1岁以内犬的皮肤肿块

王帆

Skin masses in dogs under one year of age

1岁以内犬的皮肤肿块

作者:D.Kim, M. J. Dobromylskyj, D. O’Neill and K. C. Smith,

翻译：王帆

Objectives: To utilise a large histopathology database to ascertain the incidence and nature of skin masses in young dogs from 0 to 12months of age.

Materials and Methods: A total of 2554 submissions received for histopathology from dogs 0 to 12months of age, clinically diagnosed with a skin mass between 2006 and 2013, were retrieved from the database of a large commercial diagnostic laboratory. The histological diagnosis and site of the lesion, together with age, breed and sex of the dog were recorded.

Results: The most common skin mass found in this study was histiocytoma (n=2212, 86.6%). The majority of all submissions were neoplastic (n=2408, 94.3%), and most of those were benign (n=2372, 98.5%). Almost all of the benign neoplastic lesions were of round cell origin (n=2229, 94.0%) whereas most of the non-neoplastic lesions were derived from the epithelium (n=136, 93.8%). The five most commonly diagnosed skin masses in young dogs were histiocytoma, papilloma, dermoid cyst, follicular cyst and mast cell tumour. A male predisposition was shown for histiocytoma (odds ratio 1.72) and mast cell tumour (odds ratio 2.18) with a strong site predilection for the limb region (30.8% and 27.8% respectively). Dermoid cysts and follicular cysts were most commonly found in the skin of the abdomen (64.7% and 52.3% respectively) with boxers being predisposed (25.9% of dermoid cyst and 25.0% of follicular cyst).

Clinical Significance: A large proportion of skin mass submissions in young dogs were neoplastic and benign. Also, the most common skin mass in young dogs was found to be histiocytoma. Tumours can occur in this age group and should be considered as a potential differential diagnosis also in young patients presenting with a skin mass.

目的:利用一个大型组织病理学数据库来确定0至12月龄的幼犬皮肤肿块的发病率和性质。

材料与方法:从一家大型商业诊断实验室的数据库中检索了2006年至2013年期间临床诊断为皮肤肿块的0至12月龄的犬，共收到2554份组织病理学报告。记录病变的组织学诊断和部位，以及犬的年龄、品种和性别。

结果:本研究中发现的最常见的皮肤肿块是组织细胞瘤(n=2212, 86.6%)。大多数提交的病例为肿瘤(n=2408, 94.3%)，大多数为良性(n=2372, 98.5%)。良性肿瘤病变几乎全部来源于圆形细胞(n=2229, 94.0%)，而非肿瘤性病变大部分来源于上皮细胞(n= 136,93.8%)。幼犬最常诊断的皮肤肿块为组织细胞瘤、乳头状瘤、皮样囊肿、毛囊囊肿和肥大细胞瘤。雄性易患组织细胞瘤(比值比为1.72)和肥大细胞瘤(比值比为2.18)，在四肢区域有强烈的部位倾向性(分别为30.8%和27.8%)。皮样囊肿和毛囊囊肿以腹部皮肤最常见(分别为64.7%和52.3%)，拳师犬易感(皮样囊肿和毛囊囊肿分别为25.9%和25.0%)。

临床意义:幼犬皮肤肿块中大部分为良性肿瘤。此外，发现年轻犬最常见的皮肤肿块是组织细胞瘤。此年龄组可能发生肿瘤，年轻患犬出现皮肤肿块应把肿瘤作为潜在鉴别诊断。

INTRODUCTION

介绍

The skin is the largest organ in the body and a system in which abnormalities can be easily recognised (Goldschmidt & Shofer 1992). It is also the most common site for tumours in dogs (Moriello & Rosenthal 1990, Dobson et al. 2006, Murphy 2006), and the incidence of tumours and tumour-like lesions of the skin has been reported to be as high as 45% of 65,000 dog specimens (Goldschmidt & Shofer 1992). Moreover, skin tumours are the most common histopathological specimen submitted to diagnostic laboratories (Meuten 2017), illustrating their importance in clinical practice.

皮肤是人体最大的器官，是一个很容易观察到异常的系统。这也是犬最常见的肿瘤部位，据报道，在65000只犬的样本中，皮肤肿瘤和皮肤肿瘤样病变的发病率高达45%。此外，皮肤肿瘤是提交到诊断实验室的最常见的组织病理学样本，说明了其在临床实践中的重要性。

