020; Chetboul et al., 2022) as well as detailed protocols for post-mortem diagnosis of CVD (Strong et al., 2018; 2021). Moreover, for most of these species, specific reference intervals of echocardiographic parameters have been developed for their antemortem diagnosis (Murphy et al., 2011; Napier et al., 2013; Sleeper et al., 2014; Drane et al., 2019; 2020; Ashley et al., 2021; Chetboul et al., 2022). However, studies on CVD in lesser apes are scarce and often limited to clinical cases, like one describing a myocardial fibrosis in a white-handed gibbon (Hylobates lar) (Borkowski et al., 2000), or others mentioning cardiac diseases without further characterization (Kershaw et al., 2020).

3Crested gibbons (Nomascus spp.) are the second most species-rich genus of gibbons, and all species within this genus are either classified as endangered or critically endangered by the International Union for the Conservation of Nature (IUCN) (Geissman, 2007). As for other gibbon species, little is known about their cardiovascular system and the importance of CVD in terms of mortality and morbidity.

4Transthoracic echocardiography (TTE) is currently one of the most practical and cost-effective diagnostic imaging technique for the evaluation of cardiac function in animals (Boyd et al., 2020), allowing qualitative description of cardiac abnormalities and quantitative assessment of heart anatomy and function.

5The main aims of this pilot prospective study were therefore to 1) develop a simple protocol for TTE evaluation of cardiac morphology and function in crested gibbons (Nomascus spp.) under general anesthesia, and 2) determine whether subclinical cardiac abnormalities are present in this genus. It was hypothesized that TTE evaluation of captive crested gibbons could be performed using similar protocols as the one commonly used in great apes, and that subclinical cardiac abnormalities would be identified in some of the evaluated animals.

2 Materials and methods

2.1 Animals

6Six apparently healthy crested gibbons were involved in the study, i.e.: two adult female yellow-cheeked gibbons (Nomascus gabriellae), two adult female Southern white-cheeked gibbons (N. siki), and one adult female and one juvenile male Northern white-cheeked gibbons (N. leucogenys). Species, sex, age and weight distribution of the animals included in the study are detailed in table 1. All animals were permanently housed at Mulhouse Zoo (France) as per-requirements of international standard (European Association of Zoos and Aquaria), in enclosures with controlled access to an outdoor area. They were fed three times a day with a mix of pellets (7%), vegetables and fruits (84%) and other products (9%), resulting in a diet composed of 10.0-15.0% of acid-detergent fiber, 20.0-30.0% of neutral-detergent fiber, 3.0-6.0% of crude fat, and 15.0-16.7% of crude protein. All animals were clinically healthy at the time of evaluation, based on general examination (including cardiopulmonary auscultation and rectal temperature evaluation, complete blood count and full biochemistry panel), except for the youngest male (individual 3), which was diagnosed with a low-grade systolic heart murmur of unknown clinical significance, with a point of maximal impulse located at the level of the apex of the heart.

Table 1

Individual 

Vernacular name 

Scientific name 

Sex 

Age (yo) 

Weight (kg) 

Southern white-cheeked gibbon 

Nomascus siki 

Female 

11 

8.4 

Southern white-cheeked gibbon 

Nomascus siki 

Female 

15 

10.9 

Northern white-cheeked gibbon 

Nomascus leucogenys 

Male 

4.7 

Northern white-cheeked gibbon 

Nomascus leucogenys 

Female 

14 

8.8 

Yellow-cheeked gibbon 

Nomascus gabriellae 

Female 

31 

9.0 

Yellow-cheeked gibbon 

Nomascus gabriellae 

Female 

11 

9.5 

Species, sex, age and weight distribution of individuals included in the study

2.2 Anesthesia

7Echocardiography was performed during routine general examinations of gibbons, i.e.: contraceptive implant removal or replacement, transponder identification. Animals were trained to enter an induction chamber using operant conditioning with positive reinforcement and could therefore be induced directly with sevoflurane (8%; 2L/min O2) in a calm quiet space without the need of premedication administration by darting. Once anesthetized, animals were intubated and plane of anesthesia, heart rate, respiratory rate, end-tidal carbon dioxide (EtCO2), peripheral capillary oxygen saturation (SpO2) and rectal temperature were closely monitored every five minutes. A general examination was carried out on all animals and venous blood samples were collected from the femoral vein for complete blood count and biochemical analysis. Whole-body radiographs (Portable X-Ray System SPL-HF-VET, Sedecal) and an echocardiogram were performed. After completion of sample collection, examination and diagnostic evaluations, animals were placed in a kennel in a quiet space for recovery. All animals recovered uneventfully from anesthesia in about 5 minutes.

