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Canine nodular dermatophytosis (kerion): 23 cases 犬结节性癣菌病（脓癣）：23例 翻译：郭润霞 Abstract 摘要 Dermatophytosis is a common zoonotic disease, and one of its clinical presentations in the dog is nodular dermatophytosis (kerion). Because the infection is located within the dermis, routine diagnostic tests such as a Wood’s lamp examination, microscopic examination of hair shafts for fungal elements and fungal culture can yield negative results. In such cases,histopathological examination with routine and special stains (periodic acid-Schiff, Gomori methenamine silver) is required to confirm the diagnosis. Nodular dermatophytosis in 23 dogs of different breed, age and sex with single or multiple nodules is described. Twelve dogs had a single nodule, and 11 dogs showed multiple lesions. Wood’s lamp examination was negative in all cases. Microscopic examination of plucked hairs showed arthrospores in 8 of 23 cases. Skin scrapings in mineral oil looking for arthrospores and/or hyphae were positive in 12 cases. Impression smears of exudates were diagnostic in 21 of 23 cases (91%), showing arthrospores within fragments of hair shafts or free among neutrophils and macrophages (pyogranulomatous inflammation). Histopathology was performed in two cases. Fungal culture was positive for Microsporum canis in 16 dogs and for Microsporum gypseum in one dog. In six cases, the causative agent was not identified by fungal culture. All dogs were treated with systemic antifungal therapy and in eight cases with concurrent antibiotic therapy. Nodular dermatophytosis resolved in all dogs with the prescribed treatments within 4 to 8 weeks. Transmission to people or other pets in the home was not found. 皮肤癣菌病是一种常见的人畜共患传染病，该病在犬的临床表现之一是结节性皮肤癣菌病(脓癣)。由于感染位于真皮内，常规诊断试验如伍德氏灯检查、毛干真菌元素显微镜检查和真菌培养常得到阴性结果。在这种情况下，需要常规和特殊染色（过碘酸-雪夫、六胺银染色）的组织病理学检查来确诊。本文描述了23只不同品种、年龄和性别的单结节或多结节犬的结节性皮肤癣菌病。12只犬为单个结节，11只犬表现为多病灶。所有病例伍德氏灯检查均为阴性。拔毛镜检23例中8例可见节孢子。12只犬进行皮肤刮片后，滴入矿物油可找到节孢子和（或）菌丝。23例中21例(91%)渗出液压片有诊断意义，显示毛干碎片内有节孢子或中性粒细胞和巨噬细胞间游离的节孢子（脓性肉芽肿性炎症）。2只犬进行组织病理学检查。16只犬真菌培养为犬小孢子菌和1只犬真菌培养为石膏样小孢子菌。6例真菌培养未明确病原体。所有犬均接受全身抗真菌治疗，8例同时接受抗生素治疗。接受处方治疗的所有犬的结节性皮肤真菌病均在4-8周内消退。未发现传播给家中的人或其他宠物。
Introduction 引言 Dermatophytosis is a cutaneous infection caused by three genera of keratinophilic fungi: Microsporum spp., Trichophyton spp. and Epidermophyton spp. Dermatophytes affect the hair shafts, stratum corneum and nails or claws of animals and human beings, with variable clinical features.Nodular dermatophytosis, also known as a ‘kerion’, is a well-known clinical presentation of canine dermatophytosis. It is clinically characterized by single or less commonly multiple erythematous, alopecic, dome-shaped, exudative nodules, and histopathologically by granuloma or pyogranuloma formation with fragments of hair shafts containing fungal spores.Diagnosis can be difficult, and histopathological examination of biopsy samples is often required because fungal culture can yield negative results.Nodular dermatophytosis in dogs is reported to be