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Abstract

The qualitative and quantitative aspects of femoral artery blood flow waveform spectra were evaluated in 15 male and 15 female Persian and mixed breed domestic cats (Felis catus), which were healthy and not sedated, using duplex Doppler ultrasonography (DDU). Spectral Doppler demonstrated a biphasic characteristic in 16 (53.34%) of the animals evaluated, and a triphasic characteristic in the 14 (46.66%) remaining animals. The systolic blood pressure and heart rate values were within the normal range for the species. The quantitative parameters evaluated, based on the spectral Doppler, were as follows: systolic velocity peak (SVP), recent diastolic velocity peak (RDVP), end diastolic velocity peak (EDVP), mean velocity (MV), integral velocity time (ITV), artery diameter (AD), femoral flow volume (FFV), pulsatility index (PI), resistive index (RI), systolic peak acceleration time (AT) and deceleration time (DT). The respective mean values were: 36.41 ± 7.33 cm/s, 4.69 ± 0.90 cm/s, 10.74 ± 2.74 cm/s, 23.06 ± 4.86 cm/s, 3.91 ± 1.05 cm, 0.17 ± 0.04 cm, 0.11 ± 0.08 cm³, 3.85 ± 0.19, 1.40 ± 0.20, 39.84 ± 7.38 ms, and 114.0 ± 22.15 ms. No significant differences were found between males and females. The analyses carried out on the femoral artery flow spectrum obtained by DDU showed that it is easy to use and highly tolerated in non-sedated, healthy cats. It appears that DDU may be a useful diagnostic technique, but further studies are needed to evaluate how it compares with invasive telemetric methodology or high-definition oscillometric waveform analytic techniques.

Introduction

Various non-invasive imaging modalities, including magnetic resonance angiography (MRA), computed tomography (CT) and duplex Doppler ultrasound (DDU) are commonly used for the diagnostic work-up of patients with peripheral arterial diseases.¹ Although MRA and CT are frequently used in medicine, DDU has proven to be a cost-effective and accurate approach for detecting changes in the vascular peripheral flow profile in animals^2,3 and humans.^1,4 It is also attractive because it is a painless screening diagnostic tool.

DDU analysis of femoral artery flow can be used as an investigative method for the detection of arteriosclerosis, similar to the carotid artery in humans. This disorder often correlates with systemic diseases known to change the quality of blood flow, such as type 2 diabetes,⁵ arterial hypertension,⁶ hyperthyroidism⁷ and obesity.⁸ In domestic felines, hypertrophic cardiomyopathy (HC) presents mainly as left ventricular hypertrophy, left atrium dilatation and arterial thromboembolism.^9,10 Thus, diseases such as hyperthyroidism and systemic hypertension should be considered in the differential diagnosis for HC because they can induce modest septal hypertrophy and concentric left ventricular hypertrophy, respectively.¹⁰ In cats with HC, the disruption of the endocardial surface exposes collagen, von Willebrand’s factor and tissue factor, which trigger the generation of cellular debris and fibrin formation, which can damage subendocardial tissues and lead to thrombus development. In addition, atrial enlargement associated with HC modifies blood flow, leads to blood stasis or turbulent flow and coagulation, and contributes to the formation of left atrial thrombi. Another important factor for intracardiac thrombi development is alteration in blood composition. Platelet hyperaggregability (inherited or acquired), coagulation protein or platelet defects can predispose animals to thromboembolisms events.^9–11 The thrombus can eventually dislodge and travel through the systemic vasculature, where it can obstruct blood flow to the femoral and other peripheral arteries.^10,11 Obesity and type 2 diabetes mellitus have been shown to predispose individuals to arteriosclerosis. The resulting adipose tissue accumulation, hypertriglyceridemia, hyperglycemia and oxidant stress alter the immune system and cause a state of chronic inflammation. This condition leads to changes in the systemic, regional and local elasticity of the vessel walls, thereby hindering blood flow to central vessels.^12–14 Previous studies have assessed alterations related to peripheral blood circulation perfusion in veterinary patients with heart failure.^2,15,16

DDU allows real-time, non-invasive evaluation of vascular anatomy and blood flow morphology, which enables the measurement of both quantitative and qualitative parameters.^17,18 Qualitative analyses are related to the identification of the spectrum of the waves formed, in which specific characteristics are recognized for each vessel.^19,20 Thus, the identification and recognition of the Doppler signal emitted from the blood flow in each vessel becomes important, particularly when changes in the local hemodynamics due to peripheral or systemic diseases are addressed. Therefore, using DDU to understand the blood flow characteristics of individual vessels in each animal species is important.

