Impact of gonadal status on ultrasonographic renal parenchymal dimensions in healthy cats

Abstract

Objectives

The aim of this study was to evaluate the effect of gonadal status on ultrasonographic renal parenchymal dimensions in healthy cats.

Methods

Forty healthy cats (10 intact males, 10 intact females, 10 castrated males and 10 spayed females) presented to the Division of Obstetrics, Gynecology and Reproduction, and the Diagnostic Imaging Unit at The Small Animal Teaching Hospital, Faculty of Veterinary Science, Chulalongkorn University. They were ultrasonographically examined to assess renal length, aortic luminal diameter, cortical thickness and medullary thickness.

Results

Regardless of gonadal status, the renal length, aortic luminal diameter, cortical thickness and medulla thickness of males were greater than those of females (P <0.05). In general, neutered cats had thicker medullae (0.36 ± 0.08 cm) and higher mean renal length:aortic luminal diameter ratio (12.15 ± 1.48) than intact cats (0.32 ± 0.08 cm and 11.22 ± 1.37 cm, respectively) (P <0.05), but no differences were observed in renal length, cortical thickness or aortic luminal diameter. Interestingly, when comparing between sexes with relatively equal body weight, only sex had an impact on renal length.

Conclusions and relevance

Gonadal status has an effect on medullary thickness and mean renal length:aortic luminal diameter ratio.

Keywords

Gonadal status kidney parenchyma ultrasound

Introduction

Kidneys are vital organs, with functions involving the control of blood volume, blood pressure, haematocrit, acid–base balance, electrolyte concentrations and metabolite excretion.¹ In cats, chronic kidney disease (CKD) is a renal disease frequently detected in clinical practice. CKD is identified as the second most common cause of illness and mortality in feline patients.² The prevalence of CKD is reported to be 1–3% in the feline population, and is rapidly increasing in cat populations.^1–3

Diagnostic testing for renal disease in cats can be divided into three steps. Primary testing includes history-taking, physical examination, serum biochemistry tests, complete blood cell count (CBC), urinalysis and abdominal radiographs. Secondary testing focuses on blood pressure measurements and abdominal ultrasonography. Finally, tertiary testing aims to exclude a diagnosis of kidney disease among less common diseases; an example of this type of testing is renal biopsy.⁴ As no single test can provide a definitive diagnosis of CKD, several methods have been suggested for inclusion in the diagnostic procedure.^1,4

Imaging techniques are not only used as a diagnostic tool, but also as a tool for monitoring kidney diseases, including CKD. Ultrasonography provides high-quality images and information about the physical structure of the kidneys, so ultrasonography can be considered a reference modality for feline renal imaging.⁵ In human medicine, decreasing cortical thickness measured by ultrasonography is used for early detection of renal failure and reduced estimated glomerular filtration rate (eGFR).^6,7 This suggests cortical thickness may be an indicator of CKD in cats, and may be useful in assessing disease progression.Renal dimensions of cats, including renal length, cortical thickness and medullary thickness, are affected by several factors, including kidney location, body weight, age and sex.^5,8,9 Gonadal status is another factor that must be considered. It has been noted radiographically that neutered cats have a lower ratio of renal length to the length of the second lumbar vertebra (L2) than intact cats.¹⁰ Although the number of neutered cats has increased as a result of concerns about cat overpopulation globally, there have been no studies regarding the influence of gonadal status on feline renal parenchymal dimensions as evaluated by ultrasonography. To use renal parenchymal dimensions to detect renal disease in cats, the effect of gonadal status on the renal parenchymal dimensions of clinically healthy neutered cats first needs to be verified. This study aimed to investigate the impact of gonadal status on renal parenchymal dimensions, and to establish a reference value of renal dimensions for healthy cats.