Multiple studies have explored the most commonly arising skin tumours in dogs of all ages and in different countries (Moulton 1978, Goldschmidt & Shofer 1992, Chikweto et al. 2011). Canine skin tumours with the highest incidence in previous studies include mast cell tumours (MCTs), lipomas and histiocytomas (Goldschmidt & Shofer 1992, Bronden et al. 2010, Chikweto et al. 2011, Graf et al. 2018). It has also been reported that most canine skin tumours are benign (Murphy 2006) and that there is a higher incidence in female dogs compared with males (Moriello & Rosenthal 1990). However, there is a lack of agreement between studies on breed predispositions, with some demonstrating an increased incidence of skin tumours in the boxer, Scottish terrier, bullmastiff, Basset Hound, Weimaraner, Kerry Blue terrier and Norwegian Elkhound (Moriello & Rosenthal 1990), while others report the giant and standard schnauzer, Magyar Vizsla, Rhodesian Ridgeback and Nova Scotia Duck Tolling Retriever to be predisposed to developing skin tumours (Graf et al. 2018). Previous studies indicate that skin tumours are more likely to occur in older dogs (Moriello & Rosenthal 1990) and are an important differential for skin masses in this older age group. However, there is a lack of research specifically focusing on the incidence and types of skin tumours in very young dogs.

多项研究探索了不同国家、不同年龄的犬最常见的皮肤肿瘤。在以前的研究中，发病率最高的犬皮肤肿瘤包括肥大细胞瘤(MCT)、脂肪瘤和组织细胞瘤。也有报道称，大多数犬的皮肤肿瘤是良性的，雌性犬比雄性犬的发病率更高。然而，关于品种倾向性的研究缺乏一致，一些研究表明，拳师犬、苏格兰㹴、斗牛犬、巴吉度猎犬、魏玛犬、凯利蓝㹴和挪威猎鹿犬的皮肤肿瘤发病率增加，而另一些研究则报告了巨型和标准雪纳瑞犬、维斯拉犬、罗得西亚脊背犬和新斯科舍猎鸭寻回犬易患皮肤肿瘤。先前的研究表明，皮肤肿瘤更可能发生在老年犬，这是老年犬皮肤肿块的重要鉴别诊断。然而，目前还缺乏专门针对幼犬皮肤肿瘤的发病率和种类的研究。

This current study aims to explore the occurrence of cystic, hyperplastic and neoplastic lesions arising in the skin of young dogs from 0 to 12months of age; to determine what proportion of the neoplastic lesions are malignant; and to report breed, age and sex as risk factors for the most common skin masses. The aim is to explore the potential importance of skin masses in very young dogs.

本研究旨在探讨0-12月龄幼犬皮肤囊性、增生性和肿瘤性病变的发生情况;确定恶性肿瘤病变的比例，以及报告最常见的皮肤肿块的危险因素：品种、年龄和性别。目的是探索年轻犬皮肤肿块的潜在重要性。

MATERIALS AND METHODS

材料和方法

Records from a large commercial diagnostic laboratory were searched for canine submissions on all skin masses submitted for histopathology from dogs aged between 0 and including 12months old received between May 31, 2006, and December 3, 2013, from practices in the UK and Europe. For each case, available data were extracted on the breed, age and sex of the dog, the body location(s) of the sample(s) and the diagnosis made by the original reporting histopathologist. A total of 18 pathologists have reviewed the submission and a small number of MCT cases had either a Giemsa or a Toluidine blue histochemical stain performed to confirm the presence of mast cell granules in the neoplastic cell population. For the purposes of this study, masses were included which were cystic, hyperplastic or neoplastic, but not inflammatory. Submissions of samples from the eyes, anal glands and nails were excluded. Papilloma submissions of both viral and non-viral origin were included in the current study. Also, only MCT submissions that were cutaneous have been included. Trichoepithelioma, tricholemmoma, trichofolliculoma, trichoblastoma, pilomatricoma and infundibular keratinising acanthoma have been grouped as benign follicular tumours. The study used a cross-sectional design and analysis. Following data cleaning in Excel (Microsoft Office Excel 2013, Microsoft Corp.), analyses were conducted using Stata Version 16 (Stata Corporation). Breed information recorded by the submitting practices was cleaned and mapped to a VetCompass breed list derived and extended from the VeNom Coding breed list (O’Neill et al. 2020, The VeNom Coding Group 2021). A breed variable included individual purebreds represented by ≥50 dogs in the overall study population, a grouped category of all remaining purebreds and a grouping of crossbred dogs. This approach was taken to facilitate statistical power for the individual breed analyses (Scott et al. 2012). A purebred variable categorised all dogs of recognisable breeds as “purebred” and dogs recorded as mixes of breeds as “crossbred” (The Kennel Club 2021). Crossbred dogs included all dogs that were not recorded with a standard recognised breed name (American Kennel Club 2021, The Kennel Club 2021); crossbreds included genuine “mixed-breed” mongrels as well as dogs where some breed parentage information was recorded including those that are so-called designer types such as labradoodle and cockapoo (Shouldice et al. 2019). Sex was categorised into male entire, male neutered, female entire and female neutered. Age was recorded in months up to 1 year old, and was further categorised into three groups:＜6 months, 6 to ＜9 months, 9 to 12months. Site of sample was categorised as the specific location recorded and also following grouping into general body areas. Submissions with multiple lesions of the same type in different locations were recorded as one submission in general but as separate cases in the analysis of site predilection.