most commonly caused by Microsporum gypseum, followed by Trichophyton mentagrophytes and Microsporum canis.A similar presentation is also observed in human beings, where it is more often caused by zoophilic or geophilic fungal species.Nodular dermatophytosis (kerion) appears to be rare in cats.Despite the well-recognized clinical and histological features of canine nodular dermatophytosis and its relatively common occurrence, there are very few published studies available in the literature,excluding single case reports. The purpose of this paper is to present the clinical, diagnostic and therapeutic findings in 23 cases of canine nodular dermatophytosis. 皮肤癣菌病是由小孢子菌属、毛癣菌属和表皮癣菌属3个属的嗜角质真菌引起的皮肤感染。皮肤癣菌影响动物和人的毛干、角质层和指（趾）甲或爪，临床特征各不相同。结节性皮肤癣菌病又称‘脓癣’，是众所周知的犬皮肤癣菌病的临床表现形式。其临床特征为单个或较少见的多发性红斑、脱毛、圆顶状、渗出性结节，组织病理学表现为肉芽肿或脓性肉芽肿，毛干碎片中含有真菌孢子。诊断可能很困难，由于真菌培养常产生阴性结果，常需对活检标本进行组织病理学检查。据报道，犬结节性皮肤癣菌病最常由石膏样小孢子菌引起，其次是须毛癣菌和犬小孢子菌。在人类中也观察到类似的表现，更常由嗜动物性或嗜土壤性真菌引起。结节性皮肤癣菌病（脓癣）似乎在猫中罕见。尽管犬结节性皮肤癣菌病具有公认的临床和组织学特征，且其发生相对常见，但文献中相关研究非常少，仅有一些单个病例报告。本文旨在介绍23例犬结节性皮肤癣菌病的临床、诊断和治疗结果。
Materials and methods 材料和方法 Twenty-three dogs of different age, breed and sex presented for single or multiple cutaneous nodules were included. A full history was taken, and a complete general and dermatological examination was performed in all cases. 所选的23个病例患犬因单个或多个皮肤结节就诊，它们不同年龄、品种和性别并采集完整病史，所有病例均进行完整的全身和皮肤科检查。
In each case, the following diagnostic tests were performed: Wood’s lamp examination, direct examination of hair shafts from hair pluckings and deep skin scrapings, cytological examination of the exudate from the nodules and a dermatophyte fungal culture. Briefly, Wood’s lamp examination was performed in a dark room, with a 253.7 nm ultraviolet lamp after warming it for approximately 5 min. The nodular lesion or lesions and the dogs’ haircoat were carefully examined for fluorescence typically associated with M. canis. Hairs from the periphery of the nodule or nodules were plucked with forceps and placed on a glass slide with mineral oil. The surface of the nodule/s was scraped with a blunted scalped blade, and the material was transferred onto another glass slide with mineral oil. Both preparations were covered with a glass coverslip and examined under the microscope at 4×, 10× and 40× magnifications for parasites and/or arthrospores within hair shafts. Cytology was carried out by gently expressing the exudate and transferring the material obtained to a glass slide by means of an impression smear. The slides were air dried and stained with a modified Wright’s stain (Hemacolor®, Merck KGaA, Darmstadt, Germany). Slides were examined at 10×, 40× and 100× under oil immersion to identify inflammatory cells, free arthrospores, fragments ofhair shafts containing arthrospores and bacteria. Fungal culture was performed using a commercial medium containing DTM (dermatophyte test medium) and Sabouraud’s agar (Dermatophyte Selective Media®, Biolife Italiana, Milano, Italy). 在每个病例中，进行以下诊断试验：伍德氏灯检查、直接拔毛检查毛干，深部皮肤刮片，结节渗出液的细胞学检查和皮肤真菌培养。简言之，在暗室中进行伍德氏灯灯检查，加热约5 min后用253.7 nm紫外线灯进行。仔细检查犬被毛中单个或多个结节性病变，是否与犬小孢子菌有相关的荧光。用镊子拔出结节或结节周边的毛发，置于含矿物油的载玻片上。用钝化的刀片刮除结节表面，用矿物油将材料转移到另一个载玻片上。用玻璃盖玻片覆盖两种制备物，并在显微镜下以4×、10×和40×放大倍数检查毛干内的寄生虫和/或节孢子。通过轻轻挤压渗液并通过压片将所得材料转移至载玻片上进行细胞学检查。风干载玻片，并用改良的瑞士染色剂染色。在油浸下以10×、40×和100×检查切片，以鉴定炎性细胞、游离节孢子、含有节孢子和细菌的毛干碎片。使用含DTM（皮肤癣菌培养基）和沙氏琼脂（皮肤癣菌选择性培养基的市售培养基进行真菌培养。