Among the quantitative variables, pulsatility index (PI) and resistive index (RI) merit special emphasis because of their close correlation with arterial capacitance measurements, which serve as non-invasive indicators of peripheral vascular resistance.^21,22 In domestic felines, a few publications have reported successfully obtaining a quantitative and qualitative hemodynamic profile of blood flow in peripheral arteries using DDU. The femoral artery is the main vessel responsible for pelvic limb perfusion in domestic felines, and variations in the blood flow waveforms may be related to common diseases in this species. Therefore, the aim of this study was to investigate the characteristics of femoral artery blood flow in healthy, non-sedated domestic felines using DDU.

Materials and methods

Animals

We assessed 30 (15 male and 15 female) healthy Persian and mixed breed domestic felines of different ages and weights, and which had been castrated or spayed within a minimum period of 1 year prior to inclusion in the study. All animals originated from the Cardiology Service of a Veterinary Teaching Hospital in the Federal University of Lavras. The study was evaluated by the bioethics committee (NINTEC/PRP) and approved under protocol 010/2012. The animals underwent a complete physical examination prior to their inclusion in this study, which included mucous membrane color and capillary refill time, auscultation and thyroid palpation. Only healthy animals were included. Each animal had its systolic blood pressure estimated, and then received electrocardiographic evaluation and conventional echocardiography without sedation or anesthesia.

Measurement of systolic blood pressure

The animals were first acclimatized in the examination room, and then had their systolic blood pressure measured non-invasively to minimize stress interference with blood pressure values. Pressure was measured using a Doppler (DV2000 Table top vascular Doppler; Medpej) device with an 8 MHz transducer. The animals were restrained in left lateral decubitus with application of the cuff in the proximal portion of the radial bone to compress the common digital artery. Five Doppler measurements were taken, and the mean values calculated as described previously.²³

Electrocardiography

Heart rate and cardiac rhythm were evaluated using conventional electrocardiography (EGC12S; Ecafix) as described previously.²⁴ All animals were positioned in right lateral recumbency, on an appropriate table, with limbs positioned perpendicular to the trunk. The electrodes were attached to fore limbs and hind limbs. The speed used was 50 mm/s, with calibration of the voltage as 1 cm for each mV (ie, 1 mV = 1 cm).

Transthoracic echocardiography

The cats were restrained manually in the lateral decubitus position. Equipment (Mylab 40; Esaote) featuring 3–11 MHz sector transducers was used to capture images in the two-dimensional (2D) mode, M-mode, color Doppler, pulsed-wave and continuous wave Doppler, as described previously.²⁵ The electrodes were attached to the extremities of the pelvic and thoracic limbs for simultaneous electrocardiography.

The dimensions of the aortic root (Ao), the left atrial diameter (LA) and the LA/Ao ratios were determined in the 2D mode, right parasternal view. The thicknesses of the interventricular septum (IVS) and the left ventricular free wall (LVFW) were measured in the short axis of the same echocardiographic window. The morphological aspects of mitral, tricuspid, pulmonary and aortic valves were investigated using the 2D mode in different echocardiographic sections. Blood flow was assessed in the heart valves and IVS for the exclusion of animals with anomalous flow in any of these segments using color Doppler, and continuous and pulsed-wave Doppler.²⁵ The ejection fraction was calculated based on Simpson’s method, and the shortening fraction was measured by M-mode according to previous recommendations.²⁵ All measurements were taken five times, and means calculated.