我们搜索了一家大型商业诊断实验室在2006年5月31日至2013年12月3日期间从英国和欧洲的临床中收到的0至12月龄的犬提交的所有皮肤肿块的组织病理学报告。对于每个病例，提取相关犬的品种、年龄和性别、样本部位和组织病理学家作出诊断的原始报告可用数据。共有18名病理学家审查了提交的报告，少数MCT病例进行了吉姆萨或甲苯胺蓝组织化学染色，以确认肿瘤细胞中存在肥大细胞颗粒。为了本研究的目的，肿块包括囊性、增生性或肿瘤性，但不包括炎性肿块。提交的眼部、肛门腺和指甲样本被排除在外。病毒和非病毒来源的乳头状瘤都包括在当前的研究中。此外，只有皮肤MCT报告被包括在内。毛上皮瘤、毛外根鞘瘤、毛囊瘤、毛母细胞瘤、毛母质瘤和漏斗部角化棘皮瘤被归为良性毛囊肿瘤。该研究采用了横断面设计和分析。在Excel中分析数据，使用Stata Version 16进行清理。提交临床记录的品种信息被清理，并映射到VetCompass品种列表中，该列表是从VeNon编码品种列表中衍生和扩展的。品种变量包括在整个研究对象中，有50只单一品种纯种犬为一组，剩余纯种犬分为一组和杂交犬分为一组。采用这种方法是为了提高单个品种分析的统计能力。纯种变量是将所有可识别品种的犬分类为纯种组，将记录为杂交品种的犬分类为杂交组。杂交犬包括所有没有被记录识别为标准品种名的犬;杂交品种包括真正的杂交犬，以及记录了一些品种亲子信息的犬，包括那些所谓的设计类型，如拉布拉多贵宾犬和可卡贵宾犬。性别分为未去势雄性、已去势雄性、未绝育雌性和已绝育雌性。年龄在1岁以内，并进一步分为3组:＜6月龄、6到9月龄，9到12月龄。样本部位被归类为特定局部，随后也被归类为全身部位。在不同部位的同一类型的多个病变一般被记录为一个病例，但在分析部位倾向性时被记录为单独的病例。

The specific histopathological diagnosis for each skin mass was recorded. These data were further grouped to describe neoplastic status (neoplastic/non-neoplastic) and cellular origin (epithelial, melanocytic, mesenchymal, round cell). Basal cell tumours excluded trichoblastomas, which were classified as hair follicle tumours. Soft tissue sarcomas were defined as mesenchymal tumours that were otherwise unspecified. Although cases of lymphoma were retrieved from the database, they were not included in the statistical analysis as in this population of young dogs because they were sampled from the lymph node, not from the skin.

记录每个皮肤肿块的具体组织病理学诊断。这些数据进一步分组，以描述肿瘤情况(肿瘤/非肿瘤)和细胞来源(上皮细胞、黑色素细胞、间充质细胞、圆形细胞)。基底细胞瘤，排除被归为毛囊肿瘤的毛母细胞瘤。软组织肉瘤定义为其他未详细说明的间充质细胞瘤。虽然淋巴瘤病例是从数据库中检索出来的，但它们并没有在年轻犬中那样被纳入统计分析，因为它们是从淋巴结采样的而不是皮肤采样。

Risk factor analysis using multivariable binary logistic regression modelling was carried out for skin masses with at least 30 submissions (histiocytoma, papilloma, dermoid cyst, follicular cyst, MCT). Each skin mass was assessed using a standard model designed based on an “information theory” approach that included three variables that were of a priori main interest: breed or purebred, sex and age (Burnham & Anderson 2002). The histiocytoma modelling used the breed variable. However, the more limited case counts for papilloma, dermoid cyst, follicular cyst, MCT meant that the purebred variable was more appropriate numerically for modelling these. Each final model was assessed for interactions with biological significance. The Hosmer–Lemeshow test was used to evaluate the quality of the model fit (Dohoo et al. 2009, Hosmer et al. 2013). Statistical significance was set at the 5% level.

对至少30例提交的皮肤肿块(组织细胞瘤、乳头状瘤、皮样囊肿、毛囊囊肿、MCT)进行多变量二元logistic回归建模的危险因素分析。每个皮肤肿块都是用一个基于信息论方法设计的标准模型进行评估的，该模型包括三个先验的主要变量:品种或纯种、性别和年龄。组织细胞瘤模型使用品种变量。然而，乳头状瘤、皮样囊肿、毛囊囊肿、MCT的病例数较少，这意味着纯种变量在数值上更适合建模。每个最终的模型都评估了与生物学意义的相互作用。采用Hosmer Lemeshow检验评价模型拟合的质量。统计学意义设为5%水平。

RESULTS

结果

The study included 2553 dogs with a submission for a skin mass aged from 0 and including 12months. The most common breeds were crossbreed (n=340, 13.32%), Labrador retriever (263, 10.30%), Staffordshire Bull terrier (189, 7.40%), cocker spaniel (184, 7.21%) and boxer (172, 6.74%). The breakdown for sex and neuter status was: female entire (n=693, 27.14%), female neuter (262, 10.26%), male entire (1033, 40.46%), male neuter (514, 20.13%) and unrecorded (51, 2.00%). The median age was 8.00months [interquartile range (IQR) 6.00 to 10.00, range 0.00 to 12.00].