When all the previously described diagnostic tests were negative, 6-mm punch biopsy samples were taken for histopathological examination. Samples were fixed in 10% neutral buffered formalin, embedded in paraffin and sections of about 5 μm were stained with haematoxylin and eosin (H&E) and periodic acid Schiff. After the diagnosis, all dogs were treated with systemic antifungal drugs until resolution of clinical lesions and negative fungal culture. Antibiotics were also prescribed where indicated by the results of cytological examination. 当上述所有诊断试验均为阴性时，使用6 mm打孔器采集活检标本进行组织病理学检查。将样本固定在10%中性缓冲福尔马林中，包埋在石蜡中，并用苏木精和伊红(H&E)以及高碘酸雪夫对约5 μm切片进行染色。确诊后，所有犬均给予全身抗真菌药物治疗，直至临床病变消退，真菌培养阴性。根据细胞学检查可能还需要使用抗生素。
Results 结果 The signalment (age, breed and sex) of the dogs is summarized in Table 1. There were eight mixed-breed dogs (34%), with the remaining dogs representing 12 different breeds. At the time of presentation, the dogs varied in age from 3 months to 10 years (mean: 4 years and 8 months, median: 6 years), with six dogs (26%) younger than 12 months. There were 10 intact/spayed female dogs (44%) and 13 intact male dogs (56%). Twelve dogs (52%) presented with one nodular lesion, seven dogs (30%) with two lesions and four dogs (18%) showed more than two nodules. Affected sites are listed in Table 1. The most commo affected sites were the head and/or neck (ten dogs, 44%) and the front or hind limbs (eight dogs, 34%). The nodules were raised, alopecic and erythematous with crusts on the surface or, in some cases, purulent exudate exuding from the lesions (Figures 1 and 2). 犬的信息（年龄、品种和性别）汇总见表1。有8只混血犬(34%)，其余犬代表12个不同品种。就诊时，犬的年龄从3个月到10岁不等（平均：4岁8个月，中位数：6岁），其中6只犬(26%)的年龄小于12个月。有10只未绝育/已绝育的雌性犬(44%)和13只未去势的雄性犬(56%)。12只犬(52%)表现为单个结节病灶，7只犬(30%)表现为2个病灶和4只犬(18%)表现为2个以上结节。患病部位见表1。最常见的患病部位为头部和/或颈部（10只犬，44%）以及前肢或后肢（8只犬，34%）。结节隆起，脱毛及红斑，表面有结痂，部分病例病变有脓性渗出物渗出（图1、2）。
Figure 1. Case no. 10. Alopecic nodule on the dorsal nose. 图1.编号10.鼻背侧脱毛性结节
Results of the diagnostic tests are summarized in Table 2. Wood’s lamp examination was negative in all cases. Microscopic examination in mineral oil of hair pluckings and skin scrapings were positive for arthrospores and/or fragments of hair shafts with cuffs of arthrospores and/or hyphae in 8 (34%) and 12 (52%) dogs, respectively. Cytological examination showed free arthrospores or arthrospores within fragmented hair shafts in 21 of 23 cases (91%). Free fungal elements and infected hair shafts were seen among neutrophils and macrophages (pyogranulomatous inflammation). Bacteria (cocci) within degenerate neutrophils were present in eight cases (34%). Fungal culture was positive in 17 cases (74%): M. canis was isolated in 16 dogs and M. gypseum in one dog. In six cases, fungal culture was negative, and