2.3 Echocardiography

8All echocardiograms were performed by a trained veterinarian using Vivid I ® ultrasound machine (Vivid I, GE Healthcare) equipped with a GE3S phased array cardiac probe (1.4-3.3 MHz). Animals were placed in left lateral recumbency with the left arm extended cranially (figure 1). The precordium was palpated and 70% ethanol and coupling gel were generously applied on this location before the examination. Both static images and 5-sec movie clips were recorded and saved during the examination for post-treatment assessment to limit the duration of the examination.

9Four 2D-mode, two M-mode and three doppler mode windows were used in this study to evaluate respectively 11, eight and six parameters based on great ape protocols (Boyd et al., 2020).

Figure 1

Figure 1

Anesthetized adult female yellow-cheeked gibbon (Nomascus gabriellae) placed in left lateral recumbency with the left arm extended cranially for echocardiographic examination, the probe being located between the 3rd and 4th intercoastal space just below the nipple for long axis apical views obtention.

2.4 2D-Mode: Long axis apical views

10Three long axis apical views were obtained in 2D-mode by placing the transducer in the left lateral portion of the chest, between the 3rd and 4th intercostal space, just below the nipple and with the index marker positioned towards the left shoulder (Boyd et al., 2020). An apical four-chamber view was firstly obtained to subjectively assess biventricular systolic function and relative chamber size (figure 2). Then, the transducer beam was slightly tilted and moved cranially to obtain the apical five-chamber view. This view is ideal for the evaluation of the left ventricular outflow track and aortic valve. Left and right ventricles were also visualized on this view. Pulsed wave and color doppler were used on this view for offline assessment of peak velocity of aortic flow (Vmax Ao). As no arrhythmia was detected, heart rate was simply assessed by calculating the time interval between two consecutive peak velocities of aortic flow. Finally, an apical two-chamber view was obtained by rotating the transducer 45° counterclockwise and angling it slightly towards the animals’ right shoulder. This view was used to measure anterior (amvl) and posterior (pmvl) mitral valve leaflets at their maximal diastolic opening. Simpson’s biplanar measurements were also assessed using this window. Left ventricular volumes were firstly measured by tracing the LV endocardial border at blood-tissue interface, from the septal mitral annulus, up to the apex and then to the lateral mitral annulus with exclusion of papillary muscles from the traced border, both in end-diastole, in the frame showing the largest LV cavity after mitral valve closure (Vol LVd), and in end-systole using the last frame before mitral valve opening (Vol LVs) (Serres et al., 2008).

Figure 2

Figure 2

(A) 2D-Mode: Short axis view centered on the aorta and pulmonary artery of individual 2 (LA: left atrium; RV: right ventricle; Ao: aorta; PT: pulmonary trunk); (B) 2D-Mode: Long axis apical 4-chamber view (RA: right atrium) of individual 4; (C) M-Mode: Short axis transventricular view (LVFW: left ventricular free wall; IVS: interventricular septum) of individual 4; (D) M-Mode: Short axis transmitral view (arrow: EPSS) of individual 3; (E) Transmitral flow visualized in pulsed-wave Doppler mode of individual 2; (F) Transpulmonary flow visualized in pulsed-wave Doppler mode of individual 4

11Ventricular volumes were then used to calculate LV ejection fraction (EF) as previously described (Serres et al., 2008) by using the following formula:

12Finally, pulsed-wave and color Doppler-modes were used on this view for offline assessment of peak velocity of early and late diastolic transmitral flows (E and A waves respectively), calculation of E/A ratio, and measurement of E wave deceleration time (DT) (figure 2), by placing the cursor at the level of the tips of the mitral valve leaflets.

