Reliability of detecting fundus abnormalities associated with systemic hypertension in cats assessed by veterinarians with and without ophthalmology specialty training

Abstract

Objectives

Systemic hypertension (SHT) causes severe target organ damage (TOD) and blood pressure (BP) measurement should be routine in at-risk populations. Fundoscopy is a tool to corroborate acute clinical relevance of high BP results and to decide on immediate therapy. Not every cat with a high BP result can be examined by an ophthalmologist. The study objective was to determine the reliability of fundoscopy in cats with SHT performed by a veterinarian without ophthalmology specialty training.

Methods

Cats with suspicion of hypertensive TOD or belonging to an at-risk population for SHT with a first measurement of elevated BP >160 mmHg were enrolled. Indirect ophthalmoscopy was performed by a recent graduate veterinarian followed by a veterinary ophthalmologist. Confirmation of SHT was based on two additional sets of systolic BP measurements >160 mmHg by Doppler sphygmomanometry.

Results

Thirty-three cats were included. SHT was confirmed in 27 cats. SHT was detected on routine examinations in 12/27 cats; fundoscopic lesions were observed in 9/12 by the non-trained veterinarian and in 11/12 by an ophthalmologist. Nine of 27 cats were neurological patients; fundoscopic lesions were detected in 4/9 by the non-trained veterinarian and in 7/9 by an ophthalmologist. Six of 27 cats were presented for acute blindness; fundus lesions were detected in all six cats by the non-trained veterinarian and ophthalmologist. SHT was not confirmed and fundoscopic lesions were not detected by either examiner in 6/33 cats. Compared with a veterinary ophthalmologist, reliability of detecting fundus abnormalities by the non-trained veterinarian was 72% (13/18) for cats with, and 100% (6/6) for cats without, vision.

Conclusions and relevance

Fundus examination by a non-specialty trained veterinarian has reasonably high reliability for the detection of ocular TOD. Private practice veterinarians are encouraged to perform an initial fundic examination in suspected hypertensive cats.

Keywords

Blood pressure feline hypertensive oculopathy situational hypertension Doppler sphygmomanometry target organ damage

Introduction

Systemic hypertension (SHT) is a well-recognised problem in elderly cats. Chronic kidney disease (CKD), hyperthyroidism, a combination of both diseases and hyperaldosteronism represent common underlying diseases. In addition, idiopathic SHT accounts for up to 40% of cases.^1–5 Persistent elevated blood pressure (BP) can lead to target organ damage (TOD), particularly in the eye, followed by the central nervous system (CNS), kidneys and cardiovascular system.^6–11 Hypertensive cats often present in an advanced stage of TOD with a guarded prognosis regarding complete recovery.^1,6 The fundus abnormalities in SHT are thought to occur in the following sequence of events: SHT causes autoregulatory vasoconstriction of retinal arterioles, visible as focal narrowing (beading) of these vessels, and causes remodelling of the smooth muscle layer, ischaemic damage and degeneration of the endothelium when persistent. Ultimately, focal disintegration and rupture of the vessel walls can lead to leakage of plasma and blood, causing vessel-associated focal retinal oedema and intraretinal haemorrhages. More widespread retinal oedema, bullous intraretinal fluid accumulation and larger intraretinal and preretinal haemorrhages can occur in later stages of the disease. Retinal detachment is most likely a direct result of plasma effusion from the choroidal vasculature, with ischaemic damage to the retinal pigment epithelium as a contributing factor. Optic nerve ischaemia leads to papilloedema and in the end stage to optic atrophy. Clinically, the ocular manifestations include retinal arterial tortuosity and beading, retinal oedema, pre-, intra- and subretinal haemorrhages, focal bullous intraretinal fluid accumulation, retinal detachment, retinal degeneration, papilloedema and optic atrophy. Pathologies associated with plasma effusion into the choroid and optic nerve can occur in parallel to retinal vessel associated changes.^1,12,13 Additional potential ocular complications of SHT include anterior segment and vitreous haemorrhage, uveitis and glaucoma.^2,6,7