Materials and methods

Animals

This cross-sectional study was conducted under the approval of the Institutional Animal Care and Use Committee of Chulalongkorn University (CU-IACUC approval number: 1831025). All clinical and ultrasonographic data were collected from cats that presented to the Division of Obstetrics, Gynecology and Reproduction, and the Diagnostic Imaging Unit, The Small Animal Teaching Hospital, Faculty of Veterinary Science, Chulalongkorn University between May 2018 and January 2019. The information collected was age, breed, body weight, body condition score, sex and gonadal status. Screening tests included physical examination, hydration status assessment, CBC, serum biochemistry (blood urea nitrogen and creatinine), urinalysis (urine specific gravity and urinary dipstick), and tests for feline leukaemia virus and feline immunodeficiency virus. Cats with a history of upper or lower urinary tract disease or abnormalities based on screening tests were excluded from the study.

Forty healthy cats were included in this study. They were divided into four groups based on their sex and gonadal status (10 intact males, 10 intact females, 10 castrated males and 10 spayed females). Gonadectomy had been performed at least 1 year before the study.

Renal dimension measurements

Renal ultrasonography of all animals was performed by a well-trained ultrasonographer, using a 7.0 MHz linear transducer (Logic P6; GE Medical System) and all cats were scanned, while conscious, in the sagittal plane. Before ultrasonography, the ventral abdomen was prepared by clipping hair and applying acoustic coupling gel to the skin. The cats were positioned in dorsal recumbency on a V-shaped pad. The renal length, cortical thickness (measured at the cranial pole, mid-area, and caudal pole), and medullary thickness (measured at mid-area) were evaluated. The measurements of aortic luminal diameter (Ao), caudal to the root of the left renal artery, excluded the vessel walls during the systolic phase (Figure 1). The ratios of left renal length:aortic luminal diameter (LK:Ao ratio), right renal length:aortic luminal diameter (RK:Ao ratio) and mean renal length:aortic luminal diameter (K_m:Ao ratio) were calculated.

Figure 1

Sagittal ultrasound image of a feline kidney. (a) When two bright parallel bars formed by cross-sectioned pelvic diverticula appear, the renal length (L), (b) cortical thickness (c) and medullary thickness (m) were measured. (c) Measurement of the aortic luminal diameter (Ao), excluding the vessel walls

Statistical analysis

Statistical analysis was performed using GraphPad Prism 7. Renal statistics such as renal length, cortical thickness, medullary thickness, Ao, LK:Ao ratio, RK:Ao ratio and K_m:Ao ratio of all cats were presented as means ± SD. Normality for each parameter was evaluated using the Shapiro–Wilk test. Parametric data were analysed using paired and unpaired t-tests. These tests were also applied to evaluate differences attributed to key experimental variables, including kidney side, sex, gonadal status and interactions between sex and gonadal status (intact males vs neutered males and intact females vs neutered females). Correlations among key parameters were assessed by Pearson correlation coefficients. All statistical analyses were considered significant if P <0.05.

Results

Forty healthy cats were enrolled, including 34 domestic shorthair cats (nine castrated males, nine spayed females, eight intact males and eight intact females), five Persians (two intact males, two intact females and one spayed female) and one Scottish Fold (castrated male). Average body weight was 3.98 ± 0.74 kg (range 2.5–5.0 kg). Mean body condition score was 2.90 ± 0.30 (range 2.5–3.5). Median age was 25.5 months (range 24–60 months). Regardless of gonadal status, male cats were significantly heavier than female cats (4.33 ± 0.60 kg and 3.63 ± 0.71 kg, respectively) (P <0.01).

Renal length

The average renal length was 3.76 ± 0.49 cm (range 2.74–5.04 cm). The right kidneys were significantly longer than the left kidneys (3.85 ± 0.50 cm and 3.67 ± 0.48 cm, respectively) (P <0.05). Kidneys of male cats were significantly longer than those of female cats (4.02 ± 0.44 cm and 3.50 ± 0.41 cm, respectively) (P <0.001). However, the renal length was not influenced by gonadal status (P = 0.58) or the interaction between sex and gonadal status (P = 0.19 and P = 0.08 for male and female groups, respectively) (Table 1). A strong positive correlation was observed between body weight and renal length (r = 0.66, P <0.0001).