2.5 2D-Mode: Short axis view centered on the aorta and pulmonary artery

13A short axis view at the level of the aorta and pulmonary artery was obtained in 2D-mode by placing the transducer between the sternum and left nipple, in the third or fourth intercoastal space, with the transducer pointing to the left shoulder of the animal (figure 2) (Boyd et al., 2020). This view allowed the visualization of the right ventricle, the pulmonary trunk, both atria, and tricuspid and pulmonary valves. Measurement of left atrium (LA), aorta (Ao) and pulmonary trunk (PT) diameters in diastole, and subsequent calculation of the LA/Ao ratio and the PT/Ao ratio, were also performed from this view. Pulsed-wave and color Doppler-modes on this view were also used for offline assessment of peak velocity of pulmonary flow (Vmax P) (figure 2).

2.6 M-Mode: Short axis transmitral view

14A short axis transmitral view was then obtained by angling the transducer beam caudally from the base while staying perpendicular to the long axis of the heart (figure 2). This view was visualized and recorded in M-mode for off-line assessment of E-point to septal separation (EPSS), that is the distance between the mitral valve and the interventricular septum at maximal mitral valve opening in early left ventricular diastole.

2.7 M-Mode: Short axis transventricular view

15A short axis transventricular view was obtained from the transmitral view by tilting the transducer even further toward the apex (figure 2). This view allowed the visualization of the left and right ventricles perpendicular to the long axis of the heart. By transecting the left ventricle, M-Mode measurements were obtained both in diastole and in systole (i.e.: interventricular septal thickness in diastole (IVSd, IVSs), left ventricular internal diameter (LVd, LVs), left ventricular free wall thickness (LVFWd, LVFWs)). M-mode cursor was placed just apical to the mitral valve for the obtention of this view. Left ventricular internal diameters were then used to calculate LV fractional shortening (FS) by using the following formula:

2.8 Statistical method

16Statistical analysis was performed by R version 4.1.2 using the Rcmdr: Rcommander package version 2.7-2 (R Foundation for Statistical Computing, https://www.R-project.org/​) (Fox, 2017; R Core Team, 2021). Descriptive statistics were performed to summarize the echocardiographic measurement collected as part of standard cardiac structural and functional assessments, which included measures of central tendency (i.e: mean and median) as well as measures of variability or spread (i.e: SD, interquartile range, minimum and maximum values). The nonparametric two-sided Spearman’s rank correlation was used to examine associations between body weight and all echocardiographic parameters evaluated, as well as between age and these parameters. Associations were considered statistically significant at P ≤ 0.05.

3 Results

17All conventional transthoracic echocardiography parameters could be obtained during the procedures, which lasted less than one hour and included a variety of other zootechnical or veterinary procedures (i.e., limb measurements and radiographs, transponder implantation, contraception implant removal and replacement). Eleven parameters were obtained in 2D-mode, eight parameters in M-Mode and six parameters in spectral Doppler-mode. Mean heart rate ± SD during TTE examination was 146 ± 15 bpm. Table 2 includes values of TTE measurements evaluated in each animal, and table 3 descriptive statistics of these examinations.

Table 2

Animal 

1 

2 

3 

4 

5 

6 

HR (bpm) 

141.0 

149.0 

123.0 

152.0 

169.0 

142.0 

IVSd (mm) 

5.3

8.50 

3.6 

8.1 

8.6 

14.20 

LVd (mm) 

13.4 

19.4 

22.0 

31.3 

21.0 

22.3

LVFWd (mm) 

5.5 

8.2 

4.5 

8.5 

9.1 

6.8 

IVSs (mm) 

4.6 

13.4 

5.0 

8.8 

9.7 

15.3 

LVs (mm) 

8.8 

12.7 

15.2 

25.4 

13.9 

16.0 

LVFWs (mm) 

6.8 

10.4 

8.2 

11.2 

14.2 

7.2 

FS (%) 

34.3 

34.5 

30.9 

18.9 

33.8 

25.6 

LA (cm) 

0.8 

1.2 

0.8 

1.1 

1.2 

1.6 

Ao (cm) 

1.0 

1.3 

0.9 

1.2 

1.2 

1.0 

LA/Ao 

0.8 

0.9 

0.9 

0.9 

1.0 

1.2 

PT (cm) 

0.8 

1.4 

0.6 

1.2 

1.1 

0.9 

Ao (cm) 

1.1 

1.4 

1.0 

1.2 

1.1 

1.3 

PT/Ao 

0.7 

1.0 

0.7 

1.0 

1.0 

0.7 

Amvl (mm) 

2.7 

2.3 

2.8 

2.5 

2.8 

2.4 

Pmvl (mm) 