Routine screening for SHT in at-risk populations is good clinical practice and an important preventive task.¹¹ However, non-invasive BP measurement in cats is not always reliable and situational hypertension in particular is an important reason for elevated BP measurements implying SHT.^3,4,14 Whereas antihypertensive treatment should not be delayed in true hypertensive cats to prevent potentially irreversible TOD, overtreating cats without real SHT is not advised. Therefore, in cats without TOD, repeated BP measurements at different time points are necessary for a definitive diagnosis of SHT and to justify lifelong antihypertensive treatment.¹¹ Retinal examination in an asymptomatic cat with a high BP measurement is an important step to detect TOD and to decide on immediate antihypertensive treatment. If lesions compatible with TOD are found, the diagnosis of SHT can be considered established and antihypertensive treatment should not be delayed.¹¹ Detecting early stages of ocular TOD affects the prognosis of regaining vision.¹⁵ However, in general practice, most cats with a high BP measurement cannot be examined immediately by an ophthalmologist.

Thus, the aim of this study was to evaluate the reliability of fundoscopic examination for identifying TOD in cats with SHT performed by a new graduate veterinarian without ophthalmology specialty training (LM) compared with a board-certified ophthalmologist or an ophthalmology resident under direct supervision.

Materials and methods

Animals

The study was approved by the State Veterinary Office of Zurich (application number 199/19, approved 12 September 2019), and informed consent was obtained from the owner before enrolling a cat into this prospective study.

The study population consisted of client-owned cats presented to any service of the Small Animal Clinic, Vetsuisse Faculty University of Zurich, between March 2019 and August 2020 with a clinical complaint potentially associated with SHT or predisposing for SHT, in which an elevated BP had been measured. Specifically, these were cats characterised by one of the following criteria: (1) acute onset of blindness; (2) central nervous system signs localised to the cerebrum (eg, seizures) in an elderly cat; (3) predisposing underlying diseases such as CKD and/or hyperthyroidism; and (4) age >10 years at a routine examination. A routine complete blood count and biochemical profile were performed to identify underlying diseases. Abdominal ultrasound was performed in cats with serum potassium <3.8 mmol/l to assess the adrenal glands in particular as an indicator of potential hyperaldosteronism.

Cats were classified as having CKD if the concentration of serum creatinine was above the reference interval (98–163 μmol/l), in non-dehydrated animals with or without clinical signs such as weight loss, polyuria/ polydipsia or abnormal kidneys on palpation (irregular size and/or surface). Cats were classified as being hyperthyroid if the concentration of serum thyroxine exceeded the reference interval (>3.3 μg/dl). Primary hyperaldosteronism was diagnosed if an adrenal mass was found on abdominal ultrasound and serum aldosterone was elevated in a hypokalemic cat. SHT was classified as primary or idiopathic if no apparent underlying cause was identified.

BP measurement

Indirect BP measurements were obtained by Doppler sphygmomanometry (Parks Device 811B) using a standard protocol. In brief, the limb circumference was measured in order to choose the appropriate cuff size (Table 1). As soon as repeated BP measurements plateaued, the average of the five subsequent consecutive measurements was obtained. Cats were included if this average systolic BP was >160 mmHg. The first BP measurements were obtained by the attending clinician or LM; all subsequent BP measurements were performed by LM. Cats were defined as truly hypertensive if fundus lesions consistent with SHT were observed, and as not hypertensive if no fundus lesions were observed and repeated BP measurements were <160 mmHg.