该研究包括2553只犬，并提交皮肤肿块，年龄从0到12月龄。最常见的品种为杂交犬(n=340 13.32%)、拉布拉多猎犬(n= 263 10.30%)、斯塔福斗牛㹴(n=189 7.40%)、可卡犬(n=184 7.21%)和拳师犬(n=172  6.74%)。性别和是否绝育分类为:未绝育雌性(n=693，27.14%)、已绝育雌性(n=262，10.26%)、未去势雄性(n=1033，40.46%)、已去势雄性(n=514，20.13%)和未记录(n=51，2.00%)。中位年龄为8.00个月[四分位数范围(IQR) 6.00 - 10.00，范围0.00 - 12.00]。

Within this group of 2553 dogs aged from 0 to 12months old that had a skin mass submitted for histopathology, the most common histopathological diagnoses for skin masses in this age group were histiocytoma (n=2212, 86.64%), papilloma (91, 3.56%), dermoid cyst (85, 3.33%), follicular cyst (44, 1.72%) and MCT (36, 1.41%) (Table 1). Across all the skin masses, 2408 (94.32%) were neoplastic while 145 (5.68%) were nonneoplastic in nature.

在2553只犬中从0岁到12月龄大,皮肤肿块提交组织病理学,此年龄组皮肤肿块最常见的组织病理学诊断为组织细胞瘤(n = 2212, 86.64%)、乳头状瘤(91 3.56%)、皮样囊肿(85 3.33%)、毛囊囊肿(44,1.72%)和MCT(36,1.41%)(表1)。在所有皮肤肿块中，2408例(94.32%)为肿瘤性质，145例(5.68%)为非肿瘤性质。

Of the neoplastic lesions, 2372 (98.50%) were considered benign while 36 (1.50%) were considered malignant. For the benign neoplastic lesions, 2229 (93.97%) were of round cell origin, 114 (4.81%) were epithelial origin and 29 (1.22%) were mesenchymal. For malignant neoplastic masses, 19 (52.78%) were of round cell origin, 10 (27.78% were epithelial origin, 4 (11.11%) were mesenchymal and 3 (8.33%) were melanocytic. Of the non-neoplastic lesions, 136 (93.79%) were of epithelial origin, 8 (5.52%) were derived from mesenchymal cells and 1 (0.69%) was of round cell origin.

其中良性肿瘤2372例(98.50%)，恶性肿瘤36例(1.50%)。良性肿瘤2229例(93.97%)为圆形细胞来源，114例(4.81%)为上皮细胞来源，29例(1.22%)为间充质细胞来源。恶性肿瘤中圆形细胞来源19例(52.78%)，上皮细胞来源10例(27.78%)，间充质细胞来源4例(11.11%)，黑色素细胞来源3例(8.33%)。非肿瘤性病变中，上皮细胞来源136例(93.79%)，间充质细胞来源8例(5.52%)，圆形细胞来源1例(0.69%)。

Demographic characteristics for the affected dogs appeared to vary widely across the five most common diagnoses for skin masses in these dogs. The male:female ratio showed a male bias in histiocytoma (1.72) and MCT (2.18). The limb was the most commonly affected body area for histiocytoma and MCT, the abdomen for dermoid cyst and follicular cyst and the head for papilloma. The most common breed was the Labrador retriever for papilloma and MCT, the boxer for dermoid cyst and follicular cyst and the crossbred for histiocytoma (Table 2).

患犬统计学特征似乎在这些犬的皮肤肿块的五种最常见的诊断中差异很大。雄性:雌性比值显示，雄性易患组织细胞瘤(1.72)和MCT(2.18)。组织细胞瘤和MCT最常见于四肢，皮样囊肿和毛囊囊肿多见于腹部，乳头状瘤多见于头部。患乳头状瘤和MCT最常见品种是拉布拉多犬，患皮样囊肿和毛囊囊肿最常见品种是拳师犬，患组织细胞瘤最常见品种是杂交犬(表2)。

As described in the methods, risk factor analyses were carried out for five common skin masses using a standard set of risk factors.

