Pulmonary hypertension (PH), defined as abnormally elevated pressure within the pulmonary vasculature, is a clinically significant syndrome in humans1,2 and dogs.3 It has been documented in cats,4–12 although PH is more difficult to recognize in the feline species. Definitive diagnosis of PH requires right heart catheterization (RHC),13 which is impractical and very rarely performed in veterinary medicine. Instead, veterinary medicine relies on echocardiography as a noninvasive tool. The recent consensus statement on diagnosis, classification, treatment, and monitoring of PH in dogs proposed using tricuspid regurgitation (TR), echocardiographic evaluation of 3 anatomic sites (the ventricles, pulmonary trunk, and right atrium [RA]), and assessment of patient clinical signs to determine the probability of PH.3 This was a shift away from the traditional reliance on the measurement of TR as a sole metric for estimation of pulmonary arterial pressure (PAP)14 and quantification of PH,3 a measurement that is generally unsuitable for cats as they rarely have reliably measurable TR.4,10,12,14,15
Currently, the incidence and clinical significance of PH in cats are unknown, a shortcoming based largely on the lack of use of RHC and, when using echocardiography, the frequent absence of a measurable TR jet to estimate PH. In turn, this has prevented the development of feline-specific guidelines for the surveillance, diagnosis, treatment, and monitoring of PH.16 One recent study14 compared echocardiographic examinations of hyperthyroid and euthyroid cats and revealed differences in right-heart and pulmonary arterial hemodynamics, with no evidence of PH. Notably, this was a retrospective study, with the limitation that echocardiographic examinations of hyperthyroid cats were not specifically optimized for the characterization of right heart and pulmonary arterial hemodynamics. Additionally, certain parameters utilized in dogs, such as pulmonary artery flow profiles and right pulmonary artery distensibility index (RPADi), have not been prospectively investigated in cats,14 and these metrics may enhance the ability to recognize PH. To better characterize the incidence and significance of PH in cats, further investigation into practical and reliable methodology using echocardiography to assess the probability of PH is required.
The primary objective of this study was to prospectively investigate the feasibility and translatability of the echocardiographic 3-site metrics scheme from the canine PH guidelines3 to cats. A secondary aim was to determine whether echocardiographic differences consistent with PH existed between healthy cats and hyperthyroid cats. We utilized hyperthyroid cats as a subset of cats thought to be at risk for the development of PH, based on the translation of the relationship between hyperthyroidism and PH in humans. We hypothesized that adaptation of the canine scheme to determine the echocardiographic probability of PH3 would be useful to help identify the intermediate or high probability of PH in cats. We further hypothesized that hyperthyroid cats would have altered right-sided cardiac and pulmonary arterial hemodynamics assessed using echocardiography compared to age-matched healthy control cats, allowing assessment of intermediate or high probability of PH in a subset of hyperthyroid cats.
Methods
Study design
This single-center, prospective, observational case-control study was conducted at the University of Missouri Veterinary Health Center. This study was conducted in accordance with the University of Missouri’s Institutional Animal Care and Use Committee (protocol No. 10121).
Hyperthyroid cats were prospectively recruited from a population of cats presenting for radioactive iodine therapy. These cats were enrolled based on (1) a diagnosis of hyperthyroidism, confirmed by serum T4 measurement 4.0 μg/dL17 on the date of examination; (2) not receiving treatment for hyperthyroidism for at least 2 weeks preceding enrollment per institution protocol for radioactive iodine therapy; and (3) no evidence of concurrent thoracic, pulmonary, or other disease that could significantly impact the right heart or pulmonary arterial hemodynamics based on history, physical examination, and available diagnostics.16 Healthy control cats were prospectively enrolled based on (1) historical and current euthyroid status, confirmed by a serum T4 measurement ≤ 4.0 μg/dL on the date of examination; (2) no palpable thyroid slip; (3) no evidence of systemic disease based on physical examination, noninvasive systolic blood pressure obtained via Doppler, CBC, serum chemistry panel, and urinalysis; (4) treatment with year-round heartworm prevention; and (5) age of ≥ 8 years old at time of enrollment. Informed consent was obtained before enrollment.