history revealed that four of these dogs had been treated topically with chlorhexidine 0.5% (Clorexyderm®, ICF Vet, ICF, Palazzo Pignano, Italy) or povidone iodine 10% (Betadine®, Viatris SPA, Milano, Italy) before the consultation (Table 3). In two cases (dog numbers 21 and 22) all the previously described diagnostic tests yielded negative results, and the diagnosis was confirmed by histopathological examination. There was pyogranulomatous folliculitis and furunculosis, with fragments of hair shafts invaded by fungal arthrospores and hyphae (Figure 3), clearly visible on H&E stain. 诊断试验结果汇总见表2。所有病例的伍德氏灯检查均为阴性。8只(34%)和12只(52%)犬拔毛和皮肤刮片矿物油镜检节孢子阳性和（或）节孢子周围和（或）菌丝阳性。细胞学检查23例中21例(91%)断裂毛干检测到有节孢子或断裂毛干内有节孢子。在中性粒细胞和巨噬细胞中观察到游离的真菌元素和感染的毛干（脓性肉芽肿性炎症）。8例病例(34%)存在退行性中性粒细胞内的细菌（球菌）。真菌培养阳性病例17例(74%)：16只犬分离出犬小孢子菌，1只犬分离出石膏样小孢子菌。6例病例真菌培养为阴性，病史显示其中4只犬在会诊前接受了0.5%氯己定或10%聚维酮碘外部治疗（表3）。这两个病例（犬编号21和22），所有先前描述的诊断试验均为阴性结果，并通过组织病理学检查证实了脓癣的诊断。有脓性肉芽肿性毛囊炎和疖病，毛干碎片被真菌节孢子和菌丝侵入（图3），H&E染色清晰可见。
Figure 2. Case no. 2. Alopecic, erythematous and exudative plaque on the neck. 图2.编号2.脱毛、红斑和渗出性斑块 Figure 3. Skin, Case no. 22. Pyogranuloma with fragments of hair shafts containing fungal spores and hyphae (black arrowheads). H&E stain, ×4, Bar: 100 micrometers. 图3。皮肤,编号22. 脓性肉芽肿中含有真菌孢子和菌丝(黑色箭头)的毛干碎片。H&E染色，×4, Bar: 100微米。
Dogs were treated with itraconazole (Sporanox®, Janssen Cilag spa, Cologno Monzese, Italy) 10 mg/kg orally once daily consecutively (3 dogs) or on alternate weeks (14 dogs) or with ketoconazole (Nizoral®, Janssen Cilag spa, Cologno Monzese, Italy) at 10 mg/kg orally once daily (6 dogs) until complete resolution, confirmed by negative fungal culture (Table 3). Eight dogs had secondary bacterial infection, based on the results of cytological examination. Antibiotic therapy with cefalexin (ICF Vet®, ICF, Palazzo Pignano,Italy) 25 mg/kg orally twice daily or cefadroxil (Cefa-Cureabs®, Intervet Italia, Peschiera Borromeo, Italy) 25 mg/kg orally once daily was given concurrently to the systemic antifungal treatment for 4 weeks. In all cases, complete clinical resolution of the nodular lesions confirmed by a negative fungal culture was observed in 4 to 8 weeks. None of the dogs relapsed after treatment discontinuation. Transmission of dermatophytosis to in-contact pets or owners was not observed, either before the diagnosis or during treatment, and topical antifungal therapy to prevent infection of in-contact pets was not prescribed. 犬接受伊曲康唑10 mg/kg每日一次连续口服（3只犬）或隔周口服（14只犬），或接受酮康唑10 mg/kg每日一次口服（6只犬），直至完全消退，并通过真菌培养证实阴性（表3）。8只犬继发细菌感染，根据细胞学检查结果。在全身性抗真菌治疗的同时给予头孢氨苄25 mg/kg口服每日两次或头孢羟氨苄25 mg/kg口服每日一次抗生素治疗4周。所有病例的结节病灶均在4～8周临床完全消退并且通过真菌培养证实阴性。治疗中止后，所有犬均未复发。在诊断前或治疗期间均未观察到皮肤癣菌病传播给接触的其他宠物或主人，未规定使用局部抗真菌治疗对所接触宠物进行感染的预防。