如方法所述，使用标准危险因素集对5个常见皮肤肿块进行危险因素分析。

Histiocytoma

组织细胞瘤

The multivariable model for histiocytoma included three variables: breed, sex and age. Among dogs that had a skin mass sample submitted to a diagnostic laboratory, golden retriever [odds ratio (OR) 0.26, 95% confidence interval (CI) 0.14 to 0.49], boxer (OR 0.38, 95% CI 0.23 to 0.62) and Labrador retriever (OR 0.52, 95% CI 0.33 to 0.83) had reduced odds of histiocytoma compared with crossbred dogs. Dogs aged 6 to ＜9months had the highest odds of histiocytoma. Neutered females had lower odds of histiocytoma than the other sex-neuter categories. The multivariable model showed an acceptable model-fit (Hosmer–Lemeshow test statistic: P=0.327) (Table 3).

组织细胞瘤的多变量模型包括三个变量:品种、性别和年龄。在提交皮肤肿块样本到诊断实验室的犬中,与杂交犬相比，金毛犬(比值比(OR)0.26,95%可信区间(CI) 0.14到0.49)、拳师犬(OR 0.38,95%可信区间0.23到0.62)、拉布拉多犬(OR 0.52,95%可信区间0.33到0.83)的组织细胞瘤比例下降。6到9月龄的犬患组织细胞瘤的几率最高。已绝育雌性患组织细胞瘤的几率比其他性别分类要低。多变量模型模型拟合可接受(Hosmer Lemeshow检验统计量:P=0.327)(表3)。

Papilloma

乳头状瘤

The multivariable models for the remaining four diagnoses included three variables: purebred status, sex and age. There was no evidence that purebred status, sex and age were substantial risk factors for papilloma among dogs that had a skin mass sample submitted to a diagnostic laboratory. The multivariable model showed an acceptable model-fit (Hosmer–Lemeshow test statistic: P=0.969) (Table 4).

其余四种诊断的多变量模型包括三个变量:纯种状态、性别和年龄。在提交皮肤肿块样本到诊断实验室的犬中，没有证据表明纯种状态、性别和年龄是犬乳头状瘤的主要危险因素。多变量模型模型拟合可接受(Hosmer Lemeshow检验统计量P=0.969)(表4)。

Dermoid cyst

皮样囊肿

There was some evidence that dogs aged 9 to 12months had higher odds of dermoid cyst compared with dogs aged under 6 months. Male neutered dogs had lower odds of dermoid cyst compared with female entire animals. There was no evidence that purebred status was associated with dermoid cyst. The multivariable model showed an acceptable model-fit (Hosmer–Lemeshow test statistic: P=0.7503) (Table 5).

有证据表明，9-12月龄犬比6月龄以下犬患皮样囊肿的几率更高。与未绝育雌性动物相比，已去势雄性犬发生皮样囊肿的几率更低。没有证据表明纯种状态与皮样囊肿有关。多变量模型的模型拟合可接受(Hosmer-Lemeshow检验统计量P=0.7503)(表5)。

Follicular cyst

毛囊囊肿

Dogs aged 9 to 12months had 5.65 times the odds (95% CI 1.33 to 23.97) of follicular cyst compared with dogs aged under 6 months. There was no evidence that purebred status or sex were substantial risk factors for follicular cyst among dogs that had a skin mass sample submitted to a diagnostic laboratory. The multivariable model showed an acceptable model-fit (Hosmer–Lemeshow test statistic: P=0.721) (Table 6).

9-12月龄犬与6个月以下犬相比，毛囊囊肿的几率为5.65倍(95% CI为1.33 - 23.97)。在提交皮肤肿块样本给诊断实验室的犬中，没有证据表明纯种状态或性别是毛囊囊肿的主要危险因素。多变量模型模型拟合可接受(Hosmer-Lemeshow检验统计量P=0.721)(表6)。

Mast cell tumour

肥大细胞瘤

Dogs aged 6 months and above showed significantly higher odds of MCT than dogs aged under 6 months. There was no evidence that purebred status or sex were substantial risk factors for MCT among dogs that had a skin mass sample submitted to a diagnostic laboratory. The multivariable model showed an acceptable model-fit (Hosmer–Lemeshow test statistic: P=0.356) (Table 7).

6月龄及6月龄以上的犬出现MCT的几率明显高于6月龄以下犬。在提交皮肤肿块样本给诊断实验室的犬中，没有证据表明纯种状态或性别是的MCT的主要风险因素。多变量模型的模型拟合可接受(Hosmer-Lemeshow检验统计量:P=0.356)(表7)。

DISCUSSION

讨论

There are several published studies reporting that cutaneous viral papillomas and histiocytomas are more commonly diagnosed in young dogs (Moriello & Rosenthal 1990,Hnilica & Patterson 2017, Meuten 2017), which correlates with the findings of the current study, with 86.64% of submissions being histiocytoma and 3.56% for papilloma being the next common. This suggests that a skin mass in a young dog is very likely to be a histiocytoma.

