In recent years, the incidence of neoplastic lesions in companion animals, especially dogs, has been steadily increasing (1, 8, 9, 10, 13, 28). Skin tumours, which rank first among neoplastic lesions in dogs, are diagnosed most frequently (8). They are characterised by a vast array of histological types and constitute the most heterogeneous group of tumours. This is associated with the structure of the skin, as all of its components can undergo neoplastic transformation. According to the WHO classification, neoplasms of epithelial origin represent various histological types and originate from the epidermis and its adnexal structures. This group comprises epidermal tumours, hair follicle tumours, sebaceous gland tumours with their modifications, and apocrine sweat gland tumours and their derivatives (11). Another large group comprises mesenchymal and melanocytic tumours divided into benign and malignant neoplasms (11, 14). Epidemiological studies in veterinary oncological medicine are particularly important, as they expand the knowledge of the prevalence and development of neoplastic lesions and provide valuable information on individual types of tumours prevailing in different regions of the world. As shown by literature reports, the prevalence of specific histological types of skin tumour differs between geographic areas. Mast cell tumours have been mainly diagnosed in the UK, the USA, Thailand, Australia, Switzerland, and Brazil (2, 7, 12, 19). In turn, histiocytomas are most frequently diagnosed in India, whereas lipomas are dominant in another Asian country,
The analysis covered 3,139 skin tumour samples collected in 2016–2021 at the Department of Pathomorphology and Forensic Veterinary Medicine, University of Life Sciences in Lublin, Poland. They were collected from dogs undergoing surgical removal of skin tumours carried out at the Veterinary Clinic of the University of Life Sciences in Lublin and in private veterinary clinics in Poland. The study involved 35 breeds, crossbreed dogs, and breeds aggregated into an „other” group represented by fewer than nine individuals. Clinical data on the breed, age and sex of the dogs and the location of the tumour were obtained from referrals delivered to the Department of Pathomorphology and Forensic Veterinary Medicine together with the tissue material intended for histopathological examination. Only dogs with a full data set qualified for the study. Multiple tumours diagnosed in one individual were assessed separately. In terms of tumour location, 10 anatomical areas were distinguished: the head, neck, torso, thoracic limbs, axilla, pelvic limbs, inguinal area, perineum, anus, and tail. The dogs were divided into four age groups: 0–3 year-olds, 4–6 year-olds, 7–10 year-olds and 11–20 year-olds. Slides for microscopic examination were routinely stained with haematoxylin and eosin. Immunohistochemical staining (anti-vimentin, anti-cytokeratin, anti-CD3, anti-CD79α and anti-Melan A) was additionally used in doubtful cases, and toluidine blue was applied to stain mast cells. The histopathological analyses of skin tumours were based on the amended WHO classification (11, 14, 27). The data were analysed statistically, and the values of qualitative variables were presented with the use of frequency and percentage. Multivariate logistic regression analysis was employed to estimate the risk of malignant
The analysis of the results of the five-year study showed the highest number of skin tumours in the last year of the study (2021), with a frequency of 25.61%, and the lowest number in 2017 with a frequency of 11.41%. The number of diagnosed tumours was noted to increase gradually every year (Fig. 1).
The highest percentage of skin tumours was diagnosed in Labrador retrievers (7.13%), German shepherds (5.60%), and Yorkshire terriers (4.96%). The crossbreed dogs also constituted a large group affected by tumours (38.70%) (Table 1).