Table 1

Choice of cuff size for measuring blood pressure in cats

Leg circumference(cm)	Cuff width(cm)	Width corresponding % circumference
2.5–4.4	1	40–23
4.5–6.9	2	44–29
7.0–9.9	3	43–33

Fundoscopy

Pharmacological mydriasis was induced via topical application of tropicamide 0.5% eyedrops (Thea Pharma SA) 20 mins prior to the examination to optimise visibility of the ocular fundus. Pharmacological pupil dilation was omitted if cats presented with persistent mydriasis. Monocular indirect ophthalmoscopy was first performed in each cat by the new graduate veterinarian without ophthalmology specialty training (LM) using a 28D indirect condensing lens (Volk) and a Finoff transilluminator (Heine). The cat was held in a sternal position in a darkened room with the help of an assistant to keep the cat’s eyelids open. The light source was positioned against the temple of the examiner and was directed towards the patient’s eye. Once the tapetal reflex was identified, the indirect condensing lens was placed in front of the eye of the cat to allow examination of the ocular fundus. The use of a 28D indirect condensing lens and Finoff transilluminator to perform fundoscopy was chosen as these devices are readily available and affordable to the general practitioner. Furthermore, 28D lenses allow relatively easy positioning and manipulation of the lens in combination with a wide-angle view of the fundus.

Subsequently, fundic examination was performed through binocular indirect ophthalmoscopy by a trained ophthalmologist using 28, 20 and/or 15D condensing lenses (Volk) and a Heine Omega 500 binocular indirect ophthalmoscope (Heine). The use of a binocular ophthalmoscope is advantageous for the evaluation of fundus lesions since it allows stereopsis and thus increases depth perception. The use of 20 and 15D lenses, which have less condensing power than a 28D lens, increases magnification of fundus details and increases depth perception while simultaneously shrinking the field of view of the fundus. Pictures of the fundus were taken using a fundus camera (Smartscope Pro; Optomed).

Results

Animals, blood pressure, underlying diseases

Selected results for all cats are presented in Table 2, with the cats listed according to the sequence of their enrolment into the study.

Table 2

Selective results of 33 consecutive feline patients examined for potential systemic hypertensive ocular target organ damage (SHT TOD)

Case	Age* (years)	BP(mmHg)	Reason for BP measurement	Cause of systemic hypertension	Fundoscopy ophthalmologist	Fundoscopy new graduate^†
1	11	180	Heart murmur	Situational	Normal	1
2	16	220	Neuro	Situational	Normal	1
3	17.5	190	Blind	CKD	brd	1
4	14	190	T4	Situational	Normal	1
5	14	180	Neuro	Situational	Normal	1
6	14.5	220	Blind	CKD	brd, ph, nph	1
7	17.5	260	Neuro	CKD	brd, ph, nph	1
8	10.5	190	Neuro	CKD	re, tv	0
9	16.5	218	CKD	Situational	Normal	1
10	14.5	180	CKD	CKD + T4	ph, re	0
11	17.5	161	Neuro	Idiopathic	re	0
12	15	200	Neuro	Idiopathic	frd	0
13	10.5	263	CKD	CKD	brd, ph	1
14	13	185	T4 CM	Situational	Normal	1
15	16.5	210	Age	Idiopathic	frd, ph, re, hyper	1
16	18	270	Blind	Idiopathic	brd, ph, nph, hyper	1
17	15.5	230	CKD	CKD	Normal	1
18	16.5	283	Neuro	Idiopathic	brd, ph, re, hyper	1
19	16	260	Neuro	T4	brd	1
20	11.5	243	Age	Idiopathic	hyper	1
21	16.5	250	Neuro	CKD	brd, ph, nph	1
22	15.5	227	Neuro	T4	Normal	1
23	19	195	Blind	CKD + T4	nph, re, hyper	1
24	17	231	CKD	CKD	re, hypo	1
25	13.5	190	Blind	Idiopathic	brd, ph	1
26	17	208	T4	T4	brd, ph, re	1
27	16	226	Blind	Idiopathic	brd, nph, hyphema	1
28	14.5	228	CKD	CKD	Normal	1
29	14	189	CKD	CKD	brd	1
30	2	166	CKD	CKD	re	0
31	15	187	T4	T4	brd, hyper, hypo	1
32	15	176	T4	T4	brd, re	1
33	16.5	204	CKD	CKD	re, tv	1