Echocardiography
Transthoracic echocardiography with electrocardiographic monitoring was prospectively performed with a conventional echocardiographic system using a 12-MHz phased array probe (Vivid E90; GE Healthcare) and interpreted by a single board-certified veterinary cardiologist (KW). Patients were gently restrained in right and left lateral recumbency. Sedation with butorphanol (up to 0.5 mg/kg administered once IV or IM) was permitted if needed. Standard echocardiographic images and measurements as well as right atrial area index (RAAi), tricuspid annular plane systolic excursion (TAPSE), RPADi, main pulmonary artery diameter-to-aortic diameter ratios (MPA:Ao), and main pulmonary artery pulsed-wave flow profiles (MPA-PW Doppler) were obtained as previously described.18–22 The tricuspid valve was interrogated in multiple imaging planes to ensure adequate alignment with regurgitant jets, when present. Peak tricuspid regurgitation flow velocity (TRFV) of > 3.4 m/s was used as a supportive criterion for intermediate or high probability of PH.3 Interrogation of pulmonary flow velocity profiles was performed by placing pulsed-wave Doppler sample volume centrally and just distal to the pulmonic valves.22 Pulmonary artery flow profiles were classified as normal (type I) if there was a symmetric envelope with similar acceleration and deceleration time; accelerated (type II) if there was an asymmetric envelope due to peak velocity early in systole with shortened acceleration time; notched (type III) if there was an asymmetric envelope with rapid acceleration and notching during deceleration; or late peaking if there was an envelope that reached peak velocity at the end of systole.23,24 Echocardiographic parameters were recorded as the average of 3 high quality but not necessarily consecutive measurements. Systolic PAP was estimated utilizing the modified Bernoulli equation as previously described.3 A hypertrophic cardiomyopathy phenotype was defined as segmental or regional wall thickness > 6 mm.25
Statistical analysis
Analyses were performed using a statistical analysis software package (SAS version 9.4; SAS Institute Inc.). Demographic and echocardiographic numerical variables were compared between control and hyperthyroid groups using the Kruskal-Wallis test. Results are reported as median (IQR), unless stated otherwise. Categorical variables were compared between control and hyperthyroid groups with Fisher exact test. P < .05 was considered statistically significant.
Results
Animals
Eleven euthyroid cats and 16 hyperthyroid cats met the entry criteria for inclusion. No cats had clinical signs or physical examination findings consistent with respiratory disease. Demographic and physical examination data are reported (Table 1). The euthyroid group included the breeds American domestic shorthair (n = 8) and American domestic medium hair (1), American domestic longhair (1), and Siamese (1). Breeds in the hyperthyroid group included American domestic shorthair (n = 8), American domestic longhair (6), Siamese (1), and Manx (1). Of the hyperthyroid cats, 13 had received treatment with methimazole before presentation for radioactive iodine therapy ranging in duration from 0.2 to 18 months (median of 2 months). All cats were neutered. Half of the hyperthyroid cats had a palpable thyroid slip. Although body condition scores between the 2 groups did not differ significantly (P = .07), body weight was significantly lower in the hyperthyroid group, compared to the healthy control group (P = .03). There were no other statistically significant differences in demographic or physical examination findings between the 2 groups.
Demographic and physical examination data for 27 cats (healthy [n = 11] and hyperthyroid [16]) undergoing echocardiographic examinations to investigate differences in echocardiographic parameters relating to right-sided cardiac and pulmonary arterial hemodynamics.
| Variable | Healthy (n = 11) | Hyperthyroid (n = 16) | P value |
|---|---|---|---|
| Demographics | |||
| Age (y) | 11 (8.5, 13) | 13 (11, 14) | .08 |
| Sex (female/male) | 5/6 | 10/6 | .45 |
| Body weight (kg)a | 5.3 (4.6, 7) | 4.3 (3.5, 5.1) | .03 |
| BCS | 7 (6, 7) | 5 (3.5, 7.5) | .07 |
| Physical examination | |||
| Rectal temperature (°F) | 101.9 (100.5, 102.2) | 102.2 (100.4, 102.5) | .64 |
| Heart rate (bpm) | 190 (180, 210) | 204 (188, 220) | .31 |
| Respiratory rate (rpm) | 30 (30, 60) | 40 (36, 60) | .13 |
| Heart murmurs: number (%) | 4 (25) | 12 (75) | .06 |
| Grade I | 1 | 1 | |
| Grade II | 2 | 2 | |
| Grade III | 1 | 9 |
Data are represented as median (IQR) unless specified otherwise.