Frequency of canine skin tumours depending on gender, age, breed and anatomical location
n | % | |||
---|---|---|---|---|
Sex | Female | 1,483 | 47.24 | |
Male | 1,656 | 52.76 | ||
Age | 0–3 y | 390 | 12.43 | |
4–6 y | 500 | 15.93 | ||
7–10 y | 1,381 | 43.99 | ||
11–20 y | 868 | 27.65 | ||
M ± SD | 8.23 ± 3.60 | |||
Me (Q1–Q3) | 9 (6–11) | |||
min–max | 0.5–20 | |||
Breed | Crossbreed | 1,215 | 38.71 | |
Labrador retriever | 224 | 7.14 | ||
German shepherd | 176 | 5.61 | ||
Yorkshire terrier | 156 | 4.97 | ||
Spaniel | 119 | 3.79 | ||
Bulldog | 104 | 3.31 | ||
Schnauzer | 95 | 3.03 | ||
Boxer | 83 | 2.64 | ||
Shih tzu | 80 | 2.55 | ||
Golden retriever | 77 | 2.45 | ||
Bernese dog | 73 | 2.32 | ||
American Staffordshire terrier | 63 | 2.01 | ||
Beagle | 56 | 1.78 | ||
Maltese | 55 | 1.75 | ||
Dachshund | 48 | 1.53 | ||
Siberian husky | 43 | 1.37 | ||
Other terriers | 40 | 1.27 | ||
West Highland white terrier | 31 | 0.99 | ||
Bull terrier | 25 | 0.80 | ||
Cane Corso | 23 | 0.73 | ||
Rhodesian ridgeback | 10 | 0.32 | ||
Chihuahua | 10 | 0.32 | ||
Pointer | 20 | 0.64 | ||
Pekingese | 19 | 0.60 | ||
Fox terrier | 19 | 0.60 | ||
Pug | 17 | 0.54 | ||
Setter | 14 | 0.45 | ||
Alaskan Malamute | 14 | 0.45 | ||
Bavarian mountain hound | 12 | 0.38 | ||
Dobermann | 12 | 0.38 | ||
Poodle | 12 | 0.38 | ||
Shar pei | 12 | 0.38 | ||
Polish hunting dog | 11 | 0.35 | ||
Pinscher | 10 | 0.32 | ||
Black Russian terrier | 9 | 0.29 | ||
Flat-coated retriever | 9 | 0.29 | ||
Other | 143 | 4.56 | ||
Location | Torso | 861 | 27.43 | |
Head | 736 | 23.44 | ||
Thoracic limb | 466 | 14.84 | ||
Pelvic limb | 456 | 14.53 | ||
Anus | 213 | 6.79 | ||
Neck | 165 | 5.26 | ||
Tail | 71 | 2.26 | ||
Axilla | 70 | 2.23 | ||
Perineum | 62 | 1.98 | ||
Inguinal area | 39 | 1.24 |
N – number of cases; M – mean; SD – standard deviation; Me – median; Q1 – lower quartile; Q3 – upper quartile; min – minimum value; max – maximum value
Significantly greater numbers of skin tumours were diagnosed in male dogs (52.75%). They were most frequently diagnosed in the group aged 7–10 years (43.99%), where the median patient age was 9 years. They were located on the torso (27.42%) and head (23.44%) (Table 2). Microscopic analysis showed a significant predominance of benign tumours, with a frequency of 65.02%, as well as of mesenchymal and melanocytic tumours with a frequency of 59.58% (Table 2). Mast cell tumours accounted for the largest percentage of the entire tumour population,
Frequency of occurrence of a particular histological types of skin tumours in dogs
N | % | N | % | ||
---|---|---|---|---|---|
Sebaceous adenoma | 133 | 4.24 | Squamous cell carcinoma | 92 | 2.93 |
Trichoblastoma | 116 | 3.70 | Hepatoid epithelioma | 88 | 2.80 |
Trichoepithelioma | 116 | 3.70 | Meibomian epithelioma | 85 | 2.71 |
Hepatoid adenoma | 92 | 2.93 | Sebaceous epithelioma | 63 | 2.01 |
Papilloma | 73 | 2.33 | Apocrine adenocarcinoma | 48 | 1.53 |
Keratoacanthoma | 68 | 2.17 | Basal cell carcinoma | 31 | 0.99 |
Pilomatricoma | 65 | 2.07 | Sebaceous adenocarcinoma | 30 | 0.96 |
Apocrine adenoma | 52 | 1.66 | Malignant trichoepithelioma | 15 | 0.48 |
Meibomian adenoma | 50 | 1.59 | Hepatoid adenocarcinoma | 13 | 0.41 |
Tricholemmoma | 13 | 0.41 | Anal sac gland tumour | 10 | 0.32 |
Ceruminous adenoma | 6 | 0.19 | Ceruminous adenocarcinoma | 7 | 0.22 |