有几项已发表的研究报告称，皮肤病毒性乳头状瘤和组织细胞瘤更常见于幼犬，这与当前的研究结果一致，其中提交的86.64%为组织细胞瘤，第二常见的乳头状瘤为3.56%。这表明，年轻犬的皮肤肿块很可能是组织细胞瘤。

One study (Chikweto et al. 2011), which included dogs of all ages, showed that 72% of examined skin masses were neoplastic while 15.6% were non-neoplastic. In comparison, the current study illustrates an even higher proportion of neoplastic (94.32%) than non-neoplastic lesions (5.68%). However, histiocytomas and viral papillomas both tend to spontaneously regress (Gross et al. 2005).

一项包括所有年龄的犬的研究表明，72%的皮肤肿块是肿瘤，15.6%是非肿瘤。相比之下，目前的研究表明肿瘤(94.32%)比非肿瘤病变(5.68%)的比例更高。然而，组织细胞瘤和病毒性乳头状瘤都倾向于可自行消退。

Although the majority of skin masses submitted in this study were neoplastic, 98.5% of them were considered benign while only 1.5% were considered malignant. This result correlates with the findings of previous publications (Murphy 2006, Pakhrin et al. 2007) and is also in agreement with another study that specifically investigated dogs under 2years of age (Moulton 1978) and found more neoplasms were benign than malignant.

虽然在本研究中提交的大部分皮肤肿块是肿瘤，但98.5%的皮肤肿块被认为是良性的，只有1.5%的皮肤肿块被认为是恶性的。这一结果与之前发表的研究结果相一致，也与另一项专门调查2岁以下犬的研究结果一致，发现良性肿瘤多于恶性肿瘤。

In contrast, the sex distribution of the dogs with skin masses in this study was different from those previously published (Moriello & Rosenthal 1990, Goldschmidt & Shofer 1992). Whereas in those studies, more females were diagnosed with skin tumours than males in general, the most common neoplastic lesions in this current study such as histiocytoma and MCT had an increased M:F ratio (>1). This might suggest that the increase in tumour incidence in older females versus males may potentially relate to differences in hormone levels between the two genders over time.

相比之下，在这项研究中，有皮肤肿块的犬的性别分布与之前发表的不同。然而，在这些研究中，雌性通常比雄性被诊断为皮肤肿瘤更多，本研究中最常见的肿瘤病变如组织细胞瘤和MCT的M:F比值(＞1)增加。这可能表明，随着时间的推移老年雌性犬肿瘤发病率的增加，与两种性别之间激素水平的差异有关。

Histiocytomas are a common benign tumour mostly occurring in dogs under 4years old (Hnilica & Patterson 2017, Meuten 2017). This is reflected in the current study where histiocytoma was by far the most commonly diagnosed skin mass in dogs aged from 0 to 12months old diagnosed, being recorded in 86.64% of all the skin masses in the current study. No sex predilection was observed in the study of Gross et al. (2005) but the current study showed a male bias with neutered females having lower odds of histiocytoma. Moreover, while one study reported breeds at increased risk of developing histiocytomas (Goldschmidt & Shofer 1992) such as bulldog, cocker spaniel, Jack Russell terrier, West Highland white terrier and springer spaniel, the current study did not find any predisposed breeds but identified golden retriever, boxer and Labrador retriever with reduced odds of histiocytoma. The study (Goldschmidt & Shofer 1992) also reported the head was the most common anatomical location for histiocytomas, followed by the limbs. According to the results of the current study, limb (30.78%) was the most common body area to have histiocytoma.

组织细胞瘤是一种常见的良性肿瘤，多见于4岁以下的犬。这反映在当前的研究中，组织细胞瘤是目前诊断的0 - 12月龄的犬最常见的皮肤肿块，在当前研究的所有皮肤肿块中有86.64%被记录在案。Gross等人(2005)的研究中没有观察到性别倾向性，但目前的研究表明，雄性倾向于和已绝育雌性患组织细胞瘤的几率更低。此外，虽然有一项研究报告称，斗牛犬、可卡犬、杰克罗素㹴、西高地白㹴和史宾格犬等品种的组织细胞瘤风险较高，但目前的研究没有发现任何易感品种，但发现金毛犬、拳师犬和拉布拉多犬的组织细胞瘤风险较低。该研究还报告了组织细胞瘤最常见的解剖位置是头部，其次是四肢。根据目前的研究结果，四肢(30.78%)是组织细胞瘤最常见的发病部位。

Papilloma is another skin tumour to which young dogs are known to be particularly predisposed (Meuten 2017), but with no consistency in breeds considered to be at a higher risk (Goldschmidt & Shofer 1992, Gross et al. 2005, Meuten 2017). The current study concurs with these findings that, while such tumours may commonly occur in young dogs, it failed to analyse its breed predisposition. Cutaneous papillomas are known to most frequently arise on the head and the limbs (Goldschmidt & Shofer 1992), which agrees with the result from the current study with papillomas in young dogs being most commonly found on the head (51.65%). Viral papillomas are benign neoplastic masses whereas squamous papillomas are non-neoplastic papillated masses (Meuten 2017). Squamous papillomas lack viral infection and are relatively less common and smaller than viral papillomas (Gross et al. 2005, Meuten 2017).