Rounded to the next half year

†

1 = agreement between veterinarians with and without ophthalmology specialty training in judging fundus to show SHT TOD; 0 = disagreement between veterinarians with and without ophthalmology specialty training in judging fundus to show SHT TOD

BP = systolic blood pressure by Doppler sphymomanometry; neuro = clinical abnormalities localised to cerebrum; T4 = hyperthyroidism; CKD = chronic kidney disease; T4 CM = hyperthyroidism-associated myocardial disease; brd = large bullous retinal detachment; frd = small focal retinal detachment; ph = punctate haemorrhage; nph = non-punctate haemorrhage; re = retinal oedema; hyper/hypo = hyper-/hyporeflective areas; tv = tortuous blood vessels

Thirty-three cats were enrolled with a BP >160 mmHg at first measurement. Of these 33 cats, 27 were diagnosed as being truly hypertensive because of the presence of TOD or based on subsequent BP measurements. Six of the 27 cats were presented because of acute onset of blindness. Nine of the 27 cats were presented because of neurological signs (seizures, ataxia, torticollis, nystagmus or intermittent strange behaviour); of these, five had been referred for a neurological work-up. Twelve of the 27 cats were not presented because of clinical signs suggesting TOD, but had SHT identified on routine BP measurement. Breeds included domestic shorthair and domestic longhair (21), Siamese (2), British Shorthair (1), Burmese (1), Persian (1) and Norwegian Forest Cat (1). Thirteen of the cats were spayed females and 14 were castrated males. An abdominal ultrasound to rule out hyperaldosteronism was performed in six cats with low serum potassium, all with negative results.

In six of the 33 enrolled cats, SHT was not confirmed on subsequent BP measurements; these six cats comprised the negative controls. Breeds included domestic shorthair (5) and British Shorthair (1). Three of the cats were spayed females and three were castrated males.

The median systolic BP in the six cats with blindness as the primary concern was 208 mmHg (190–270 mmHg). Their median age was 17 years (13–19 years). The underlying diseases were CKD (n = 2), concurrent CKD and hyperthyroidism (n = 1) and idiopathic SHT (n = 3).

The median systolic BP in the nine cats with neurological signs as the primary concern was 230 mmHg (161–283 mmHg). Their median age was 16 years (10–17 years). The underlying diseases were CKD (n = 4), hyperthyroidism (n = 2) and idiopathic SHT (n = 3).

The median systolic BP in the 12 cats with SHT as the primary concern was 206 mmHg (166–263 mmHg). Their median age was 15 years (range 2–17 years). The underlying diseases were CKD (n = 6), hyperthyroidism (n = 3), concurrent CKD and hyperthyroidism (n = 1), and idiopathic SHT (n = 2).

The median systolic BP in the six control cats was 188 mmHg (180–220 mmHg). Their median age was 14 years (11–16.5 years). The primary reasons for BP measurement in these cats were hyperthyroidism (n = 2) or age >10 years (n = 4).

Fundoscopy

Fundus lesions were detected both by LM and by the attendant ophthalmologist in all six cats presented with blindness due to SHT. The attendant ophthalmologist identified ocular TOD in 7/9 cats with neurological signs, whereas LM correctly identified TOD in 4/7 cats. The attendant ophthalmologist identified ocular TOD in 11/12 cats with a primary concern of SHT, whereas LM correctly identified TOD in 9/11 cats. In summary, 24/27 cats with SHT had ocular TOD confirmed by the attendant ophthalmologist, with LM correctly identifying TOD in 19/24 cats. LM identified ocular TOD in all cats presenting with blindness (sensitivity 100%) and in 13/18 cats with neurological signs or SHT as the primary complaint (sensitivity 72%).