Meibomian adenocarcinoma | 3 | 0.10 | |||
Histiocytoma | 371 | 11.82 | Mast cell tumours | 433 | 13.79 |
Lipoma | 202 | 6.43 | Haemangiopericytoma | 187 | 5.96 |
Fibroma | 108 | 3.43 | Malignant melanoma | 146 | 4.65 |
Haemangioma | 64 | 2.04 | Fibrosarcoma | 77 | 2.45 |
Plasmacytoma | 43 | 1.37 | Peripheral nerve sheath tumour | 34 | 1.08 |
Melanocytoma | 43 | 1.37 | Haemangiosarcoma | 21 | 0.67 |
Fibrolipoma | 41 | 1.31 | Liposarcoma | 20 | 0.64 |
Lymphangioma | 8 | 0.25 | Myxosarcoma | 16 | 0.51 |
Myxoma | 4 | 0.12 | Cutaneous lymphoma | 13 | 0.41 |
Hibernoma | 1 | 0.03 | Histiocytic sarcoma | 33 | 0.15 |
Neurofibroma | 1 | 0.03 | Malignant histiocytosis | 4 | 0.13 |
Total: n = 3,139 |
The statistical analysis revealed that the risk of a tumour being malignant rather than benign was 1.212 times higher in the female than in the male dogs. The odds ratio (OR) for the occurrence of a malignant tumour in the group of the youngest dogs aged 0–3 years was 0.24, which indicates a fourfold lower risk of development of malignant tumours than for dogs aged 4–6 years. The risk of development of malignant neoplasms on the neck was 1.850 higher than the risk of benign neoplasms in this location. It was found that the following breeds of dogs faced a higher risk of developing malignant tumours than crossbreed dogs: golden retrievers (OR 2.096), boxers (OR 2.255), German shepherds (OR 1.878) and Maltese (OR 2.926) (Table 3).
Odds ratios (ORs) and 95% confidence intervals (CIs) of malignant canine skin neoplasia in relation to benign ones by sex, age, tumour location and breed
OR | 95% CI | P-value | ||
---|---|---|---|---|
Sex (reference: male) | Female | 1.211 | 1.033–1.419 | 0.018 |
Age (reference: 4–6 years) | 0–3 y | 0.245 | 0.177–0.339 | <0.001 |
7–10 y | 0.659 | 0.528–0.823 | <0.001 | |
11–20 y | 0.530 | 0.413–0.679 | <0.001 | |
Location (reference: torso) | Head | 0.454 | 0.363–0.568 | <0.001 |
Thoracic limb | 0.493 | 0.382–0.635 | <0.001 | |
Perineum | 0.950 | 0.552–1.637 | 0.855 | |
Pelvic limb | 0.804 | 0.630–1.026 | 0.080 | |
Neck | 1.850 | 1.296–2.642 | <0.001 | |
Anus | 0.236 | 0.155–0.360 | <0.001 | |
Tail | 1.259 | 0.759–2.090 | 0.373 | |
Inguinal area | 1.472 | 0.754–2.873 | 0.257 | |
Axilla | 0.604 | 0.356–1.026 | 0.062 | |
Breed (reference: crossbreed) | Golden retriever | 2.096 | 1.297–3.386 | 0.003 |
Bull terrier | 1.148 | 0.490–2.689 | 0.750 | |
Boxer | 2.255 | 1.405–3.620 | <0.001 | |
Bulldog | 0.628 | 0.371–1.065 | 0.084 | |
West Highland white terrier | 0.911 | 0.405–2.050 | 0.822 | |
German shepherd | 1.878 | 1.342–2.628 | <0.001 | |
Pekingese | 0.823 | 0.283–2.389 | 0.720 | |
Black Russian terrier | 0.706 | 0.160–3.114 | 0.646 | |
Other terriers | 0.720 | 0.338–1.536 | 0.396 | |
Yorkshire terrier | 0.997 | 0.695–1.431 | 0.988 | |
American Staffordshire terrier | 0.959 | 0.551–1.669 | 0.882 | |
Shih tzu | 0.469 | 0.263–0.836 | 0.010 | |
Beagle | 0.624 | 0.326–1.193 | 0.154 | |
Schnauzer | 0.983 | 0.626–1.544 | 0.940 | |
Labrador retriever | 0.842 | 0.616–1.153 | 0.284 | |
Spaniel | 0.607 | 0.380–0.969 | 0.037 | |
Maltese | 2.926 | 1.634–5.239 | <0.001 | |
Bavarian mountain hound | 0.261 | 0.055–1.244 | 0.092 | |
Siberian husky | 0.732 | 0.363–1.476 | 0.383 | |
Bernese mountain dog | 0.717 | 0.417–1.234 | 0.230 | |