Table 1

Ultrasonographic renal dimensions of 40 healthy cats

Mean ± SD	Renal length (cm)	Ao (cm)	RK:Ao	LK:Ao	K_m:Ao	Parenchymal thickness (cm)
						Cortex	Medulla
Overall	3.76 ± 0.49	0.32 ± 0.04	11.98 ± 1.59^g‡	11.39 ± 1.35^g‡	11.69 ± 1.49	0.47 ± 0.09	0.34 ± 0.08
Neutered	3.79 ± 0.35	0.32 ± 0.04	12.59 ± 1.53^g‡	11.17 ± 1.32^g‡	12.15 ± 1.48^c†	0.46 ± 0.07	0.36 ± 0.08^e*
Intact	3.73 ± 0.61	0.33 ± 0.05	11.37 ± 1.42^g†	11.08 ± 1.34^g†	11.22 ± 1.37^c†	0.47 ± 0.12	0.32 ± 0.08^e*
Male	4.02 ± 0.44^a†	0.34 ± 0.04^b†	12.04 ± 1.56^g‡	11.53 ± 1.62^g‡	11.79 ± 1.59	0.51 ± 0.11^d‡	0.36 ± 0.08^f*
Neutered male	3.93 ± 0.35	0.33 ± 0.04	12.47 ± 1.47^g‡	11.78 ± 1.64^g‡	12.13 ± 1.55	0.47 ± 0.08	0.38 ± 0.08
Intact male	4.12 ± 0.51	0.36 ± 0.04	11.61 ± 1.60^g†	11.28 ± 1.64^g†	11.45 ± 1.59	0.54 ± 0.12	0.35 ± 0.07
Female	3.50 ± 0.41^a†	0.30 ± 0.04^b†	12.26 ± 1.04^g†	11.92 ± 1.65^g†	11.59 ± 1.40	0.43 ± 0.06^d‡	0.31 ± 0.08^f*
Neutered female	3.66 ± 0.32	0.30 ± 0.04	12.72 ± 1.66^g†	11.64 ± 0.98^g†	12.18 ± 1.44	0.45 ± 0.05	0.34 ± 0.08
Intact female	3.45 ± 0.44	0.31 ± 0.04	11.82 ± 1.25^g†	10.87 ± 1.01^g†	11.70 ± 1.11	0.41 ± 0.06	0.29 ± 0.08

*P <0.05; †P <0.01; ‡P <0.001; a, b, d, f: male compared with female; c, e: neutered compared with intact; g: RK:Ao compared with LK:Ao

Ao = aortic luminal diameter; RK = right kidney; LK = left kidney; K_m:Ao = mean renal length:aortic luminal diameter

Aortic luminal diameter

The average Ao was 0.32 ± 0.04 cm (range 0.23–0.43 cm). The Ao differed significantly between males and females (0.34 ± 0.04 cm and 0.30 ± 0.04 cm, respectively) (P <0.01). However, the Ao was not influenced by gonadal status (P = 0.18), nor by the interaction between sex and gonadal status (P = 0.07 and P = 0.86 for male and female groups, respectively) (Table 1).

Overall, the LK:Ao, RK:Ao and Km:Ao ratios were 11.39 ± 1.35, 11.98 ± 1.59 and 11.69 ± 1.49 (range 8.84–14.06, 8.30–16.13 and 8.30–16.13, respectively). The RK:Ao ratio was significantly greater than the LK:Ao ratio (P <0.05). The K_m:Ao ratio of neutered cats (12.15 ± 1.48) was significantly greater than that of the intact cats (11.22 ± 1.37) (P <0.01) (Figure 2a). Conversely, sex (P = 0.56) and the interaction between sex and gonadal status (P = 0.18 and 0.07 for male and female groups, respectively) had no effect on the K_m:Ao ratio (Table 1). Moderately positive correlations were observed between Ao and body weight (P <0.0001, r = 0.53) and between Ao and renal length (P <0.0001, r = 0.53). Hence, cats with a heavier body weight tended to have a wider Ao than cats with lighter body weight, and cats with a wider Ao tended to have longer kidneys than cats with a narrower Ao.

