Feline cystadenomatosis affecting the ears and skin of 57 cats (2011

Abstract

Objectives

This study aimed to understand epidemiological factors associated with feline cystadenomatosis, including signalment and papillomavirus PCR status. Cystadenomatosis is an uncommon condition primarily involving the ceruminous and apocrine skin and ear glands.

Methods

This was a retrospective case series. Clinical records from 2011 to 2019 from a tertiary referral hospital in Boston, MA, USA were screened for cases, and case data were re-evaluated and analyzed. The total patient pool contained 65,385 individual cats, of which 797 were referred to the dermatology service. Medical records and biopsy specimens were reviewed; the information collected included signalment, clinical signs, physical examination and diagnostic tests, comorbidities and histopathologic findings. PCR was performed on biopsy specimens to test for papillomavirus DNA.

Results

The cystadenomatosis population consisted of 57 cases (7.1% of total cases referred to the dermatology service) with 105 affected ears. Twenty-seven cases (48 ears) were confirmed via histopathology; four cats (7%) exhibited clinically cystic lesions on the periocular, periorbital and perianal regions; only one cat did not have pinnal lesions. Domestic shorthair cats were most often affected. Relative risk for cystadenomatosis was 2.24 times higher in male cats. In 48 cats (84.2%), ears were bilaterally affected. Seven cats (12.3%) had malignant neoplasia, which included: inflamed adenocarcinoma (n = 5); mast cell tumor (n = 1); or squamous cell carcinoma (n = 1). PCR testing on biopsy specimens from 24 cats revealed feline papillomavirus type 2 DNA in only four cats.

Conclusions and relevance

Cystadenomatosis was more prevalent in senior non-purebred cats, over-represented in male cats and did not appear to be associated with papillomavirus, feline infectious peritonitis, feline immunodeficiency virus/feline leukemia virus status or other identifiable illnesses. Further studies are needed to investigate the causes of cystadenomatosis.

Keywords

Otitis externa periocular cysts cysts cystadenomatosis apocrine glands ceruminous glands

Introduction

Cystadenomatosis involves the formation of multiple cysts originating from the secretory portion of modified apocrine sweat glands, leading to the development of characteristic focal to coalescing bluish-black cystic skin and ear nodules that range from 1 mm to several centi-meters in diameter (Figure 1). The cysts are often located in areas of the body where modified apocrine sweat glands are known to be located.^1–6 They have also been reported to occur in dogs and humans.^3,7 Cystadenomatosis has been found to primarily affect the preauricular region, concave pinna, concha, tragus and antitragus, and the external ear canal of cats,^8–12 while less commonly affected areas include the periocular,^8,10,13 perioral and perianal regions (Figure 2).⁹

Figure 1

Extensive classic bluish-black cystic lesions on the entire concave pinna and into tragus folds

Figure 2

Open arrows indicate the apocrine cystic lesions along the eyelids. The solid arrows indicate pre-aural cysts in an Abyssinian cat. Courtesy of Dr M Coster

The nomenclature for this condition can be confusing, and terms such as sebaceous or ceruminous cysts,^5–7,14,15 apocrine cystadenoma, ceruminous cystadenoma,⁸ apocrine cysts, apocrine hidrocystomas,^8,13,16 sweat gland cysts of the skin,^5,6,11,12 melanotic ceruminous cysts,^17,18 ceruminous gland adenomas, ceruminous gland cysts,¹⁹ ceruminous gland hyperplasia,^19,20 ceruminous cystomatosis^21,22 and epitrichial cystadenomas¹⁵ have all been used. We have previously used the term ‘cystomatosis’ in abstracts.^4,23

An adenoma is defined as a benign epithelial neoplasm of glandular origin; however, it is non-specific and hence the microanatomical glandular tissue of origin is often indicated (ie, apocrine gland) to further specify the pathology.^5,24,25 ‘Cystadenoma’ describes an adenoma in which the glandular space is cystic.²⁵ According to the Merriam-Webster medical dictionary,²⁵ the term ‘adenomatosis’ is defined as ‘a condition marked by growths consisting of glandular tissue’. In our view, the term ‘cystadenomatosis’ is a more comprehensive term for the description of this particular dermatosis. We therefore propose that the term ‘feline cystadenomatosis’ be used to describe this clinical syndrome.