BCS = Body condition score.
Value with a superscript is significantly (P < .05) different.
Systolic blood pressure and serum T4 measurements
Systolic blood pressure ranged from 110 to 160 mmHg (median, 130 mmHg) in healthy cats and 110 to 210 mmHg (median, 155 mmHg) in hyperthyroid cats. Circulating T4 concentrations ranged from 2.1 to 3.5 μg/dL (median, 2.4 μg/dL) in healthy cats and 5.3 to 49 μg/dL (median, 10.8 μg/dL) in hyperthyroid cats. Both systolic blood pressure and T4 measurements were significantly greater in hyperthyroid cats, with P = .02 and P < .0001, respectively.
Echocardiographic data
Echocardiographic data from healthy and hyperthyroid cats are summarized (Table 2). Two euthyroid cats and no hyperthyroid cats required sedation. Hyperthyroid cats had a significantly (P = .0004) greater RAAi than healthy cats. Diagnosis of a hypertrophic cardiomyopathy phenotype was made in 6 hyperthyroid cats and no healthy cats (P = .054). Out of all cats, only 1 hyperthyroid cat (serum total T4 concentration of 27.1 μg/dL) had a high probability of PH. The high probability of PH in this cat was based on TRFV > 3.4 m/s and a type II MPA-PW Doppler flow profile. One additional hyperthyroid cat (serum total T4 concentration of 8.8 μg/dL) had measurable TR with a low probability of PH. The low probability of PH in this cat was based on an otherwise unremarkable echocardiographic exam. Among healthy cats, 6 had visible but not measurable TR, and 5 had no noted TR. In the hyperthyroid group, 8 cats had visible but not measurable TR, and 6 had no noted TR. Pulsed-wave Doppler profiles of the pulmonic valve demonstrated a significant difference between profile types, with 10/11 healthy cats exhibiting type I profiles and 9/16 hyperthyroid cats exhibiting late-peaking profiles (P = .003). Right pulmonary artery distensibility index was below 30% for all cats except 1 hyperthyroid cat. This was the same cat who had a high probability of PH. The remainder of the echocardiographic parameters were not significantly different between groups. Right pulmonary artery distensibility measurements (diastolic RPAD, systolic RPAD, and RPADi) were technically difficult to acquire and measure but were collected in all but 1 hyperthyroid cat. Main pulmonary artery-to-aorta ratios were also technically difficult to acquire but were collected in all cats.
Echocardiographic data for healthy and hyperthyroid cats.