Flat-coated retriever | 3.685 | 0.887–15.309 | 0.073 | |
Dobermann | 0.159 | 0.020–1.289 | 0.085 | |
Poodle | 0.321 | 0.067–1.541 | 0.156 | |
Dachshund | 0.313 | 0.136–0.720 | 0.006 | |
Fox terrier | 0.912 | 0.330–2.520 | 0.859 | |
Shar pei | 0.597 | 0.153–2.328 | 0.458 | |
Cane Corso | 1.194 | 0.488–2.922 | 0.698 | |
Polish hunting dog | 0.427 | 0.088–2.065 | 0.290 | |
Setter | 0.734 | 0.219–2.463 | 0.617 | |
Pug | 2.315 | 0.794–6.753 | 0.124 | |
Alaskan Malamute | 0.376 | 0.096–1.470 | 0.160 | |
Rhodesian ridgeback | 0.907 | 0.243–3.392 | 0.885 | |
Pointer | 0.881 | 0.330–2.351 | 0.801 | |
Pinscher | 0.000 | – | 0.998 | |
Chihuahua | 0.351 | 0.068–1.808 | 0.211 | |
Other | 1.036 | 0.709–1.516 | 0.854 |
In the group comprising only epithelial tumours, a higher risk of development of malignant
Odds ratios (ORs) and 95% confidence intervals (CIs) of malignant canine epithelial skin tumours in relation to benign ones by sex, age, tumour location and breed
OR | 95% CI | P-value | ||
---|---|---|---|---|
Sex (reference: male) | Female | 2.087 | 1.294-3.366 | 0.003 |
Age (reference: 4–6 years) | 0-3 y | 0.358 | 0.151-0.847 | 0.019 |
7-10 y | 0.922 | 0.469–1.814 | 0.814 | |
11-20 y | 0.740 | 0.345–1.589 | 0.440 | |
Location (reference: torso) | Head | 0.115 | 0.051–0.260 | <0.001 |
Thoracic limb | 0.343 | 0.152–0.776 | 0.010 | |
Perineum | 0.733 | 0.154–3.481 | 0.696 | |
Pelvic limb | 1.179 | 0.624–2.227 | 0.611 | |
Neck | 1.928 | 0.743–5.002 | 0.177 | |
Anus | 0.105 | 0.024–0.454 | 0.003 | |
Tail | 0.509 | 0.134–1.932 | 0.321 | |
Inguinal area | 1.144 | 0.122–10.762 | 0.906 | |
Axilla | 2.444 | 0.610–9.798 | 0.207 | |
Breed (reference: crossbreed) | Golden retriever | 1.275 | 0.340–4.775 | 0.718 |
Bull terrier | 0.000 | - | 0.998 | |
Boxer | 4.091 | 1.607–10.416 | 0.003 | |
Bulldog | 0.210 | 0.027–1.651 | 0.138 | |
West Highland white terrier | 1.355 | 0.164–11.224 | 0.778 | |
German shepherd | 4.085 | 1.866–8.942 | <0.001 | |
Pekingese | 0.000 | - | 0.998 | |
Black Russian terrier | 3.181 | 0.310–32.684 | 0.330 | |
Other terriers | 0.517 | 0.062–4.295 | 0.541 | |
Yorkshire terrier | 0.552 | 0.184–1.660 | 0.290 | |
American Staffordshire terrier | 0.000 | - | 0.997 | |
Shih tzu | 0.000 | - | 0.995 | |
Beagle | 0.947 | 0.203–4.422 | 0.945 | |
Schnauzer | 0.917 | 0.260–3.241 | 0.893 | |
Labrador retriever | 1.516 | 0.581–3.957 | 0.395 | |
Spaniel | 0.000 | - | 0.994 | |
Maltese | 2.220 | 0.417–11.819 | 0.350 | |
Bavarian mountain hound | 0.000 | - | 0.998 | |
Siberian husky | 0.000 | - | 0.997 | |
Bernese mountain dog | 1.130 | 0.303–4.218 | 0.856 | |
Flat-coated retriever | 43.596 | 2.982–637.459 | 0.006 | |
Dobermann | 0.000 | - | 0.999 | |
Poodle | 0.000 | - | 0.999 | |
Dachshund | 0.000 | - | 0.996 | |
Fox terrier | 0.000 | - | 0.998 | |
Shar pei | 0.000 | - | 0.998 | |
Cane Corso | 0.746 | 0.079–7.034 | 0.798 | |
Polish hunting dog | 0.000 | - | 0.998 | |
Setter | 3.627 | 0.317–41.574 | 0.300 | |
Pug | 0.000 | - | 0.999 | |
Alaskan Malamute | 0.000 | - | 0.998 | |
Rhodesian ridgeback | 8.452 | 0.502–142.217 | 0.138 | |
Pointer | 0.000 | - | 0.998 | |
Pinscher | 0.000 | - | 0.998 | |
Chihuahua | 0.000 | - | 0.999 | |
Other | 0.998 | 0.326–3.057 | 0.997 |