Cystadenomatosis has been reported in Europe,^7,26 North America,^4,21,23 Asia^2,27 and South America.¹⁶ The clinical sign associated with this benign cutaneous neoplasia is minimal inflammation in the surrounding skin.^5,6,28,29 However, it can cause obstructive conformational changes in ear canals and enhance the likelihood and severity of secondary infectious otitis externa.^11,20,21,30

The glands involved in cystadenomatosis are the modified sweat apocrine glands, which can be found in the skin surrounding the eyelid margins (Moll’s glands), lip margins and perianal regions, but are most prevalent in and around the ears.^{5–7,9,13,15,31} The external acoustic meatus of cats contains ceruminous and sebaceous glands,^9,11,12 with mixed epitrichial and atrichial units,^5,6,24,32 which produce the waxy cerumen emulsion that coats the ear canal surface.^12,33 Cerumen is a mixture of desquamated flattened keratinized squamous epithelial cells and the fatty secretions from sebaceous and ceruminous glands, and helps to maintain barrier function within the ear canal.^1,12,33 In cats, the ceruminous glands of the external acoustic meatus are folded tubular glands with a wide tubular glandular architecture and are surrounded by a single or double layer of myoepithelial cells (Figure 3). The secretory material from these modified sweat glands in and around the ears, eyes and lip margins can be both atrichial (away from the follicular infundibulum) and epitrichial (terminate in the follicular infundibulum).^5,6,24,32

Figure 3

Histopathology from a cystadenomatosis-affected ear. Courtesy of Dr P Mouser

Human and canine ceruminous glands are located in the deeper layers of the tissue, just beneath the deeper aspects of the apocrine glands of the ear canal.^3,6,7,34 To our knowledge, this has not been shown in the feline literature and, according the authors of Skin Diseases of the Dog and Cat, ‘Interestingly, cysts derived from eccrine sweat glands have not been observed in dogs or cats’ (p 666).⁶ The proportion of the ceruminous to sebaceous glands within the length of the ear canal appears to change as one moves away from the tympanic membrane.^12,35 This ratio of mainly ceruminous glands is higher in the horizontal meatus compared with the vertical meatus, where there are more sebaceous and apocrine glands.^6,12 The thin, smooth, epidermally stratified squamous epithelial lining of the external ear canal is histologically similar to that of the pinna and epidermis;¹² however, in most dog breeds, there are less simple single hair follicles within the canal, and the hairs do not extend throughout the length of the canal except in the Cocker Spaniel, which has more compound hair follicles within the acoustic meatus.^{2,12,33,36,37} Little has been published regarding this in cats. According to Fernando’s 1965 paper, secretions from the cells of the ceruminous glands do not stain histologically on Mallory’s triple staining, which differs from what is reported in dogs.^2,35 The modified apocrine glands in cat’s external ears contain acidic mucous substances, which are found in the apical parts of the glandular cells and the lumen of these glands, and have properties similar to mucous glands.^2,35The diastase-resistant periodic acid–Schiff-positive granules of the apocrine glands found in the external ear canal are located near the apical borders of the glandular cells in cats.^2,35

The bluish-black clinical appearance of the cystadenomatosis lesions are partially a reflection of the distended skin and partially attributed to the pigmentary contributions from hemosiderin and ceroid of the thick acellular or cell-poor fluid filling the cystic lumen.^5,12,15 Histopathologically, these cysts have been theorized to be caused by obstructed glandular ducts,^13,16 or retention cysts, based on the flattened appearance of epithelial cells with dermal fibrosis or due to compression exerted from benign adenomas process with papillary digital projections into the cystic cavities.¹⁵ No known etiology has been identified as a potential cause for the cyst formation, but some authors have theorized that a senile change may play a role in cyst formation.^5,6