| Parameters | Healthy (n = 11) | Hyperthyroid (n = 16) | P value |
|---|---|---|---|
| Ventricles | |||
| RV size | Normal | Normal | |
| TAPSE | 8.40 (7.10, 9.70) | 9.45 (8.35, 10.05) | .14 |
| SF | No | No | |
| LVIDd (mm) | 15.40 (12.80, 17.20) | 14.80 (13.90, 15.90) | .71 |
| LVIDs (mm) | 6.40 (4.70, 8.00) | 5.90 (5.35, 7.15) | .64 |
| LVPWd (mm) | 4.40 (3.90, 4.70) | 4.40 (4.10, 5.40) | .35 |
| IVSd (mm) | 4.00 (3.50, 4.40) | 4.20 (3.85, 4.80) | .25 |
| Right atrium | |||
| RAA (cm2) | 1.24 (1.10, 1.40) | 138 (1.14, 1.82) | .14 |
| RAA indexa | 3.78 (3.71, 4.71) | 5.51 (4.93, 5.79) | .0004 |
| Pulmonary circulatory characteristics | |||
| TR | .71 | ||
| Present | 6 | 10 | |
| Measurable | 0 | 2 | |
| RPADs (mm) | 6.30 (5.50, 6.50) | 5.80 (4.70, 6.80) | .42 |
| RPADd (mm) | 4.80 (4.40, 5.30) | 4.20 (3.70, 5.40) | .27 |
| RPADi (%) | 20.30 (18.30, 22.10) | 21.70 (20.20, 26.90) | .25 |
| MPA (mm) | 7.00 (6.50, 7.60) | 7.54 (6.74, 7.97) | .32 |
| AoD (mm) | 9.50 (9.00, 10.90) | 9.57 (8.92, 9.99) | .64 |
| MPA:Ao | 0.73 (0.68, 0.77) | 0.77 (0.71, 0.90) | .13 |
| MPA PWb | .003 | ||
| Type I | 10 | 5 | |
| Type II | 1 | 2 | |
| Type III | 0 | 0 | |
| Late peaking | 0 | 9 | |
| PI | Not present | Not present | |
| Left-sided cardiac structures | |||
| LAD (mm) | 14.10 (13.20, 14.60) | 14.30 (12.95, 15.71) | .84 |
| LA:Ao | 1.30 (1.20, 1.41) | 1.34 (1.21, 1.44) | .82 |
AoD = Aortic diameter. IVSd = Interventricular septum thickness in diastole. LAD = Left atrial diameter. LA:Ao = Left atrium-to-aortic ratio. LVIDd, s = Left ventricular internal dimension at end diastole, systole. LVPWd = Left ventricular posterior wall at end diastole. MPA = Main pulmonary artery diameter. MPA:Ao = Main pulmonary artery-to-aorta ratio. MPA PW = Main pulmonary artery pulsed wave Doppler tracing. PI = Pulmonic insufficiency. RAA = Right atrial area. RPADi = Right pulmonary artery distensibility index. RPADs, d = Right pulmonary artery diameter in systole, diastole. RV = Right ventricle. SF = Septal flattening. TAPSE = Tricuspid annular plane systolic excursion. TR = Tricuspid regurgitation.
Values with different superscripts are significantly (P < 0.05) different.
See Table 1 for remainder of key.
Discussion
This study documented the feasibility of an expanded echocardiographic approach to survey for the probability of feline PH in healthy and hyperthyroid cats. The approach followed the canine 3-site metrics scheme3 and investigated for peak TRFV > 3.4 m/s in conjunction with changes to 3 echocardiographic sites: the ventricles, pulmonary trunk, and RA. Additional echocardiographic metrics are needed in cats due to the frequent absence of a measurable TR jet to estimate PH, as was also shown in this study (ie, 0/11 healthy cats and only 2/16 hyperthyroid cats had measurable TR jets; Table 2). Relevant challenges associated with the current use of the 3-site metrics scheme in cats included the lack of feline-specific reference values, technical difficulty of acquisition of RPADi and MPA:Ao measurements, and the possibility that cats manifest changes as a consequence of PH differently than dogs, in which case alternative metrics might need to be considered. Regardless, differences in right-sided cardiac and pulmonary arterial hemodynamics between healthy and hyperthyroid cats were noted, specifically an increased RAAi and pulmonic valve interrogation documenting a significant difference between profile types. Using this more comprehensive echocardiographic approach, 1 hyperthyroid cat had a high probability of PH. Despite speculating that hyperthyroid cats would be a population more likely to have echocardiographic evidence of intermediate to high probability PH using this scheme, this was not supported by our results.