Duplex Doppler ultrasonographic evaluation of the right femoral artery

The animals were restrained manually in right lateral decubitus, and the right femoral artery pulse was identified by digital palpation to confirm the anatomical location. A commercial DDU machine was used (Mylab 40; Esaote), which was equipped with linear transducers at a frequency of 5–11 MHz. The Doppler spectrum was obtained in the proximal portion of the right femoral artery with the transducer positioned parallel to the reported vessel, 1–2 cm after its perception, on the medial surface of the limb. The hair from the region was removed by local trichotomy. In the 2D mode, the arterial lumen was identified as an anechoic area delimited by hyperechoic, pulsatile walls. The color Doppler mode was used to confirm the existence of flow and for a more accurate determination of the vessel’s delimitations. The ultrasound beam was positioned in a region of larger arterial diameter with the sample volume placed in the center of the vessel. The Doppler angle was fixed at 25° with respect to the long axis of the artery. After identification of the femoral spectrum, all images and waveforms were stored on the ultrasonic device for ‘off-line’ analyses. For the images collected, the following parameters were determined: mean velocity (MV), systolic velocity peak (SVP), recent diastolic velocity peak (RDVP), end diastolic velocity peak (EDVP), acceleration time (AT) and deceleration time (DT) of the systolic peak, integral velocity time (ITV), arterial diameter (AD) and femoral flow volume (FFV). The femoral area (FA) was obtained using the formula: FA = π (AD/2)². The FFV was obtained using the following formula: FFV = FA × TVI. The SVP, AT and DT were obtained directly from the generated spectra. PI and RI measurements were taken using a commercially available software package.³ For each examination, three distinct pulsed-wave spectral tracings containing three nonconsecutive cardiac cycles were recorded and the mean value determined.

Statistical analysis

The data obtained for sex, breed and age were used for frequency analysis. For the other variables of descriptive statistic processes, the values of the means, as well as the minimum and maximum SDs, were determined. The data were separated into two categories: males and females. The normality of distribution was evaluated using the Shapiro–Wilk test. When normal, the variables were compared using the unpaired Student’s t-test. For the variables that did not achieve normality, the data were compared using the Mann–Whitney test. The correlation (Pearson or Spearman tests) observed the normality study and were conducted for the different variables obtained by DDU. Intra-observer reproducibility was evaluated using a 3-day interval for the different parameters with different Doppler spectra of the femoral artery, in the off-line images, by analysis of the coefficient of variation between repeated measures. The variability was defined using an intra-observer variability coefficient (IVC) between days, where an IVC <15% indicated low variability, an IVC between 15% and 25% indicated moderate variability, and an IVC >25% indicated high variability.²⁶ All statistical analyses were carried out using SPSS version 17.0 for Windows.

Results

The mean values obtained for age, weight, heart rate and systolic blood pressure were 36 ± 32.90 months, 3.9 ± 0.97 kg, 153 ± 32.99 beats per minute and 125.47 ± 16.39 mmHg, respectively. There were no statistical differences between males and females in the physiological parameters assessed (Table 1).

Table 1

Values (mean ± SD) of age, weight and variables obtained through ultrasonography of the femoral artery of healthy cats

Variable	Sex*		General mean value	P
	Male (n = 15)	Female (n = 15)	General mean value	P
Age (months)	34.46 ± 34.06	38.40 ± 32.76	36.43 ± 32.94	0.75
Weight (kg)	4.28 ± 1.14	3.67 ± 0.67	3.97 ± 0.97	0.08
AD (cm)	0.16 ± 0.03	0.18 ± 0.04	0.17 ± 0.04	0.38
SVP (cm/s)	37.80 ± 6.48	31.80 ± 8.69	36.41 ± 7.33	0.06
RDVP (cm/s)	5.10 ± 0.92	4.39 ± 0.31	4.69 ± 0.90	0.11
EDVP (cm/s)	11.18 ± 2.15	9.20 ± 3.03	10.74 ± 2.74	0.36
MV (cm/s)	23.31 ± 5.75	17.87 ± 5.90	23.06 ± 4.86	0.73
ITV (cm)	3.88 ± 0.99	3.07 ± 1.15	3.91 ± 1.05	0.10
FFV (cm³)	0.11 ± 0.08	0.07 ± 0.04	0.11 ± 0.08	0.18
PI	3.4 ± 0.62	4.12 ± 0.72	3.85 ± 0.19	0.09
RI	1.41 ± 0.81	1.40 ± 0.78	1.40 ± 0.20	0.12
AT (ms)	42.50 ± 6.95	37.39 ± 7.11	39.84 ± 7.38	0.05
DT (ms)	116.20 ± 23.45	112.79 ± 19.23	114.0 ± 22.15	0.66
SAP (mmHg)	125.20 ± 20.85	125.72 ± 12.08	125.47 ± 16.39	0.94