Ocular lesions were not detected by either the attendant ophthalmologist or by LM in three cats with confirmed SHT, nor in the six cats with an initial BP >160 mmHg, but no confirmation of SHT on subsequent BP measurements. Thus, LM correctly classified all nine cats without ocular TOD.

Fundic lesions detected by the non-specialised veterinarian included haemorrhages and retinal detachments and were usually more severe in nature than the ones that were missed (Figures 1 –3). Fundic lesions that escaped detection by LM were typically more subtle, including retinal oedema, punctate haemorrhages, areas of mild hypo- or hyper-reflectivity and tortuous blood vessels, particularly when located peripherally (Figure 4).

Figure 1

Fundus of a 17.5-year-old cat with a systolic blood pressure of 260 mmHg. The presenting complaint was acute vestibular syndrome. Pathological findings include a nasoventral preretinal haemorrhage of approximately twice the optic nerve head diameter (*), punctate retinal haemorrhages in the temporal and dorsal midperipheral tapetum (arrowheads) and multifocal bullous retinal detachments (arrows). The generalised haziness of the nasal half of the fundus suggests the presence of either generalised retinal oedema or a large flat or mildly elevated retinal detachment

Figure 2

Fundus of a 17-year-old cat with a systolic blood pressure of 208 mmHg. The presenting complaint was diarrhoea. Pathological findings include multifocal bullous retinal detachments (arrows) and areas of focal retinal oedema (dashed arrows)

Figure 3

Fundus of a 14.5-year-old cat with a systolic blood pressure of 220 mmHg. The presenting complaint was impaired vision. Pathological findings visible on this image include large dorsal retinal detachments (arrows), punctate haemorrhages (arrowheads) and larger retinal or preretinal haemorrhages (*), as well as generalised retinal oedema. The last is indicated by the fact that the image seems well focused but there is a generalised haziness/loss of fine retinal detail compared with the crisp detail visible in Figure 2

Figure 4

Fundus of a 10.5-year-old cat with a systolic blood pressure of 190 mmHg. The presenting complaint was ataxia. Pathological findings include an area of tapetal hyporeflectivity (star), a mild tortuosity of blood vessels (dotted arrows) and mild diffuse retinal oedema of the nasal retina. The last is indicated by the fact that the image seems well focused but there is a generalised haziness/loss of fine retinal detail in the nasal half of the fundus (right-hand side of the image) compared with the crisp detail visible in Figure 2 and in the temporal half of the fundus (left-hand side of the image)

A training effect seemed present for the non-specialised veterinarian during the course of the study: LM missed lesions in four of the first seven cases with fundus abnormalities, whereas lesions were missed in only one of the subsequent 17 cases with fundus abnormalities (Table 2).

Discussion

The results of this study, with focus on fundic examination in cats with suspected SHT, allows the conclusion that a non-specialty trained veterinarian can reach a reasonably high sensitivity of detecting hypertensive ocular TOD while not overdiagnosing fundic lesions. In particular, the more obvious fundic lesions can be detected by a non-specialised veterinarian. The sensitivity for detecting hypertensive ocular TOD was 100% in hypertensive cats with acute blindness as the presenting complaint for both the veterinarians with and without ophthalmology specialty training. In the hypertensive cats where the presenting complaint was not blindness, that is, the more challenging cases, the sensitivity for detecting hypertensive ocular TOD was 72%. Thus, non-specialised veterinarians cannot completely replace veterinary ophthalmologists in such cases. However, the argument could be made that delaying antihypertensive treatment may be justifiable if only subtle lesions are present. With good clinical practice, BP measurement will be repeated within days and antihypertensive treatment started if SHT is confirmed. The likelihood of delaying treatment to the detriment of the patient would probably be small in such cases. As a matter of fact, repeating BP measurements within days is also the lege artis approach if the ophthalmologist does not detect TOD in a cat suspected of SHT.