2.3 

2.0 

2.2 

3.5 

2.4 

2.5 

Vol LVs (mL) 

6.2 

6.0 

2.1 

7.8 

3.4 

4.9 

Vol LVd (mL) 

12.3 

14.4 

4.7 

15.2 

12.4 

13.9 

EF (%) 

49.3 

58.3 

55.0 

49.1 

72.4 

64.8 

EPSS (mm) 

5.5 

6.7 

4.9 

6.5 

5.1 

7.0 

Vmax Ao (m/s) 

1.2 

3.2 

1.2 

0.9 

0.9 

1.0 

Vmax P (m/s) 

0.7 

1.1 

0.8 

0.8 

0.6 

1.2 

Mitral E wave (m/s) 

0.9 

1.5 

0.9 

1.2 

0.9 

1.1 

Mitral A wave (m/s) 

0.3 

1.1 

0.7 

0.6 

0.4 

0.5 

E/A ratio 

3.0 

1.4 

1.4 

2.1 

2.1 

2.3 

DT (ms) 

89.0 

140.0 

162.7 

125.8 

83.5 

136.0 

Description of TTE parameters obtained by 2D-mode, M-mode and spectral Doppler mode in each gibbon (Nomascus spp.) evaluated. HR: heart rate; d: diastole; s: systole; IVS: interventricular septum; LV: left ventricular diameter; LVFW: left ventricular free wall; FS: fraction shortening; LA: left atrium; Ao: aorta; PT: pulmonary trunk; Amvl: anterior mitral valve leaflet; Pmvl: posterior mitral valve leaflet; EF: ejection fraction; EPSS: E-point to septal separation; DT: deceleration time

Table 3

Animal 

Mean 

SD 

Median 

Q1 

Q4 

Max 

Min 

HR (bpm) 

146.0 

15.1 

145.5

141.3 

151.3 

169.0 

123.0 

IVSd (mm) 

8.1 

3.6 

8.3

6.0 

8.6

14.2

3.6

LVd (mm) 

21.6 

5.8 

21.5 

19.8 

22.2 

31.3 

13.4 

LVFWd (mm) 

7.1 

1.8 

7.5 

5.8 

8.4 

9.1 

4.5 

IVSs (mm) 

9.5 

4.3 

9.3 

6.0 

12.5 

15.3 

4.6 

LVs (mm) 

15.4 

5.6 

14.6 

13.0 

16.3 

25.4 

8.8 

LVFWs (mm) 

9.7 

2.8 

9.3 

7.5 

11.0 

14.2 

6.8 

FS (%) 

29.7 

6.3 

32.4 

26.9 

34.2 

34.5 

18.9 

LA (cm) 

1.1 

0.2 

1.2 

0.9 

1.2 

1.2 

0.8 

Ao (cm) 

1.1 

0.2 

1.1 

1.0

1.2 

1.3 

0.9 

LA/Ao 

1.0 

0.2 

0.9 

0.9 

1.0 

1.2 

0.8 

PT (cm) 

1.0 

0.3 

1.0 

0.8 

1.2 

1.4 

0.6 

Ao (cm) 

1.1 

0.2 

1.2 

1.1 

1.3 

1.4 

1.0 

PT/Ao 

0.8 

0.2 

0.9 

0.7 

1.0 

1.0 

0.7 

Amvl (mm) 

2.6 

0.2 

2.6 

2.4 

2.8 

2.8 

2.3 

Pmvl (mm) 

2.5 

0.5 

2.4 

2.2 

2.5 

3.5 

2. 

Vol LVs (mL) 

5.1 

2.0

5.5 

3.8 

6.2 

7.8 

2.1 

Vol LVd (mL) 

12.2

3.8 

13.2 

12.3 

14.3 

15.2 

4.7 

EF (%) 

58.1

9.1 

56.7 

50.7 

63.2 

72.4 

49.1 

EPSS (mm) 

6.0

0.9 

6.0 

5. 