AD = arterial diameter; SVP = systolic velocity peak; RDVP = recent diastolic velocity peak; EDVP = end diastolic velocity peak; MV = mean velocity; ITV = integral velocity time; FFV = femoral flow volume; PI = pulsatility index; RI = resistive index; AT = acceleration time of systolic peak (SP); DT = deceleration time of SP; SAP = systemic systolic blood pressure

Based on clinical examination, All animals in this study were healthy. None of the animals exhibited any increase in thyroid hormone levels, and all had normal cardiac sinus rhythms without evidence of a wandering pacemaker. Based on the transthoracic echocardiogram examination, the individuals included in this study all lacked free fluid in the thoracic, pleural and pericardial cavities. The heart valves did not present thickening in any of their leaflets, and no systolic anterior motion in the cranial leaflet of the mitral valve was observed. In the color Doppler mode, the transvalvular blood flows were normal, with an absence of regurgitation and swirling, which was in agreement with the previous cardiac auscultation. Pulsed-wave Doppler confirmed the absence of regurgitating flows.

The femoral artery in the animals appeared, in the 2D mode, as an anechoic structure with thin hyperechogenic walls and was differentiated from the femoral vein by the pulsatile characteristic of the artery. No structures that resembled thrombi or atheromatous plaques were found in any animal.

The quantitative hemodynamic parameters obtained through DDU of the femoral artery and the respective differences between males and females are described in Table 1. Of the domestic felines evaluated in this experiment, 46.66% presented with RDVP, which was absent in the others. No correlation was observed between age and any of the femoral artery blood flow parameters assessed in this study.

Intra-observer variability was evaluated by analysis of the coefficient of variation between repeated measures. As shown in Table 2, AD, SVP, RDVP, PI, AT, DT, and FFV showed low variability, while EDVP and MV had moderate variability. None of the variables demonstrated high variability.

Table 2

Variability of the intra-observer measurements, obtained through Doppler duplex ultrasonography of the femoral artery in non-sedated domestic cats, with an interval of 15 days (n = 10)

Variable	Mean ± SD	CV (%)	IOVD (%)
SVP RDVP EDVP AD AT DT FFV PI RI MV	34.54 ± 8.03 cm/s 4.78 ± 0.90 cm/s 10.19 ± 2.77 cm/s 0.17 ± 0.03 cm 39.95 ± 7.38 m/s 114.49 ± 21.14 m/s 0.095 ± 0.06 cm³ 1.27 ± 0.48 0.78 ± 0.28 20.09 ± 6.16 cm/s	23.24 18.82 27.18 17.64 18.47 18.46 63.15 37.79 35.89 30.66	0.14 1.80 15.15 10.11 7.54 1.97 6.21 8.76 9.34 24.67

CV = coefficient of variation; IOVD = intra-observer variability between days; SVP = systolic velocity peak; RDVP = recent diastolic velocity peak; EDVP = end diastolic velocity peak; AD = arterial diameter; AT = acceleration time of systolic peak (SP); DT = deceleration time of SP; FFV = femoral flow volume; PI = pulsatility index; RI = resistive index; MV = mean velocity

Discussion

DDU is an important non-invasive, low-cost, painless examination used to obtain early information about hemodynamic parameters of arterial or venous blood flow.^7,8 Previous application of the technique has clearly illustrated the clinical and experimental importance of this technique in veterinary medicine.^2,15,16

Aortoiliac obstructions modify the femoral artery flow; in humans this has been diagnosed with excellent sensitivity and acuity using DDU during patient follow-up.^27,28 Another important aspect of this technique is in regard to probable modifications that occur in blood flow related to systemic disorders, such as diabetes mellitus type 2,⁵ arterial hypertension,⁶ hyperthyroidism,⁷ obesity⁸ and heart failure.²⁹ In humans, such diseases can directly modify the blood flow volume and velocities by inducing structural modifications in the arterial walls. Therefore, similar to the carotid artery, it is possible that the femoral artery could be used as a prognostic marker of these alterations using DDU.