Discussion 讨论 In this paper, we describe the clinical, diagnostic and therapeutic features of 23 cases of canine nodular dermatophytosis. This disease is reported to be most commonly caused by M. gypseum, followed by T. mentagrophytes and less frequently by M. canis in textbooks。In the present study, M. canis was the most common isolate (16 dogs), and M. gypseum was found in one dog. Fungal culture did not identify the aetiological agent in six cases; in these cases the diagnosis was confirmed by cytological examination of impression smears that showed definitive evidence of dermatophyte infection. The same results were reported in a recent paper, published in Italy, and in a congress presentation by Greek authors.6,7 It is therefore very likely that, at least in Mediterranean countries, M. canis is the most common cause of nodular dermatophytosis in dogs. 本文描述了23例犬结节性皮肤癣菌病的临床、诊断和治疗特点。据报道，本病最常由石膏样小孢子菌引起，其次为须毛癣菌，犬小孢子菌较少引起。在本研究中，犬小孢子菌是最常见的分离株（16只犬），在1只犬中发现石膏样小孢子菌。6例病例的真菌培养未确定病原体；在这些病例中，通过压片细胞学检查证实了脓癣的诊断，压片显示了皮肤癣菌感染的明确证据。最近在意大利发表的一篇论文和希腊作者在大会上的演讲中也报道了同样的结果。因此，至少在地中海国家，犬小孢子菌很可能是犬结节性皮肤癣菌病的最常见原因。
Most of the affected dogs (34%) were mixed-breed dogs, with the remaining cases being dogs of 12 different breeds, and male and female dogs were equally represented, so we can not draw any conclusion on breed or sex predisposition. Dermatophytosis is reported to be more common in dogs less than 1 year of age,and in one study nodular dermatophytosis was described in more than 50% of the cases in dogs of the same age.In this study, it was diagnosed in dogs of any age (3 months to 10 years), with only 26% of the dogs being younger than 12 months. A possible explanation of this finding may be resulting from the fact that M. canis infection can be acquired from different sources, such as carrier cats, fomites and the environment.Unfortunately, it was not possible to identify the source of the infection in these dogs. Another explanation relies on the pathogenesis of nodular dermatophytosis. This peculiar clinical presentation is thought to be the result of an enhanced host immune response or to a hypersensitivity reaction to the fungus associated with bacterial complication.These immune responses are more likely to occur in adult dogs with a fully developed immune system. In humans, nodular dermatophytosis occurs in children and adults and the main factor leading to kerion formation is thought to be lack of host adaptation to the zoophilic or geophilic fungi and/or a hypersensitivity reaction. 大部分患病犬(34%)为混血犬，其余病例为12个不同品种的犬，雄性和雌性犬数量相当，因此我们无法得出关于品种或性别倾向的任何结论。据报道，皮肤癣菌病在1岁以下的犬中更常见，在一项研究中，在超过50%的同龄犬病例中描述了结节性皮肤癣菌病。在本研究中，在任何年龄（3个月至10岁）的犬中均有确诊该病对病例，仅26%的犬年龄小于12个月。对这一发现的可能解释是由于犬小孢子菌感染可从不同来源获得，如带菌猫、污染物和环境。不幸的是，无法确定这些犬的感染源。另一种解释依赖于结节性皮肤癣菌病的发病机制。这种特殊的临床表现被认为是宿主免疫应答增强或对与细菌并发症相关的真菌引起超敏反应的结果。这些免疫应答更可能发生在免疫系统发育完全的成年犬中。在人类中，结节性皮肤癣菌病发生在儿童和成人中，导致脓癣形成的主要因素被认为是宿主对嗜动物性或嗜土壤性真菌缺乏适应和/或超敏反应。
Most cases of nodular dermatophytosis present as single nodules on the face or distal limb.In this study, 48% of the dogs showed two or more nodules, and the most common locations were the head, neck and limbs. A similar prevalence of multiple lesions was also observed by Koutinas et al. whereas in the Italian study only 29% of cases showed multiple nodules. 大多数结节性皮肤癣菌病表现为面部或肢体远端的单发结节。在本研究中，48%的犬显示两个或多个结节，最常见的位置是头部、颈部和四肢。Koutinas等也观察到类似的多发病灶患病率。而在意大利的研究中，只有29%的病例显示多发性结节。