Figure 2

Comparison of the renal dimensions between neutered and intact cats. (a) The mean renal length:aortic luminal diameter (K_m:Ao) ratio of neutered cats was significantly higher than that of intact cats. (b) The medullary thickness of neutered cats was significantly thicker compared with intact cats

Cortical and medullary thicknesses

The average cortical thickness of kidneys was 0.47 ± 0.09 cm (range 0.30–0.83 cm). The left (0.46 ± 0.11 cm) and right kidneys (0.47 ± 0.08 cm) had similar ranges of the cortical thickness (P = 0.57). The cortical thickness of male cats (0.51 ± 0.11 cm) was remarkably thicker than that of the female cats (0.43 ± 0.06 cm) (P <0.001) (Table 1).

The average medullary thickness of the kidneys was 0.34 ± 0.08 cm (range 0.19–0.60 cm). The thickness of the medulla did not differ between the left and right kidneys (0.34 ± 0.09 cm and 0.34 ± 0.08 cm, respectively) (P = 0.71). The medullary thickness was influenced by gonadal status (Figure 2b) and sex (P <0.05), with male cats having a thicker medulla than female cats and the medullary thickness of neutered cats being thicker than in intact cats (Table 1).

A moderately positive correlation was observed between body weight and cortical thickness (P <0.0001, r = 0.46) (Figure 3a). However, the correlation between body weight and medullary thickness was weak (P <0.001, r = 0.38) (Figure 3b). A strong positive correlation was observed between renal length and cortical thickness (P <0.0001, r = 0.60), and a moderate positive correlation was observed between renal length and medullary thickness (P <0.0001, r = 0.46) (Figure 3c,d).

Figure 3

(a) Correlation between body weight and cortical thickness and (b) between body weight and medullary thickness. (c) Correlation between renal length and cortical thickness and (d) between renal length and medullary thickness

When comparing male and female cats with similar body weights (five male cats: 3.74 ± 0.21 kg; six female cats: 3.73 ± 0.26 kg), we found that, irrespective of gonadal status, males had longer kidneys (3.72 ± 0.21 cm) than females (3.44 ± 0.17 cm) (P <0.05). The Ao of males (0.35 ± 0.03 cm) was larger than that of females (0.31 ± 0.01 cm) (P <0.01). However, there were no differences in cortical (P = 0.40) and medullary thicknesses (P = 0.18) between the sexes. Hence, only sex affected the renal length. Medullary thickness was affected by both body weight and gonadal status, while cortical thickness was affected by body weight and the calculation of an estimated renal cortex thickness in a normal healthy animal based on the body weight, using X = (Y – 2.4)/3.4 (X = cortical thickness [cm], and Y = body weight [kg]).

Discussion

Renal dimensions are useful for distinguishing a normal kidney from an abnormal kidney. For example, reduced kidney size and irregular shape suggest CKD, while increased kidney size suggests an acute kidney injury (AKI).^4,10 In human medicine, the renal parenchymal information gained through diagnostic imaging assists with the renal diagnosis. In humans with CKD, the renal cortex usually becomes thin and renal echogenicity increases on ultrasound; reduction in cortical thickness could be an early sign of renal failure and eGFR reduction. The eGFR is even more correlated to cortical thickness than renal length in CKD; this implies that cortical thickness can be a predictor of CKD, and may serve as a monitoring parameter for disease progression in human medicine.^6,7 However, reference intervals for cortical thickness that can be used to assess renal function have not been established in cats, and the impact of gonadectomy on renal parenchymal dimensions have never been reported in cats. Therefore, this study aimed to investigate the relationship between gonadal status and feline kidney parenchyma in healthy cats. The results from this study may be used as references for renal parenchymal dimension in healthy cats.