乳头状瘤是另一种已知的年轻犬易患的皮肤肿瘤，但没有一致的高风险品种倾向性。目前的研究与这些发现一致，即尽管这种肿瘤通常发生在年轻犬上，但它未能分析其品种的易感性。皮肤乳头状瘤最常见于头部和四肢，这与目前对年轻犬乳头状瘤最常见于头部的研究结果一致(51.65%)。病毒性乳头状瘤是良性肿瘤，而鳞状乳头状瘤是非肿瘤性乳头状肿块。鳞状乳头状瘤不受病毒感染，与病毒性乳头状瘤相比，相对少见且体积较小。

Dermoid cysts are an uncommon, non-neoplastic skin mass which, as a congenital anomaly, mostly occur in young dogs under 2 years of age (Gross et al. 2005, Meuten et al. 2017). The current study also found that dermoid cyst is the third most common skin mass among young dogs, with higher odds in dogs aged 9 to 12months old. Rhodesian Ridgebacks are reported to be predisposed due to having a simple recessive gene (Gross et al. 2005, Maxie 2016, Meuten 2017), and boxers are another reported predisposed breed (Gross et al. 2005). However, the current study could not find predisposed breeds for developing dermoid cysts in young dogs. Also, previous studies have reported that dermoid cysts most often occur in the dorsal midline (Gross et al. 2005, Meuten 2017), but the current showed that the skin of the abdomen was the most common site.

皮样囊肿是一种罕见的非肿瘤性皮肤肿块，是一种先天性异常，多发生在2岁以下的年轻犬犬。目前的研究还发现，皮样囊肿是年轻犬中第三常见的皮肤肿块，在9至12月龄犬中发病率更高。据报道，罗得西亚脊背犬因具有一个简单的隐性基因而易患病，而拳师犬是另一个报道的易患病品种。然而，目前的研究没有发现容易在年轻犬中发展皮样囊肿的品种。此外，以前的研究报告皮样囊肿最常发生在背侧中线，但目前的研究表明腹部皮肤是最常见的部位。

Three and a half percent of tumour-like lesions arising in the skin are follicular cysts (Gross et al. 2005). They are reported to be most frequent in middle-aged dogs (Hnilica & Patterson 2017). It is also the fourth most common skin mass (1.72%) to be found in young dogs from the current study. The odds of follicular cyst in dogs aged 9 to 12months were 5.66 times higher than those aged under 6 months, suggesting an increased frequency with age during the first year of life. Shih-tzu, Miniature schnauzer and boxer are the breeds previously reported to be at higher risk in several studies (Gross et al. 2005, Hnilica & Patterson 2017, Meuten 2017). On the other hand, the current study was not able to reveal breeds at risk of developing follicular cyst. The finding that the skin of the abdomen is the most common site for follicular cyst development in the current study is also in disagreement with previous studies (Gross et al. 2005, Hnilica & Patterson 2017), where the head was reported to be the predisposed site.

3.5%的皮肤肿瘤样病变是毛囊性囊肿。据报道，它们在中年犬中最常见。这也是目前研究中发现的年轻犬第四常见的皮肤肿块(1.72%)。9-12月龄犬的毛囊囊肿发生率是6月龄以下犬的5.66倍，表明在出生后1年内随年龄增长而增加。在之前的几项研究中，西施犬、迷你雪纳瑞犬和拳师犬被报道为高风险品种。另一方面，目前的研究未能揭示出有发生毛囊囊肿风险的品种。目前的研究发现，腹部皮肤是毛囊囊肿最常见的发病部位，这与之前的研究也不一致，此前的研究报告称头部是毛囊囊肿的易感部位。

MCTs are reported to be the most common skin tumour in dogs in general (Hnilica & Patterson 2017), however these tumours accounted for only 1.41% of submissions from the very young dogs in this study. While these findings are consistent with MCTs arising much more frequently in older animals (Hnilica & Patterson 2017), it highlights the potential for MCT to also occur in very young animals such as a 2-month-old dog in this study. Occurrence of MCT in young dogs concurs with a previously published case of MCT developing in a 4-week-old male boxer dog (Mahler 2012), and previous studies by Goldschmidt & Shofer (1992) and Gross et al. (2005) had cases diagnosed at 6 months or 4 months of age, respectively. The present study also showed that there are significantly higher odds of developing MCT in dogs that are aged 6 months and above compared with those aged under 6 months. Hence, these findings emphasise that diagnosis of MCT should not be ruled out even in very young dogs.