Of 27 cats with SHT, 15 were presented because of SHT-induced TOD, either neurological or ocular. In an additional 11/12 cats in which SHT was detected by BP screening, ocular TOD was detected. Thus, 26/27 cats with SHT had some sort of TOD at the time of first presentation to our hospital and, of these, 24 had some degree of ocular TOD. This is comparable to other studies in which the frequency of ocular lesions was as high as 100%.^1,2,9,16 This finding supports the concern that BP evaluation in cats is mostly performed too late. It also supports the recommendation to routinely measure BP in the feline population at risk for SHT, including asymptomatic elderly cats.¹⁷

The occurrence of neurological signs as the presenting complaint in hypertensive cats in this study was comparable to other studies where the prevalence of hypertensive encephalopathy was 29–46%.^1,6 Neurological deficits by themselves should trigger veterinarians to measure BP in elderly cats, certainly before performing MRI of the brain. Neurological signs are most likely the result of hypertensive encephalopathy in cases where SHT is diagnosed and neurological signs resolve under antihypertensive treatment.

Study limitations

A non-trained veterinarian may not remain non-trained after performing fundus examinations on a number of cats because of the expected training effect. The training effect observed in this study was likely exacerbated since fundic examinations were the focus of this study; that is, the non-trained veterinarian invested a significant amount of time in autodidactic training by consulting the relevant literature. Nevertheless, for any non-specialty trained veterinarian the primary obstacle for detecting fundic lesions is the will to actually perform a thorough enough fundic examination that allows a representative view of the retina. This can be attained without a specialised education. Of note is the fact that LM did not receive any ophthalmic examination training that was not part of her veterinary school curriculum prior to conducting this study.

The small sample size is an additional study limitation. However, as pointed out above, the more cases are examined by a non-trained veterinarian, the less the term ‘non-trained’ holds true. In fact, lesions were primarily missed early in the study by the non-trained veterinarian.

The fact that the detection of fundic lesions in a suspected hypertensive cat is not conclusive proof of a hypertension-induced lesion is a further limitation of this study. Retinal haemorrhages, for example, can be induced by several other causes, including coagulopathies, trauma, chorioretinitis or neoplasia.^18,19

Finally, fundic examination by a veterinary ophthalmologist was defined as the gold standard for the detection of ocular TOD in this study. However, veterinary ophthalmologists performing indirect ophthalmoscopy may also miss lesions on occasion. Advanced imaging modalities, including fundus angiography, scanning laser ophthalmoscopy (cSLO) and optical coherence tomography (OCT), might have detected lesions in cats graded as non-affected in this study.²⁰ However, the use of such imaging modalities exceeded the possibilities of this study.

Conclusions

Measuring BP should be part of a routine health check examination in elderly cats. A fundic examination should be performed immediately if an elevated BP at a level that puts a patient at high risk for developing TOD is measured.^10,11 Antihypertensive treatment could then be initiated immediately if evidence of ocular TOD, corroborating the suspected SHT, is detected. Even though the incidence of SHT in cats may be low and no immediate feedback by a specialist can be obtained in a general practice, which complicates autodidactic learning, the results of this study should encourage general practitioners to perform an initial fundic examination in suspected hypertensive cats before starting treatment or sending to a board-certified ophthalmologist.

Footnotes

Accepted: 30 November 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 study was in part funded by the Swiss Association for Small Animal Medicine, Hüneberg, Switzerland.

Ethical approval

This work involved the use of non-experimental animals only (including owned or unowned animals and data from prospective or retrospective studies). Established internationally recognised high standards (‘best practice’) of individual veterinary clinical patient care were followed. Ethical approval from a committee, while not necessarily required, was nonetheless obtained, as stated in the manuscript.

Informed consent

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

ORCID iD

Arnold Lavaud

Christian Günther

Tony Glaus

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