Feline cystadenomatosis has been reported in the literature to be a rare benign neoplasia, and has been observed to occur most commonly in middle-aged to older Abyssinian, Himalayan and Persian cats.^{6,9,12,13,15,24} Therapeutic approaches ranging from benign neglect to various topical and systemic anti-inflammatory treatments to draining of the cysts to chemical ablation,^14,15,21 cauterization, cryosurgery,^27,33 surgical excision^15,31 or laser surgery^4,19,38 have been suggested; however, continued development of new lesions after removal is common.^4,15,21

In order to better understand this clinical syndrome, a retrospective study was conducted to investigate any potential association between cystadenomatosis and factors such as age, sex, breed, feline immunodeficiency virus (FIV)/feline leukemia virus (FeLV) status and comorbidities. We also decided to screen for the presence of papillomavirus (PV) DNA in tissue collected from 24/44 cystadenomatosis cases, as PV is known to be associated with the development of several types of cutaneous neoplasms.^39–41 Only cases that were examined and sampled in the period 2011–2015 were tested for PV.

Materials and methods

The medical records of 797 individual feline patients, seen by the dermatology service at Angell Animal Medical Center in Boston, MA, USA from January 2011 to December 2019 exclusively, were reviewed.

Signalment information and other data were included in the study and reviewed. To determine prevalence, the number of cases consistent with a clinical diagnosis of cystadenomatosis was compared with the total referred feline population seen by the dermatology service during the same 84 months. The medical records of all patients were reviewed. We used the first mention of otitis externa or lesions consistent with a likely diagnosis of cystadenomatosis. The identification of cysts in medical records was used as the best estimate for age of onset of cystadenomatosis in a given patient. Where such information was missing from the records, we used the date of first presentation to the dermatology service for referral as the age of onset. Data regarding sex, breed (when provided by owner) and FIV/FeLV status (when available) were collected. The histopathologic findings from 27 cats (if applicable; see Figure 3) and concurrent medical conditions were also collected.

Biopsy specimens from 24 of these animals were submitted for PCR testing to evaluate for the presence of PV. Either fresh frozen or paraffin-embedded tissue was used, and DNA was extracted with a DNeasy extraction kit (Qiagen) according to the manufacturer’s recommendations. In order to detect PV DNA in the extracts, six different PCR assays were employed. Two of the PCRs used degenerate primers for conserved regions to detect a broad spectrum of PV types, with the FAP59/FAP64 assay targeting the L1 gene and the CP4/CP5 assay targeting the E1 gene.^39,41 Additionally, four PCRs were used to test specifically for feline PV2 (FcaPV) types 1–4. For FcaPV2, the JMPF/JMPR primers were selected, while new primers were designed for FcaPV1, FcaPV3 and FcaPV4: FcaPV1_L1 f (5’-TTG GGA GAG GAC AAC CTT TG-3’)/FcaPV1_L1 r (5’-GGC TTA CAG CCC ACC ATA AA-3’), FcaPV3_L1 f (5’-GTT TGC TTT GGC AGA CCC TA-3’)/FcaPV3_L1 r (5’-TGG ACA CAT TTT GCC TTT CA-3’) and FcaPV4_L1 f (5’-TGG TGA TGA AAG GCA AAA CA-3’)/FcaPV4_L1 r (5’-CAA AGC CCA CAT CAC ACA TC-3’), respectively.⁴² The FAP59/FAP64, CP4/CP5 and JMPF/JMPR PCRs were performed as previously published,^39,41,42,43 while for the other three PCR assays an initial denaturation of 94°C for 3 mins was used, followed by 40 cycles of 94°C for 30 s, 55°C for 30 s and 72°C for 30 s. PCR products were loaded and visualized on an agarose gel, amplicons were cut out and DNA was purified using a QIAquick DNA extraction kit (Qiagen). Sequencing was performed in an ABI 3730 sequencer (Applied Biosystems), and the results were compared with the National Center for Biotechnology Information (NCBI) database using the BLAST N algorithm. The PCR protocols were performed as published and, in the case of the novel PCR assays, an initial denaturation of 94°C for 3 mins was used, followed by 40 cycles of 94°C for 30 s, 55°C for 30 s and 72°C for 30 s. PCR products were loaded and visualized on an agarose gel, amplicons were cut out and DNA was purified using a QIAquick DNA extraction kit (Qiagen). Sequencing was performed in an ABI 3730 sequencer (Applied Biosystems), and the results were compared with the NCBI database using the BLAST N algorithm.