Application of the 3-site metrics scheme3 to cats was feasible. Images fulfilling expanded metrics were successfully obtained in all cats, with the exception of RPADi in 1 hyperthyroid cat, which was unobtainable. Certain echocardiographic parameters derived from the canine consensus statement3 were relatively easy to obtain or evaluate in this cat population. Such parameters include RAAi,18 the presence or absence of septal flattening, subjective evaluation of right ventricular (RV) hypertrophy (wall thickening, chamber dilation, or both),26,27 and TAPSE.20 Both RPADi28 and MPA:Ao22 measurements were technically difficult and more time consuming to obtain compared to dogs. Difficulty in image acquisition was related primarily to challenges in obtaining images containing adequate resolution of the endothelial margins to allow for accurate measurements. These regions (ie, right branch pulmonary artery and main pulmonary artery) often required prolonged interrogation (duration of image acquisition was not measured in this study; however, image acquisition subjectively took about 1.5 times as long as a standard feline echocardiographic exam) with obliqued echocardiographic imaging planes. This highlights a potential practical limitation of collecting RPADi and MPA:Ao in an uncooperative or unstable cat.
Tricuspid annular plane systolic excursion has been validated against invasive methods as a marker of RV systolic function in human medicine.29 This measurement provides important prognostic information for patients with PH, with values below 1.8 cm correlating with reduced survival time. Because of the important prognostic information, TAPSE is recommended as a portion of the routine echocardiographic assessment of humans with PH.30 Similarly, TAPSE is recognized to be significantly decreased in dogs with PH compared to dogs without PH.20 To date, assessment of TAPSE has been reported infrequently in cats4,31 and is not routinely obtained during standard feline echocardiographic examinations. A retrospective study4 that investigated the presence of PH in cats with left-sided congestive heart failure reported TAPSE in less than 60% of echocardiographic exams, likely based on the retrospective nature of data collection. Of note, these retrospectively reported feline TAPSE values were similar to values collected in the current study. Together, these data support the continued development of feline-specific TAPSE reference values using a large population of healthy control cats to strengthen the optimization and understanding of feline right-heart echocardiographic findings.
Right pulmonary artery distensibility indices were collected in 26/27 cats in this study. While specific cut-off values differ between canine and human reports, the consensus that pulmonary artery distensibility is greater in healthy controls than in cases of PH remains consistent.3,21,28,32,33 In dogs, RPADi < 30% is highly suggestive of PH. Conversely, dogs with an RPADi > 35% have been found to have normal PAP.28 Interestingly, 25/26 cats in our population had an RPADi of < 30% (ranging from 15.1 to 29.3%) with no other echocardiographic evidence to support an intermediate or high probability of PH. In contrast, the single cat in our population with a high probability of PH had an RPADi > 30%. The underlying mechanisms influencing RPADi in cats have not yet been investigated. However, the authors propose the consideration that RPAD may be partially influenced by factors hypothesized to influence systemic hypertension in hyperthyroid cats. Such factors include decreased systemic vascular resistance, stimulation of the renin-angiotensin-aldosterone system causing expanded intravascular volume, and increased vessel wall stiffness. While the specific mechanisms remain unknown and were not investigated in this study, our results suggest that RPADi in cats may behave dissimilarly to dogs and humans,32,34 and again highlight the need for the development of feline-specific reference values in healthy cats and comparison to RPADi in cats with a high probability of or invasively confirmed PH.
As described above, our study population of healthy and hyperthyroid cats documented 1 hyperthyroid cat with a high probability of PH based on echocardiography. The high probability of PH in this cat was based on TRFV > 3.63 m/s and a type II MPA-PW Doppler profile. Per the canine guidelines,3 peak TRFV > 3.4 m/s with 1 or more concurrent echocardiographic signs of PH in the 3 anatomic sites indicates a high probability of PH. The remaining healthy and hyperthyroid cats had subtle differences detected among echocardiographic parameters of right heart and pulmonary arterial hemodynamics, with significant differences in RAAi and MPA-PW Doppler profile types, with a low probability of PH. The significantly higher RAAi in hyperthyroid cats (P = .0004) is likely a reflection of the significantly lower body weight in this group (P = .03), rather than a reflection of truly altered right heart size or hemodynamics given that RAA did not differ between groups. Conversely, the significant difference detected between MPA-PW Doppler profile types in healthy and hyperthyroid cats (P = .003) is considered to be indicative of altered hemodynamics between these 2 groups. Healthy cats were more likely to exhibit type I profiles while hyperthyroid cats were more likely to exhibit late-peaking profiles. Late-peaking profiles are consistent with hyperdynamic circulation, and in this population, similar to the retrospective study14 that evaluated healthy and hyperthyroid cats for PH, hyperdynamic circulation is thought to be a result of hyperthyroidism rather than PH.35 This prior retrospective study14 documented a significant increase in acceleration time-to-ejection time ratios when comparing hyperthyroid to euthyroid cats. An increased acceleration-to-ejection time ratio is consistent with a late-peaking profile and was speculated to potentially be a result of dynamic RV outflow tract obstruction.35 In our prospective population, only 1 hyperthyroid cat was documented to truly have dynamic RV outflow tract obstruction (late-peaking profiles within the distal RV > 1.7 m/s) with the remaining cats displaying late-peaking profiles within the proximal main pulmonary artery, leading us to believe that the late-peaking profiles, while not necessarily an indicator of PH, support altered hemodynamics associated with a hyperthyroid state.