6.7 

7.0

4.9 

Vmax Ao (m/s) 

1.4 

0.9 

1.0 

1.0

1.2 

3.2 

0.9 

Vmax P (m/s) 

0.9 

0.2 

0.8 

0.7 

1.0 

1.2 

0.6 

Mitral E wave (m/s) 

1.1 

0.2 

01.0 

0.9 

1.2 

1.5 

0.9 

Mitral A wave (m/s) 

0.6 

0.3 

0.5 

0.4 

0.6 

1.1 

0.3 

E/A ratio 

2.1 

0.6 

2.1

1.6 

2.3 

3.0 

1.45 

DT (ms) 

122.8 

30.9 

130.9 

98.2 

139.0 

162.7 

83.5 

Descriptive statistics of parameters obtained by 2D-mode, M-mode and spectral-Doppler mode in 6 crested gibbons (Nomascus spp.). HR: heart rate; d: diastole; s: systole; IVS: interventricular septum; LV: left ventricular diameter; LVFW: left ventricular free wall; FS: fraction shortening; LA: left atrium; Ao: aorta; PT: pulmonary trunk; Amvl: anterior mitral valve leaflet; Pmvl: posterior mitral valve leaflet; EF: ejection fraction; EPSS: E-point to septal separation; DT: deceleration time

18Mild aortic and mitral insufficiencies without cavitary consequences were identified in a 15-year-old female Southern white-cheeked gibbon and a 5-year-old male Northern white cheeked gibbon (figure 3). Moreover, one 14-year-old female northern white cheeked gibbon was diagnosed with an apparently low fractional shortening (18.9%) (figure 3).

Figure 3

Figure 3

(A) M-Mode short axis transventricular view of individual 4 showing a decreased fractional shortening (18.9%) ; (B) 2D-Mode short axis view centered on the aorta and pulmonary artery of individual 2 showing an aortic insufficiency (arrowhead) (Ao: aorta; LA: left atrium; LV: left ventricle); (C) 2D-Mode long axis apical 2-chamber view of individual 3 showing a mitral insufficiency (arrow)

19Nonparametric two-sided Spearman tests showed a significant positive correlation between aortic diameter in diastole and both age (Spearman correlation: rs = 0.83; n = 6; P = 0.042) and weight (Spearman correlation: rs = 0.94; n =6 ; P = 0.005). A significant positive correlation was also identified between the weight of the animal and the thickness of the interventricular septum both in systole (Spearman correlation: rs = 0.88; n = 6; P = 0.019) and diastole (Spearman correlation: rs = 0.83; n = 6; P = 0.042). Finally, heart rate was positively correlated with age (Spearman correlation: rs = 0.89; n = 6; P = 0.019).

4 Discussion

20This study describes a basic and feasible TTE echocardiographic protocol in anesthetized crested gibbons, based on the methodology developed in great apes (Strong et al., 2015; 2018; 2021; Drane et al., 2019; 2020; Murphy et al., 2019; Atencia et al., 2020; Boyd et al., 2020; Cloutier et al., 2020), in an effort to better understand, diagnose and treat cardiovascular disease in this genera. It also establishes an initial database, with the assessment of 25 basic parameters in six crested gibbons and shows that subclinical cardiac disorders like valvular insufficiencies may be present in asymptomatic animals.

21Although it is well known that cardiovascular diseases are a major cause of mortality and morbidity in great apes, accounting for up to 10%, 43%, 41% and 45% of deaths in captive orangutans (Pongo spp.; Besnard et al., 2021), chimpanzees (Pan troglotydes; Gamble et al., 2004; Gamble & Terio, 2023), gorillas (Gorilla spp.; Meehan & Lowenstine, 1994) and bonobos (Pan paniscus) respectively (McManamon & Lowenstine, 2012; Lowenstine et al., 2016), and that standardized protocols for TTE, electrocardiography, and post-mortem evaluation of the cardiovascular system have been developed in this taxon (Strong et al., 2015; 2018; 2021; Drane et al., 2019; 2020; Murphy et al., 2019; Atencia et al., 2020; Boyd et al., 2020; Cloutier et al., 2020), cardiology knowledge in other NHP species is scarce, and often limited to clinical cases (Borkowski et al., 2000; Koenhemsi et al., 2012). Larger cohort studies in other NHP include reports of cardiac abnormalities in 25% of François’ Langur (Trachypithecus francoisi) housed in North American zoos (Flanders et al., 2016), as well as descriptions of echocardiographic parameters in various species like squirrel monkeys (Saimiri spp.; Locquet et al., 2020), macaques (Macaca spp.) (Ueda et al., 2017; Orlov et al., 2021) and baboons (Papio spp.) (Dennis et al., 2012). Only two publications report cardiopathies in hylobatids: Borkowski et al. (2000) describe a post-mortem diagnosis of myocardial fibrosis in a white-handed gibbon (Hylobates lar), and Kershaw et al. (2020) mention the diagnosis of three cardiopathies in a population of 33 gibbons (10% of the population), diagnosed during elective health checks with cardiac ultrasound performed based on clinical suspicion. To the best of the authors’ knowledge, there are currently no studies providing quantitative data on heart morphology and function nor publication mentioning prevalence of cardiovascular diseases in gibbons. The main objective of this study was hence to establish a basic TTE protocol and initial database of 25 parameters in clinically healthy animals undergoing general anesthesia using sevoflurane only for routine opportunistic general examinations.