Statistical analysis

Descriptive data were generated using www.medcalc.org and Microsoft Excel; comparison of means and a χ² test of independence were performed.

Results

Cystadenomatosis was found in 7.1% (n = 57/797) of referrals and in 0.1% of the total hospital feline population seen (n = 57/65,385) during the study period. Of the 57 cats that had lesions consistent with cystadenomatosis, 84.2% (n = 48/57) had both ears affected, and in 4/57 cats (7.0%), clinically similar cystic lesions were also noted in other locations on the body (one in the periocular region, two in the periorbital region and one in the perianal region). In 27 cats (48 ears) (47.4%, n = 27/57), the diagnosis of cystadenomatosis was confirmed histopathologically and PCR testing for the presence of PV was conducted on biopsy material from 24 of these cats. FcaPV2 DNA was detected in 4/24 (16.7%) cats.

The mean ± SD age of onset among affected cats was 11 ± 3.0 years (range 3.5–17). The mean ± SD age of unaffected cats seen by the dermatology service (n = 740) at the time of referral was 7.31 ± 4.37 years (range 0.5–19.2) (P <0.0001). Domestic shorthair cats were most commonly affected (57.9%, n = 33/57). Other breeds included domestic mediumhair (n = 13 [22.8%]), domestic longhair (n = 7 [14%]), Persian (n = 2 [3.5%]), Himalayan (n = 1 [1.8%]) and Abyssinian (n = 1 [1.8%]) (Table 1). There was no significant breed predisposition in the overall population of cats referred to the dermatology service (χ² [degrees of freedom 6, n = 797] = 0.786275, P = 0.992439, P <0.05).

Table 1

Distribution of breeds seen by the dermatology service, 2011–2019

Breed as reported by owner	Referred patients (n = 797)	Cystadenomatosis cases (n = 57)
Abyssinian	5	1
DLH	87	7
DMH	71	13
DSH	491	33
Himalayan	8	2
Persian	13	1
25 other breeds (at least one cat)	122	0

DLH = domestic longhair; DMH = domestic mediumhair; DSH = domestic shorthair

Cystadenomatosis was found in one intact female (1.8%), 14 spayed females (24.6%), two intact males (3.5 %) and 40 castrated males (70.2%). Most of the cats in both the affected and the total referred populations were spayed or castrated (n = 54/57 [94.7%] and n = 776/797 [97.4%], respectively) (Table 2). Of the 57 affected cats, there was a male:female ratio of 2.8. The male (intact plus castrated, n = 387) to female (intact and spayed, n = 410) ratio in the referral population was 0.94. The male cats had a 2.24 higher relative risk of developing cystadenomatosis than female cats (99% confidence interval 1.27–1.809).

Table 2

Sex distribution of all cats (n = 797) seen by the dermatology service, 2011–2019

Sex	Non-affected (n = 740)	Affected (n = 57)
Male intact	12	2
Male castrated	375	40
Female intact	9	1
Female spayed	401	14

Seven of the 57 cases (12.3%) were diagnosed with malignant neoplasia in and around the ears and included the following diagnoses: inflamed adenocarcinoma (n = 5); mast cell tumor on pinna (n = 1); and squamous cell carcinoma (n = 1). A range of concurrent clinical conditions was reported in the 57 affected cats, with a range of clinical signs and/or a medical history of dermatologic problems and treatments suggestive of some form of allergic dermatosis (n = 3); chronic renal failure (n = 2); pancreatitis (n = 1); chylothorax (n = 1); diabetes mellitus (n = 1); hyperthyroidism (n = 2); atopic dermatitis (n = 1); and lymphoma (n = 1). However, the majority of cases (n = 48) had no known clinical disease requiring medical attention besides secondary otitis externa (bacterial, yeast or mixed) owing to cystadenomatosis. No cats in the study had required treatment for an ear infection prior to developing cysts, other than a single cat that had a history of ear mites (Otodectes species). A review of the medical records showed that in 42 of the cases of cystadenomatosis, there had been clinical signs consistent with secondary otitis externa unilaterally or bilaterally upon or within the 6 months prior to referral.