This study had several limitations. First, one significant limitation was surveillance of the most at-risk population of cats. We selected hyperthyroid cats as a population considered likely to have PH, albeit without definitive confirmation of PH using RHC, which is not practically performed in pet cats. The possibility of being a high-risk population was based on extrapolation from human medicine, as 35 to 65% of hyperthyroid humans develop PH.36,37 This work suggests that hyperthyroid cats behave dissimilarly to hyperthyroid humans, and are unlikely to develop PH. Future studies could consider echocardiographic application of the American College of Veterinary Internal Medicine consensus statement guidelines in dogs3 to cats with experimentally induced PH that is confirmed with cardiac catheterization, and subsequently apply these findings to a larger population of hyperthyroid cats. Second, it is recognized that cats often behave dissimilarly to dogs, and it must be considered that cats may manifest PH differently than dogs. The canine consensus guidelines mandate that dogs demonstrate clinical signs suggestive of PH (eg, respiratory signs, exercise intolerance) in conjunction with echocardiographic changes to be considered to have a high probability of PH.3 This may affect surveillance of at-risk cats, as some cats with severe respiratory disease can be apparently asymptomatic due to their sedentary nature (for example, exercise intolerance is often very challenging to assess in cats). It is unclear if cats are able to compensate for, or mask, clinical signs relevant to PH more effectively than dogs. Additionally, there is likely variation between echocardiographic findings of PH between cats and dogs, supported by discrepant RPADi values. This variation, in the absence of feline-specific reference ranges, poses a limitation in the current surveillance of cats for PH. Third, it is possible that the evaluation of a larger population of cats and the evaluation of cats experiencing thyrotoxicosis or exhibiting respiratory signs may have increased the chances of uncovering PH. Fourth, the single investigator performing echocardiographic exams was aware of the thyroid status of all cats, possibly inducing an information bias. Fifth, interobserver and intraobserver reliability was not determined, although understanding possible variations between collected measurements, particularly RPADi and MPA:Ao, would be beneficial. Sixth, invasive pressure measurements such as RHC were not performed to definitively rule PH in or out in any of the included cats.
In conclusion, the application of an expanded echocardiographic approach was feasible to investigate altered right-sided cardiac and pulmonary arterial hemodynamics in hyperthyroid and healthy cats. Similar to other studies, most hyperthyroid and healthy cats did not have a measurable TR jet to estimate systolic pulmonary arterial pressure, making alternate echocardiographic metrics to estimate the probability of PH appealing. Results suggest that hyperthyroid cats are not an ideal model to evaluate metrics for detection of PH in cats, as hyperthyroid cats appear dissimilar to hyperthyroid humans, who are likely to develop PH.38 Echocardiographic metrics obtained from healthy cats in this study are the first step to generating feline-specific reference values that can be used to assess PH probability in cats with chronic bronchopulmonary and primary pulmonary parenchymal diseases,16 where PH may be more likely. Future studies in cats suspected to have PH could also consider using expanded echocardiographic metrics such as myocardial strain and speckle tracking.
Acknowledgments
None reported.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
This research was funded by the University of Missouri College of Veterinary Medicine, Committee on Research Clinician Scientist grant.
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