22As the main goals of performing cardiac ultrasounds are to diagnose and monitor cardiac diseases and assess the effect of therapeutic interventions in primates with known cardiovascular disease, the cardiovascular effect of anesthetic agents selected needs to be considered amongst other factors (Boyd et al., 2020). According to Species360, the most commonly used anesthetic protocol in yellow-cheeked gibbons (N. gabriellae) and northern white-cheeked gibbons (N. leucogenys) is a combination of ketamine at a median-dose of 6.41 and 5.64 mg/kg respectively, and medetomidine at a median-dose of 0.06 and 0.05 mg/kg respectively (Species 360, 2022). Ketamine is a dissociative agent which increases heart rate and sympathetic tone, with minimal impact on echocardiographic cardiac indices (Boyd et al., 2020). However, medetomidine is an α-2 adrenergic agonist which is known to increase systemic vascular resistance and decrease heart rate and cardiac output (Rand et al., 1996). This may cause artefactual left ventricular dilation, systolic dysfunction, mitral valve regurgitation, and left atrial enlargement (Rand et al., 1996; Napier et al., 2013; Lopez del Rio et al., 2014; Ashley et al., 2021), and might place animals with significant systolic dysfunction at risk of acute deterioration. Effects of medetomidine have been described to be minimal to absent in chimpanzees if the examination is completed approximately 20-30 min after induction (Drane et al., 2021). An alternative anesthetic protocol was used in this study, i.e: sevoflurane without premedication. Discrete inotropic, lusitropic, and chronotropic effect of sevoflurane has been demonstrated in dogs (Kato et al., 2004), but the molecule seems to have minimal effect on echocardiographic parameters (Malan et al., 1994; Brioni et al., 2017). Other advantages of this anesthetic protocol include rapid induction and recovery after the procedure namely due to sevoflurane’s low blood-gas solubility (Pawson & Forsyth, 2008).

23Using the proposed method, 25 basic 2D-, M-Mode, and Doppler TTE parameters could be obtained in all six crested gibbons, with most measurements performed offline allowing limited image acquisition duration. All procedures lasted less than one hour, during which both echocardiographic examination and routine procedures like blood sampling, X-Rays, contraceptive implant removal or replacement and transponder identification were performed simultaneously. The mean of each parameter was determined, as well as their SD. SD were quite low, except for fractional shortening (29.7 ± 6.1%), ejection fraction (58.1 ± 9.3%), and deceleration time (122.8 ± 30.9 ms). This can be explained by the wide range of characteristics of animals evaluated due to opportunistic sampling. Animals included in this study included both juveniles and adults, with age ranging from 5 to 31 years old. Both males and females were evaluated, and weights ranged from 4.7 kg to 10.9 kg. Both age and body weight have been shown to have an impact on TTE parameters in small animal medicine (Sisson & Schaeffer, 1991; Morrison et al., 1992; Snyder et al., 1995; Misback et al., 2014; Borgeat et al., 2015; Häggström et al., 2016). Moreover, a wide variation in SD of some parameters is frequently described in primates (Napier et al., 2013; Sleeper et al., 2014).

24Overall, echocardiographic parameters obtained in the six crested gibbons evaluated in this study were similar to values obtained in awake Borneo Orangutans (Pongo pygmaeus) for the SF, EF, thickness of mitral valve leaflets, LA/Ao, peak velocity of aortic and pulmonary flow, early (E) and late (A) mitral flow, E/A ratio and deceleration time (Chetboul et al., 2022); anesthetized chimpanzees (Pan troglodytes) for SF, EF, early (E) and late (A) mitral flow, E/A ratio and deceleration time (Ashley et al., 2021; Drane et al., 2021); anesthetized gorillas (Gorilla gorilla) (Murphy et al., 2011; Napier et al., 2013); humans for EF (Lang et al., 2015), and companion animals for SF, LA/Ao, peak velocity of aortic and pulmonary flow, early (E) and late (A) mitral flow and E/A ratio (Serres et al., 2008).