Medical management of clinical signs in these 42 cats ranged from maintenance cleaning with various cleaning solutions to prescription otic topical medications for inflammatory and/or infectious otitis signs. No obvious pattern was seen, and comparison of effect was not performed on the different treatments, since patients were presented at various times during their treatment and disease progression.

Four cats (seven ears) needed to undergo total ear canal ablation and bulla osteotomy (TECABO) owing to progression of the cystadenomatosis and/or complications from chronic otitis externa and/or neoplasia in or around the ears. Two of the cats that underwent TECABO had initially had their diagnosis confirmed via histopathology, and had failed to resolve with CO₂ laser therapy prior to needing more extensive surgery. A single case had a unilateral TECABO and two had pinnectomy performed prior to referral owing to a diagnosis of suspected cystadenomatosis.

The FIV/FeLV status of 5/57 cats was unknown. Fifty-one cats were either listed as negative for FIV and FeLV by owners, or as current or up to date with vaccine protection for FeLV. One cat was FIV-positive and was euthanized due to a brain tumor. One cat was considered positive for feline infectious peritonitis (FIP) but remained non-clinical for FIP. None of the other cats with unknown FIV/FeLV status had malignant neoplasia in the ears. Only three (5.3%) of the 57 cats with cystadenomatosis had signs and/or medical history of dermatologic problems and treatments suggestive of some form of allergic dermatosis, prior to developing clinical cystadenomatosis.

Discussion

In this retrospective study from a referral tertiary animal hospital population, we found that feline cystadenomatosis was not associated with certain breeds such as Persians or Himalayans, as previously sugges- ted,^{13,15,16,21,27,32,44} although in a 2005 textbook one author noted that DSH cats were the most affected breed.⁶ In this study, cystadenomatosis was over-represented in non-purebred cats, though the association was not statistically significant. In the present study, male cats were 1.52 times more likely to develop ceruminous cysts than female cats, and affected male cats were more likely to be castrated than intact, consistent with previous studies and publications.^7,22,44 This raises the question of whether male sex hormones could potentially affect glandular tissue and play some role in its progression into a cystic pathology, even with the majority of patients being spayed or castrated. Similar to previous studies, the condition appears to occur in cats as young as 3.5 years of age but more commonly affects older cats, as in our study population (mean of 11 years).^7,15,24,44

Most cats had bilateral disease, with or without lesions associated with the ears (n = 4/57). The periocular zone appears to be the second most common area to develop cystic lesions (n = 2/57), which is consistent with the ophthalmology literature.^13,16,27 The condition has been recognized in almost all regions of the world short of Oceania and Africa. In our view, this is more likely to be due to a lack of publications on the topic, rather a true reflection of the prevalence of disease. The most common clinical presentation beside cysts was the owner experiencing increasing difficulty with the management of secondary bacterial and/or Malassezia otitis externa. This was likely due to growth of the cystic lesions in the tragus and meatic entrance, making topical treatments more difficult for owners.^4,15,21,41

CO₂ laser surgery using a model LX-20SP (www.aesculight.com) was carried out by two of the authors (KEL and BS) on a total of 34 ears and in three non-ear locations (chin, lip, perianal area) in 23 patients (three cats had TECABO or pinnectomy prior to referral). In this study, we found that CO₂ laser surgery was, subjectively, a good treatment option for patients where cysts had reached a size or distribution that caused increased risk of otitis externa owing to the obstructive nature of the lesions, patient discomfort or increased difficulty in resolving secondary infections. Post-laser complications were short term and only three cats required 14 days of treatment. Regarding secondary infections, the most common clinical post-procedural observation by owners and clinicians was, surprisingly, minimal local discomfort for a few days after the procedure (Figure 4). However, a limitation of CO₂ laser therapy is that it is unable to treat cysts that extend deep into the horizontal canal without causing damage to unaffected tissues. Diode laser and holmium type lasers will likely be advantageous in these cases, but the cost might be a limiting factor. We have carried out ‘touch-up’ treatment on four severely affected cases over the span of the study, mainly when the cats where under general anesthesia for other reasons such as for dental cleaning. In two cats with malignant ear tumors, we performed a second round of CO₂ laser treatment in an attempt to give those cats additional quality of life and allowing for topical palliative care, without resolving the malignancy.