The diagnosis of nodular dermatophytosis may be difficult, given the dermal location of the infection. The diagnostic tests routinely used for fungal infections, such as Wood’s lamp examination, microscopic examination of hairs and fungal culture can be negative, requiring histopathological examination of biopsy samples to confirm the diagnosis. In this study, we found that cytological examination of the exudate expressed from the lesion was the most useful diagnostic test for nodular dermatophytosis, being positive for fungal arthrospores in 91% of the cases. It confirmed the diagnosis in 21 of 23 cases, the remaining two cases requiring diagnosis with histopathology. Positive findings of arthrospores in cytological specimens were reported by Albanese and Caruso (38%) and again in one single case report.6,12 Cytology also has the advantage to be diagnostic for secondary bacterial infections, allowing the clinician to institute antibiotic therapy where needed. We can therefore add cytology to the list of diagnostic tests for fungal infections, when they present clinically with exudative nodular lesions. In this study, histopathological examination was required to make a definitive diagnosis in two cases only (dog numbers 21 and 22). 考虑到脓癣感染位置为真皮层，结节性皮肤癣菌病的诊断可能很困难。常规用于真菌感染的诊断试验，如伍德氏灯检查、毛发镜检及真菌培养均可为阴性，需通过组织病理学检查确诊。本研究发现病变的渗出液细胞学检查是结节性皮肤癣菌病最有用的诊断方法，91%的病例节孢子阳性。23例中21例可确诊，其余2例需组织病理学诊断。Albanese和Caruso(38%)报告了细胞学样本中节孢子的阳性结果，并在一份单个病例报告中再次报告。细胞学还具有诊断继发性细菌感染的优势，指导临床医生在需要时进行抗生素治疗。因此，当临床上表现为渗出性结节性病变时，我们可以将细胞学检查添加到真菌感染的诊断试验列表中。在本研究中，仅有两个病例需通过组织病理学检查来做出明确诊断（犬编号21和22）。
In nodular dermatophytosis, the severity of the inflammatory reaction is believed to contribute to spontaneous resolution of the disease, which is commonly observed, and some authors state that treatment is not necessary.All the dogs in this study were treated with systemic antifungal agents, and the disease resolved within 4 to 8 weeks.It is possible that our cases resolved spontaneously, but we felt that we could not leave a potentially zoonotic disease untreated. None of the dogs relapsed or transmitted the infection to the owners. A study regarding environmental contamination with M. canis showed that dogs are less important sources of infection compared to cats. Another study showed that 36% of dogs belonging to owners with dermatophytosis (tinea corporis) were culture positive, compared to 53% of cats. In nodular dermatophytosis, the fungal agent is located in the dermis, within hair shafts embedded in a pyogranulomatous reaction; this peculiar location may explain why, in this study, the disease was not contagious to owners. 在结节性皮肤癣菌病中，常观察到，严重的炎症反应有助于疾病的自发消退，一些作者指出治疗是不必要的。本研究中的所有犬均接受了全身性抗真菌剂治疗，疾病在4-8周内消退。我们的病例有可能自发消退，但我们认为我们不能不去治疗有潜在人畜共患风险的传染病。所有犬均未复发或将感染传播给犬主人。一项关于犬小孢子菌环境污染的研究表明，与猫相比，犬是不太重要的传染源。另一项研究表明，主人患有皮肤癣菌病(体癣)的犬中，36%的犬在培养中呈阳性，而猫的这一比例为53%。在结节性皮肤癣菌病中，真菌元素位于真皮内，毛干嵌入于脓性肉芽肿反应中；这种特殊的位置可以解释为什么，在本研究中，疾病不会对主人传染。
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发表于 2022-6-27 22:27:29
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