25Body weight has been shown to have a significant effect on selected echocardiographic parameters in cats (Borgeat et al., 2015; Häggström et al., 2016) and dogs (Sisson & Schaeffer, 1991; Morrison et al., 1992; Snyder et al., 1995; Misbach et al., 2014). This coincides with the positive correlation observed between the weight of the evaluated gibbons and their IVS thickness both in systole and diastole and their aortic diameter. Absence of correlation between body weight and other parameters, namely LVFW thickness may be associated to the small sample size and interaction with other potential influencing factors like age or species. Allometric scaling may hence be interesting to predict echocardiographic dimensions in this genus (Häggström et al., 2016).

26Age had a significant effect on heart rate and aortic diameter in this study. Age is known to be an important factor that may influence intrinsic heart rate in humans (Kostis et al., 1982; Marcus et al., 1990; Mason et al., 2007) and animals (Ferasin et al., 2010; Hezzel et al., 2013). This can be explained by age-related changes in density of specific membrane currents, different activities of gap junctions and tissue fibrosis (Opthof, 2000). However, a larger sample with a wider range of ages would be necessary to confirm this hypothesis in crested gibbons. Age was also positively correlated with aortic diameter in the evaluated gibbons, which is explained in human medicine by tissue degeneration (Vasan et al., 1995; Alegret et al., 2006).

27Three mild heart functional abnormalities were diagnosed in this study: one mitral valve insufficiency in a five-year-old male Northern white-cheeked gibbon, one aortic insufficiency in a 15-year-old female Southern white-cheeked gibbon and a suspected cardiomyopathy in a 14-year-old female Northern white-cheeked gibbon characterized by a decreased fractional shortening as compared to the other gibbons evaluated and to data previously published in orangutans (Chetboul et al., 2022), chimpanzees (Sleeper et al., 2014; Drane et al., 2021) and companion animals (Fuentes, 2015). However, ejection fraction (49.1%) was conserved in this case, as compared to the other animals evaluated and to data previously published in orangutans (Chetboul et al., 2022), chimpanzees (Drane et al., 2021), gorillas (Murphy et al., 2011), companion animals (Serres et al., 2008), and humans (Lang et al., 2015). Interestingly, of the cardiopathies diagnosed, only the mitral valve insufficiency was associated with a discrete systolic heart murmur with a point of maximal impulse located at the level of the apex of the heart. Prevalence of cardiopathies is unknown in hylobatids. Only one study mentions 10% of cardiopathies in this order without further details (Kershaw et al., 2020). Moreover, to the author’s knowledge, this is the first study to describe heart function abnormalities in crested gibbons, with a 50% prevalence. However, it is difficult to determine whether the insufficiencies and decreased contractility observed in this study are pathological or physiological, as all animals evaluated were clinically healthy except for one heart murmur auscultated. Nonetheless, it is important to consider that heart diseases are most often subclinical until sudden death in apes (McManamon & Lowenstine, 2012). Complementary examinations such as cardiac troponin I testing on the animal with a suspected decreased contractility to confirm a cardiomyopathy, or systemic pressure measurement on the animal affected by an aortic insufficiency, to associate it to systemic hypertension, as often described in gorillas, could be interesting (McManamon & Lowenstine, 2012).

28This preliminary work on TTE in crested gibbons presents several limitations. Different species of Nomascus were evaluated in this study, with a heterogeneous distribution of sex, weight and age due to opportunistic sampling. All of these factors have been shown to impact heart function and morphology in small animal (Sisson & Schaeffer, 1991; Morrison et al., 1992; Snyder et al., 1995; Misbach et al., 2014; Borgeat et al., 2015; Häggström et al., 2016) and human medicine (Pfaffenberger et al., 2013). A larger and more homogeneous sample should therefore be evaluated to confirm the findings of this study and establish reference values for the genus to better interpret TTE results. Previous work on small animal TTE show that this exam is highly observer dependent (Chetboul et al., 2004). As cardiac evaluations were all performed by the same trained observer in this study, it is important to consider that the results presented here are only valid for the observer involved, and that veterinarians should determine their own TTE variability before undertaking echocardiographic examinations in gibbons. No repeatability and reproducibility analysis were carried out and should be determined in the future to evaluate the precision and accuracy of the results presented in this study. Finally, no newborn nor geriatric animal were included in this study, which may have created a bias in the prevalence of heart diseases diagnosed, as congenital defects, degenerative disorders and neoplasia may have been underestimated.