Figure 4

Post-CO₂ laser of same cat as in Figure 1. Courtesy of Dr P Mouser

The nine cats with concurrent non-cystadenoma medical conditions were considered to be within the normal occurrence in a population of senior cats, and we could not establish any pattern between their conditions and cystadenomatosis. No association with PV infection was found with the PCR testing carried out in 24 cases. Although FcaPV2, in particular, has been found to be causally involved in the etiology of certain human and feline cutaneous tumors,^39,40,45,46 the virus may also be found in or on the skin of cats without any associated clinical signs.⁴³ The detection of FcaPV2 DNA in 4/24 tested cats indicates no connection between cystomatosis and PV infection. We also did not establish any association between FIV/FeLV or FIP and cystadenomatosis in our population. In a previous study, 1/4 cats with benign ear tumors tested positive for FeLV and two and one of 56 cats with malignant ear tumors were FeLV positive and FIV positive, respectively.

Based on the documented communication with the client or owner, the cats in our study did not have a history of aural clinical signs prior to the cysts being noted by the owners and/or veterinarians. Only one of the affected cats was confirmed to have had ear mites (Otodectes cynotis) prior to the development of cystadenomatosis. However, the lack of previous history of otitis externa suggests that cystadenomatosis does not appear to be a reactive hyperplastic change for the majority of cases or appear to be over-represented among allergic or hypersensitive cats since only 3/57 had signs of allergic skin disease. Furthermore, the prevalence of ear mite infestations is highest in young individuals owing to transmission from the queen to the kitten.^15,20,47,48 However, feline cystadenomatosis is more commonly found in cats that are middle-aged and older and could support a possible senile or degenerative change in the tissue or its associated structures, and be less supportive of a congenital etiology.²² The finding of neoplastic conditions in 17% of the cases is in line with what has previously been reported in the literature, where the mean age of onset for malignant ear tumors (such as ceruminous adenocarcinoma and squamous cell carcinoma) is 11 years.^7,12,15,44 In the present study, there was no significant association between cystadenomatosis and malignant ear neoplasia.

Conclusions

Further investigation into the pathology of adenoma formation, and particularly into the feline apocrine and ceruminous glands, will be needed to identify specific etiologic factors and subsequent potential effective strategies for reducing the complications associated with cystadenomatosis.

In our experience, CO₂ laser therapy appears to be a useful approach for ablating cysts in more mild cases and minimizing the risk of obstruction in more severe cases.^19,21,38

It is possible that a similar effect could be achieved with cryotherapy and/or electrocautery, but we have had less success with this approach. In cases with moderate obstructive changes of the upper sections of the acoustic meatus, the reconstructive surgery proposed by Pavletic³¹ could be a viable consideration.

Footnotes

Acknowledgements

We would like to thanks Drs Coster, Ewing and Mouser (all from Angell AMC, Boston, MA, USA) for their generous help in reviewing sections of the article, as well as gathering images of feline patients and in providing photomicrographs of the tissue.

Accepted: 23 May 2021

Author note

This study was presented, in part, at the North American Veterinary Dermatology Forum (NAVDF) 2014 in Phoenix, AZ, USA, and the NAVDF 2017 in Orlando, FL, USA. These two initial presentations was approved by the Angell Institutional Research Board.

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 self-funded.

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 recognized high standards (‘best practice’) of individual veterinary clinical patient care were followed. Ethical approval from a committee was therefore not specifically required for publication in JFMS.

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

Klaus E Loft

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Feline cystadenomatosis affecting the ears and skin of 57 cats (2011–2019)

Abstract

Objectives

Methods

Results

Conclusions and relevance

Keywords

Introduction

Materials and methods

Statistical analysis

Results

Discussion

Conclusions

Footnotes

Acknowledgements

Author note

Conflict of interest

Funding

Ethical approval

Informed consent

ORCID iD

References