In this study, gonadectomised cats were eligible only if they had been neutered at least 1 year prior because a previous study investigated the effect of gonadal status on feline renal size in radiography reported that the effect occurred 7 months after gonadectomy.¹⁰ Therefore, we decided to choose neutered cats that had undergone gonadectomy at least 1 year prior to explore the effect of gonadal status more accurately. Additionally, only cats with normal hydration were included in the study to improve measurement precision. It has been reported that the renal length of human patients with normal hydration was significantly longer than that of dehydrated human patients.¹¹ Finally, this study included three breeds of cats (the majority were domestic shorthair) as no statistically significant differences were observed in renal dimensions in a previous study⁵ comparing different feline breeds and all criteria for selecting the sample cats, such as age, body weight and body condition score, were set to be comparable across individuals.

In general, we found that the right kidney was longer than the left kidney, which is in agreement with a previous report.⁵ Similar to previous studies,^5,8,9,12,13 we found that sex and body weight had an effect on renal length, although some studies have found no difference with respect to sex.^10,14 Although gonadal status had no effect on renal length, female neutered cats and neutered cats (regardless of sex) may tend to have longer kidneys. This finding may be caused by fat accumulation in the kidneys of neutered cats.¹⁵ A previous report showed that on radiographic images neutered cats had a lower ratio of renal length to the length of the second lumbar vertebra (L2) (range 1.9–2.6) than intact cats (range 2.1–3.2).¹⁰ There was another study in cats that investigated the effect of neutering on radial physeal closure. Cats that were neutered at 7 weeks and 7 months of age had a significantly delayed physeal closure and longer radial bones when compared with intact cats.¹⁶ Therefore, gonadal status may impact lumbar physeal closure as well. Likewise, the previous study¹⁰ was performed on cats of the same age and the L2 of neutered cats may be slightly longer.

To our knowledge, ultrasonographic evaluation of kidney size using Ao in cats has never been studied. Our findings showed that the Ao, RK:Ao and LK:Ao ratios were slightly lower than previously reported from CT (Ao: 0.33 ± 0.05 cm; RK:Ao ratio: 12.05 ± 1.47; LK:Ao ratio: 11.72 ± 1.37).¹⁷ The RK:Ao ratio was significantly greater than the LK:Ao ratio owing to a larger mean right kidney length. This result differed from a previous study in healthy dogs, which found no significant difference in the ratios between the left and right kidneys.¹⁸

Even though the K_m and Ao did not differ significantly between intact and neutered animals, the neutered group showed a slightly higher K_m and lower Ao, which led to the conclusion that gonadal status affected the K_m:Ao ratio. However, differences in K_m:Ao ratio were not observed by gonadal status within sex groups owing to a small sample size. Our findings suggested that the K_m:Ao of healthy cats was 11.69 ± 1.49. In clinical practice, our results must be carefully interpreted together with other test results and clinical signs.

The cortical thicknesses of the left and right kidneys in our cats were slightly lower that a previous report (0.71 ± 0.14 cm for the left and 0.74 ± 0.14 cm for the right).⁵ Different results might be caused by the different image planes used; the previous study was conducted in the dorsal plane, while the present study was conducted in the sagittal plane. In addition, a moderate positive correlation was observed between body weight and cortical thickness, which agrees with an earlier study.⁸ Cats with a heavier body weight tended to have a thicker cortex. Moreover, we found that the cortical thickness had a strong positive correlation with renal length. This demonstrated that longer kidneys tended to have a thicker cortex. Overall, cortical thickness was not different between the left and right kidneys,⁵ and similar results were observed in all groups in our study. Finally, we found that the cortex size was significantly influenced by sex, but not by gonadal status or the interactions between sex and gonadal status.