Domestic felines are susceptible to the development of arterial thromboembolisms, which are secondary to HC and lodge in the abdominal aorta bifurcation with a higher incidence, which results in a change in femoral artery flow.^9–11 Using DDU in healthy, non-sedated domestic felines, we showed that it was possible to evaluate different hemodynamic parameters of femoral artery flow, which allowed for the identification and complete morpho-physiological recognition of blood flow in the vessels of this species.

Future research on the quantitative parameters assessed with DDU in this study may be able to provide detailed functional information on the degree of arterial flow impairment in felines. Importantly, this would allow for the early detection of changes in the form and quality of blood flow arterial velocities in patients suspected of arterial occlusive diseases.

In feline medicine, arteriosclerosis can be mistakenly underestimated, as there has been a growing incidence in the abovementioned conditions for this species. It is worth emphasizing that the animals included here were middle aged and their weight, systolic blood pressure and body temperature measurements were within a range of values considered normal for the species.^23,30–32 Therefore, the hemodynamic parameters presented can be considered physiological for animals with similar clinical characteristics.

Of the domestic felines evaluated in this experiment, 53.34% presented without the negative phase of the Doppler triphasic spectrum (Figure 1). In medicine, the absence of this velocity component is related to the development of arterial diseases from arterial wall thickening or mechanical obstruction of the vessel lumen.^27,28 One reason for the absence of RDVP is related to the image-capturing technique, which depends on the adjustment of the sample volume of the equipment inside the blood vessel.³³ The lowest known value of the sample volume in the equipment model used was 0.20 cm (2.0 mm), and the mean arterial diameter found in the felines evaluated was 0.17 ± 0.039 cm. This value is similar to that reported in other studies³⁴ of DDU in domestic felines, with the reported values of right and left femoral artery diameters being 0.19 ± 0.02 cm and 0.17 ± 0.02 cm, respectively. It is known that sample volume should be adjusted to occupy half of the arterial diameter in order to obtain the highest velocities of the blood flow.³³ Therefore, during image capture in this study, the inability to reduce the sample volume for better acuity of the Doppler effect may have interfered with the triphasic spectrum formation. Furthermore, the anatomical proximity of the femoral artery and vein may also have limited RDVP recognition due to interference of the vein wall. It is important to emphasize that the insonation angle was fixed at 25° by the operator for all images used here with the goal of obtaining the greatest laminar flow, especially for determining the quantitative variables of the vessel analyzed. This challenge in adjusting the sample volume could create a limitation in recording the maximum velocities of femoral blood flow because the mean values described here were lower than those reported in other studies.³⁴

Figure 1

Doppler spectrum recorded by duplex Doppler ultrasound from the right femoral artery of a healthy domestic cat. The arrow indicates the insonation angle.

To date, few studies have described spectral characteristics related to femoral artery flow in domestic felines, and our results indicate the innovation and applicability of this procedure in clinical practice. The sample size used in this study was 30 animals, which is six times larger than that published in any related study to date.³⁴ The MV of the femoral artery blood flow presented a variation coefficient of 23.24%, which is considered acceptable for experimentation with biological samples.³⁵ Moreover, there was no significant difference between males and females in the quantitative indices for evaluation of femoral artery blood flow, which is in contrast to other animal species described previously.³⁶

Another limitation of this study was the inability to adjust the sample volume to the vessel. This may have impeded our ability to record the maximum velocities of femoral blood flow because the mean values described here were lower than those reported by other authors.³⁴ It is important to note the quantitative PI and RI variables because they correlate closely with the arterial capacitance measurements and serve as non-invasive indicators of peripheral vascular resistance.^21,22 Thus, the values obtained in this study could serve as a reference for animals with systemic conditions where vascular repercussions could occur, which has already been demonstrated in other species.^8,11,37,38

Conclusions

In this study, DDU was not compared with either the gold standard invasive telemetric method, or the previously published high definition oscillometric wave form analytic technics. Therefore, we cannot draw conclusions regarding accuracy. However, we believe that DDU proved to be a useful diagnostic technique in healthy, non-sedated domestic cats to evaluate the qualitative and quantitative parameters of femoral artery flow, and can serve as a guide in diagnosis and in therapeutic monitoring of diseases with vascular repercussion until more detailed studies are published.

Footnotes

Conflict of interest

The authors do not have any potential conflicts of interest to declare.

Funding

We are thankful for the financial support received from CAPES, Brazil.

Accepted: 19 February 2014

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