据报道，MCT通常是犬上最常见的皮肤肿瘤，但在本研究中，这些肿瘤仅占年轻犬提交的1.41%。虽然这些发现与MCT在年龄较大的动物中出现的频率更高相一致，但在这项研究中，它强调了MCT在非常年幼的动物中也可能出现，如2月龄的犬。幼犬MCT的发生与之前发表的4周龄的雄性拳师犬MCT的发生一致，Goldschmidt & Shofer(1992)和Gross等人(2005)在之前的研究中分别在6月龄或4月龄时诊断出此病例。目前的研究还表明，与6月龄以下的犬相比，6月龄以上的犬患MCT的几率显著更高。因此，这些发现强调，即使在非常年轻的犬中，MCT的诊断也不应被排除。

The current study was underpowered to show any breed predisposition for MCT, unlike those identified in older dogs in previous studies (Goldschmidt & Shofer 1992, Gross et al. 2005, Hnilica & Patterson 2017, Meuten 2017). In one study (Goldschmidt & Shofer 1992), the site of the highest incidence was the limb, which correlates with the findings of the present study, and therefore it does not appear that age influences the most likely site of MCT development.

目前的研究不足以证明任何品种的犬都有MCT的倾向，不像以前的研究中发现的那些年龄较大的犬。在一项研究中，发病率最高的部位是四肢，这与本研究的发现一致，因此年龄似乎不会影响MCT最可能发生的部位。

Despite the large number of cases available for this retrospective study, there are several limitations. Data were obtained only from submissions where the age of the animal was recorded as “months” as opposed to “years” to facilitate the searching of the database, and therefore it is possible that data from dogs with their age recorded as “1 year” rather than “12 months” were omitted. Secondly, the data were not retrieved directly from first opinion practice but via a diagnostic laboratory; while this approach has the advantage of highly precise lesion identification it potentially underestimates the number of lesions that are commonly diagnosed on clinical presentation but without laboratory confirmation, especially where those lesions are common and clinically characteristic, such as histiocytoma and papilloma, and therefore might not be biopsied. Thirdly, interobserver variations between the 18 pathologists that were involved in diagnoses need to be considered, which could have affected the diagnoses of the skin mass submissions. Breed popularity is another factor that changes over time, and which could impact on the findings of apparent breed predispositions for certain lesions, particularly since the dataset utilised in this study is from a previous time period.

尽管这项回顾性研究有大量的病例，但仍存在一些局限性。数据仅来自于将犬的年龄记录为月份而不是年份，以方便检索数据库，因此，有可能从犬的年龄记录为1岁而不是12月龄的数据被省略。其次，数据不是直接从第一临床医院中获得的，而是通过诊断实验室获得的;虽然这种方法具有高度精确的病变识别的优势，但它可能低估了通常根据临床表现而无需实验室确认的病变数量，特别是那些常见的和具有临床特征的病变，如组织细胞瘤和乳头状瘤，因此可能不会做活组织检查。第三，需要考虑参与诊断的18名病理学家之间的观察者间差异，这可能会影响皮肤肿块提交的诊断。品种倾向性是另一个随时间变化的因素，它可能会影响某些病变的明显品种易感性的发现，特别是因为本研究使用的数据集来自以前的时期。

As this was a retrospective study, with data collected from a broad spread of different clinics across several countries, details of each submission were not uniform or complete. For example, the site of a lesion is not always specific or consistent, and it was not possible to clarify this with the original submitting practice. Some submission forms also lacked some patient or valuable lesion details such as signalment, sampling site, mitotic count and histological grade for MCTs, which therefore could not be included in statistical analysis. This study was also restricted to lesions arising in the skin and soft tissues, and a potential area for further investigation would be the incidence of lesions affecting other body systems in young dogs, for a more complete picture.

由于这是一项回顾性研究，数据来自几个国家广泛分布的不同诊所，每一份报告的细节都不统一或不完整。例如，病变部位并不总是特定的或一致的，并且不可能在最初提交的临床中澄清这一点。一些提交的表格还缺少一些病患或有价值的病变细节，如症状、采样部位、有丝分裂计数和MCT的组织学分级，因此无法纳入统计分析。本研究还局限于皮肤和软组织的病变，进一步研究的潜在领域是影响幼犬其他机体系统的病变发生率，以获得更完整的图像。

In conclusion, the most common skin masses in dogs aged between 0 months and 12months old were histiocytoma, papilloma, dermoid cyst, follicular cyst and MCT. The general characteristics of these lesions found in previous studies, such as the most commonly affected site and the predisposed breeds, were not completely replicated in the young dogs in this study. Although most lesions typically appear from 6 to 14years of age (Moulton 1978), this study has shown that certain tumours can develop even at just a few months of age. It also highlights that a high proportion of skin masses in young dogs are benign neoplasms.

由此可见，0-12月龄犬皮肤肿块以组织细胞瘤、乳头状瘤、皮样囊肿、毛囊囊肿和MCT最为常见。在之前的研究中发现的这些病变的一般特征，如最常见的感染部位和易感品种，在本研究中没有在年轻犬中完全复制。虽然大多数肿瘤通常出现在6到14岁之间，但这项研究表明，某些肿瘤甚至可以在月龄的时候出现。本文还强调，在年轻犬皮肤肿块中，良性肿瘤比例高。

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