The statistical analysis of the occurrence of mesenchymal neoplasms showed no statistically significant differences between the sexes. In comparison with the torso, the tail (OR 4.563) and anus (OR 8.235) locations were associated with a higher risk of neoplasm development. In terms of the breed, a higher risk of malignant mesenchymal tumours was found in Golden retrievers (OR 4.693), boxers (OR 2.342), bulldogs (OR 3.469) and Maltese (OR 2.757) (Table 5).
Odds ratios (ORs) and 95% confidence intervals (CIs) of malignant canine mesenchymal skin tumours in relation to benign ones by sex, age, tumour location and breed of dogs
OR | 95% CI | P-value | ||
Sex (reference: male) | Female | 0.875 | 0.708–1.082 | 0.218 |
Age (reference: 4–6 years) | 0–3 y | 0.851 | 0.484–1.495 | 0.574 |
7–10 y | 0.542 | 0.400–0.733 | <0.001 | |
11–20 y | 0.488 | 0.348–0.684 | <0.001 | |
Location (reference: torso) | Head | 2.468 | 1.698–3.587 | <0.001 |
Thoracic limb | 0.541 | 0.400–0.730 | <0.001 | |
Perineum | 1.301 | 0.620–2.730 | 0.486 | |
Pelvic limb | 0.742 | 0.550–0.999 | 0.049 | |
Neck | 2.218 | 1.388–3.543 | <0.001 | |
Anus | 8.235 | 2.431–27.896 | <0.001 | |
Tail | 4.563 | 1.703–12.221 | 0.003 | |
Inguinal area | 1.151 | 0.543–2.440 | 0.715 | |
Axilla | 0.387 | 0.213–0.704 | 0.002 | |
Breed (reference: crossbreed) | Golden retriever | 4.693 | 1.913–11.514 | <0.001 |
Bull terrier | 1.910 | 0.575–6.339 | 0.290 | |
Boxer | 2.342 | 1.171–4.684 | 0.016 | |
Bulldog | 3.469 | 1.137–10.584 | 0.029 | |
West Highland white terrier | 1.479 | 0.420–5.207 | 0.542 | |
German shepherd | 1.546 | 0.995–2.400 | 0.053 | |
Pekingese | 1.060 | 0.298–3.774 | 0.928 | |
Black Russian terrier | 0.576 | 0.069–4.814 | 0.611 | |
Other terriers | 1.168 | 0.372–3.667 | 0.790 | |
Yorkshire terrier | 1.465 | 0.854–2.511 | 0.165 | |
American Staffordshire terrier | 0.843 | 0.439–1.618 | 0.607 | |
Shih tzu | 0.771 | 0.362–1.645 | 0.501 | |
Beagle | 0.543 | 0.240–1.229 | 0.143 | |
Schnauzer | 1.361 | 0.726–2.549 | 0.336 | |
Labrador retriever | 0.635 | 0.438–0.923 | 0.017 | |
Spaniel | 1.520 | 0.705–3.276 | 0.285 | |
Maltese | 2.757 | 1.218–6.243 | 0.015 | |
Bavarian mountain hound | 0.415 | 0.070–2.452 | 0.332 | |
Siberian husky | 0.674 | 0.295–1.541 | 0.350 | |
Bernese mountain dog | 0.712 | 0.351–1.442 | 0.345 | |
Flat-coated retriever | 1.987 | 0.341–11.583 | 0.445 | |
Dobermann | 0.101 | 0.012–0.873 | 0.037 | |
Poodle | 0.258 | 0.044–1.529 | 0.136 | |
Dachshund | 0.565 | 0.202–1.579 | 0.277 | |
Fox terrier | 1.317 | 0.343–5.061 | 0.688 | |
Shar pei | 1.076 | 0.208–5.556 | 0.930 | |
Cane Corso | 1.620 | 0.406–6.466 | 0.495 | |
Polish hunting dog | 0.638 | 0.101–4.027 | 0.633 | |
Setter | 0.257 | 0.059–1.123 | 0.071 | |
Pug | 3.684 | 0.755–17.976 | 0.107 | |
Alaskan Malamute | 0.495 | 0.096–2.556 | 0.401 | |
Rhodesian ridgeback | 0.373 | 0.078–1.781 | 0.216 | |
Pointer | 0.896 | 0.215–3.735 | 0.880 | |
Pinscher | 0.000 | – | 0.999 | |
Chihuahua | 0.377 | 0.053–2.684 | 0.330 | |
Other | 1.143 | 0.672–1.943 | 0.622 |
The highest prevalence of skin tumours was observed in the last year (2021) of the five-year study, with a frequency of 25.60%, and the lowest number was recorded in 2017 (11.41%). The number of diagnosed tumours was found to increase gradually each year. As it would seem from the literature data, the prevalence of tumours in companion animals, mainly dogs, has been growing in recent years (8). Certainly, the present results confirm this, but factors must also be taken into account for a true interpretation of tumour incidence data,