Previous studies reported that, on average, the left and the right medullary thicknesses were 0.87 ± 0.19 and 0.93 ± 0.21, and 0.79 ± 0.22 cm, respectively, and that medullary thickness differed between the left and right sides.^5,9 The difference in medullary thickness between the left and right kidneys may result from an oblique angle at ultrasound during the examination. Generally, a weak correlation between body weight and medullary thickness has been observed, which is in agreement with our study.⁸ To our knowledge, this is the first report showing that renal medullary thickness is moderately correlated with renal length, suggesting that cats with longer kidneys tend to have a thicker medulla, and that the size of the medulla is also influenced by sex and gonadal status. Further research, comparing the histopathology of the renal medulla between entire and neutered cats, is necessary to explain these differences.

This was a cross-sectional study conducted using client-owned animals. It was not possible to perform a prospective study comparing the same animal pre- and post-gonadectomy, but this would be an interesting comparison for future studies. According to the regulation of animal use for scientific research, the number of animals were statistically calculated. Although it seemed that the number of animals was relatively low, it was enough to answer the hypothesis of this study and differences between sexes and gonadal status in some parameters, that is, renal length, K_m:Ao, cortical thickness and medullary thickness, were strongly significant.In our study, we are fully aware of good image resolution and measurement accuracy. From the literature reviews,^5,8 4–12 MHz linear transducers were suggested for feline abdominal imaging and a 7 MHz linear transducer was used in all ultrasonographic examinations. All measurements were clearly made and the quality of images is shown in Figure 1. Repeatability of the results was one of our major concerns. In humans, it has been suggested that renal ultrasound is simple and can be performed with a low inter-observer variability.^19,20 In the present study, all measurements of renal parenchymal thickness were made by an experienced ultrasonographer (PT) to avoid any inter-observer variations. For further study, factors affecting the repeatability of feline renal dimension measurement should be investigated; for example, intra- and inter-observer reliability and sedation. Moreover, the examination procedure was conducted in manually restrained cats without any sedation, which may have increased the difficulty of the renal scan. Because we wanted to eliminate dehydration, withholding food and drink from the animals (as required before sedation) was not desired. Although parenteral intravenous fluid could be given prior the ultrasonographic examination, diuretic renomegaly may also occur.²¹

Conclusions

Feline renal dimensions depend on several factors. Gonadal status has an effect on medullary thickness and K_m:Ao ratio. Nevertheless, when comparing male and female cats with relatively similar body weight, only sex affected the renal length. Hence, cortical thickness was affected by body weight and we suggest the formula in our results to calculate feline cortical thickness to monitor CKD, like in human medicine.^6,7 The results of this study can be used as reference values for normal ultrasonographic renal dimensions in cats. Further studies are necessary to evaluate the utility of the measurement of the cortical thickness in cats with renal disease.

Footnotes

Acknowledgements

We would like to express our thanks for the scholarship from the Graduate School, Chulalongkorn University to commemorate the 72nd anniversary of his Majesty King Bhumibala Aduladeja and the 90th anniversary Chulalongkorn University Fund (Ratchadaphiseksomphot Endowment Fund).

Accepted: 7 February 2020

Conflict of interest

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

This work was supported by the scholarship from the Graduate School, Chulalongkorn University to commemorate the 72nd anniversary of his Majesty King Bhumibala Aduladeja; and the 90th anniversary Chulalongkorn University Fund (Ratchadaphiseksomphot Endowment Fund) (grant number GCUGR1125614082M,82).

Ethical approval

This work involved the use of non-experimental animals only (owned or unowned), and followed established internationally recognised high standards (‘best practice’) of individual veterinary clinical patient care. Ethical approval from a committee was therefore not necessarily required.

Informed consent

Informed consent (either verbal or written) was obtained from the owner or legal custodian of all animal(s) described in this work for the procedure(s) undertaken. No animals or humans are identifiable within this publication, and therefore additional informed consent for publication was not required.

ORCID iD

Nan Choisunirachon

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