5 Conclusion

29This study demonstrates the feasibility of cardiac morphology and function evaluation using a simple and rapid TTE protocol allowing the assessment of 25 basic parameters, which can easily be performed during gibbon anesthesia. The protocol herein described may serve as an initial database for future clinical work. Moreover, this study shows that subclinical cardiac disorders such as valvular insufficiencies may be present in crested gibbons and should be further studied in future research. Based on these results, the authors would recommend performing routine TTE to early diagnose subclinical cardiovascular diseases in crested gibbons.

Acknowledgments

30The authors would like to thank the team of keepers from Mulhouse Zoo lemur section for their collaboration in this work.

Conflicts of interests

31The authors declare having no conflicts of interest to disclose.

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List of illustrations

Title Figure 1
Caption Anesthetized adult female yellow-cheeked gibbon (Nomascus gabriellae) placed in left lateral recumbency with the left arm extended cranially for echocardiographic examination, the probe being located between the 3rd and 4th intercoastal space just below the nipple for long axis apical views obtention.
URL http://journals.openedition.org/primatologie/docannexe/image/17740/img-1.png
File image/png, 7.5M
Title Figure 2
Caption (A) 2D-Mode: Short axis view centered on the aorta and pulmonary artery of individual 2 (LA: left atrium; RV: right ventricle; Ao: aorta; PT: pulmonary trunk); (B) 2D-Mode: Long axis apical 4-chamber view (RA: right atrium) of individual 4; (C) M-Mode: Short axis transventricular view (LVFW: left ventricular free wall; IVS: interventricular septum) of individual 4; (D) M-Mode: Short axis transmitral view (arrow: EPSS) of individual 3; (E) Transmitral flow visualized in pulsed-wave Doppler mode of individual 2; (F) Transpulmonary flow visualized in pulsed-wave Doppler mode of individual 4
URL http://journals.openedition.org/primatologie/docannexe/image/17740/img-2.png
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URL http://journals.openedition.org/primatologie/docannexe/image/17740/img-3.jpg
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URL http://journals.openedition.org/primatologie/docannexe/image/17740/img-4.jpg
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Title Figure 3
Caption (A) M-Mode short axis transventricular view of individual 4 showing a decreased fractional shortening (18.9%) ; (B) 2D-Mode short axis view centered on the aorta and pulmonary artery of individual 2 showing an aortic insufficiency (arrowhead) (Ao: aorta; LA: left atrium; LV: left ventricle); (C) 2D-Mode long axis apical 2-chamber view of individual 3 showing a mitral insufficiency (arrow)
URL http://journals.openedition.org/primatologie/docannexe/image/17740/img-5.png
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References

Electronic reference

Irène Vonfeld, Anaïs Nowakowski, Brice Lefaux and Benoît Quintard, Heart morphology and function evaluation by transthoracic echocardiography in six captive crested gibbons (Nomascus spp.)Revue de primatologie [Online], 15 | 2024, Online since 25 June 2024, connection on 24 June 2025. URL: http://journals.openedition.org/primatologie/17740; DOI: https://doi.org/10.4000/11vx9

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About the authors

Irène Vonfeld

Parc Zoologique et Botanique de Mulhouse, 51 rue du Jardin Zoologique, 68100 Mulhouse, France
Corresponding author: irene.vonfeld@gmail.com

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Anaïs Nowakowski

Parc Zoologique et Botanique de Mulhouse, 51 rue du Jardin Zoologique, 68100 Mulhouse, France

Brice Lefaux

Parc Zoologique et Botanique de Mulhouse, 51 rue du Jardin Zoologique, 68100 Mulhouse, France

By this author

Benoît Quintard

Parc Zoologique et Botanique de Mulhouse, 51 rue du Jardin Zoologique, 68100 Mulhouse, France

By this author

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