Benign tumours were the most numerous in the analysed group of neoplasms (65.02%), as in other reports from Europe (6, 13, 20). In contrast, in Asia different proportions with a predominance of malignant tumours were recorded,
The highest number of skin tumours was diagnosed in dogs aged 7–10 years, with the median animal age being 9 years. Similarly, over 50% of dogs examined in a study conducted in Switzerland were 8–11 years old, and the median age in Japan was similar,
When sex is the factor of interest instead of age, the results of analyses of the development of tumours are highly diverse. Some studies have shown no sex dependence of the tumour risk, whereas other reports have confirmed one (12, 16, 20). The present statistical analyses indicated for the first time an increased risk of malignant neoplasms and skin tumours in female dogs. No relationship between dogs’ sex and skin tumour malignancy had been documented prior to this. We had no data on the sterilisation or castration status of the dogs to determine the effect of sex hormones. It is generally agreed that castration can reduce the risk of development of malignant tumours of the reproductive system. However, contrasting reports show that castration and sterilisation increase the risk of MCT development (30). Therefore, the present results can serve as a reference point for further studies.
It has been reported in the literature that golden retrievers face an increased risk of malignancies, with which our observations are in agreement (1, 29). Previous studies confirmed their predisposition to develop soft tissue sarcomas, lymphomas, mast cell tumours and melanomas,
Besides being identified in golden retrievers, an increased risk of mesenchymal malignancies was also found in the bulldogs. The studied group comprised both French and English bulldogs, which are breeds phylogenetically related to the boxer. An increased risk of MCT in these dogs has been confirmed by the available literature data (21, 23). A high prevalence of histiocytic hyperplasia in this breed was shown in one of the reports (20). In the current investigation, an increased risk of skin tumour development was also observed in the Maltese breed. There are no data on the prevalence of tumours in this breed, and the elevated risk of skin neoplasms in these dogs has been reported for the first time. The result concerning the risk of skin tumours in flat-coated retrievers should be treated with caution. The high value of OR 43.596 and the wide range of 95% CI (2.982–637.459) may be related to the small number of cases available for statistical analysis, as this breed is rare in Poland. However, it should be emphasised that more than half of the population of dogs of this breed studied by Adams
The present study extends the current knowledge on the prevalence of canine skin tumours and disseminates new data. These data provide additional knowledge of the clinical nature of skin tumours and breed-, age-, and location-related predispositions. The results presented here may also serve as a reference point for further studies of the complex biology of these tumours and as prognostic factors.