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    Characteristics of Cutaneous and Subcutaneous Infectious Granuloma at a Signal Center in China:A Five-Year Retrospective Study

    2019-08-06 13:05:30ZhenZhenYanYouMingMeiHaiQingJiangYongNianShenPanGenCuiWeiDaLiuMeiHuaFuHongShengWangJianFangSun
    國際皮膚性病學(xué)雜志 2019年2期

    Zhen-Zhen Yan, You-Ming Mei, Hai-Qing Jiang, Yong-Nian Shen, Pan-Gen Cui, Wei-Da Liu,,?,Mei-Hua Fu,?, Hong-Sheng Wang, Jian-Fang Sun,

    1Department of Pathology, 2Jiangsu Key Laboratory of Molecular Biology for Skin Diseases and STIs, 3Department of Mycology,4Department of Dermatology, Hospital for Skin Diseases (Institute of Dermatology), Chinese Academy of Medical Sciences and Peking Union Medical College, Nanjing, Jiangsu 210042, China.

    Abstract Objective:Cutaneous and subcutaneous infectious granuloma(CSIG)is a broad group of inflammatory conditions that share important similarities in granulomatous reaction pattern and nonspecific clinical presentation. Here, we conducted the retrospective study to identify the clinical,pathological,and epidemiological correlations of CSIG cases at a signal center in China.Methods: Data of patients diagnosed with CSIG between January 1, 2011 and December 31, 2015 were retrospectively collected,including socio-demographic information,pathogen diagnosis,clinical features,pathological results, treatment, and prognosis.Results:This study included 256 patients(137 males and 119 females)with a mean age of 52 years.Infections were more common in those aged over 40 years old(76.17%).The most common pathogens were Mycobacterium leprae(26.56%), Sporothrix schenckii (23.83%), and Mycobacterium tuberculosis (15.63%). Mycobacterium marinum(8.98%)accounted for 51.11%of nontuberculous mycobacterial contagion.Lesions were most common in the distal extremities(32.03%).The predominant clinical forms were plaques(61/142,42.96%)and nodules(41/142,28.87%).Conclusions:Various pathogens were responsible for the CSIG cases in this study,with M.leprae being the most common.CSIG should be considered as a likely diagnosis for patients with lesions on exposed parts of the body that present as plaques or nodules and has a history of trauma.

    Keywords: infectious skin diseases, granuloma, mycobacterium, fungus, retrospective study

    Introduction

    Cutaneous and subcutaneous infectious granuloma(CSIG) is a broad group of inflammatory conditions involving the skin and soft tissues. These diseases share important similarities in their granulomatous reaction patterns. The major sources of CSIG include a diverse group of fungi and mycobacteria. Many species have been shown to cause infectious granulomatous diseases,but there is great variability in their geographical distribution. Recent studies suggest that there has been an increase in the detection of mycobacterial and fungal isolates and an emergence of new strains worldwide, a trend that might be attributed to several factors,including improved detection technology, population aging, the extensive use of antibiotics and immunosuppressants, and a surge of HIV infection.1Because of its nonspecific clinical presentation and similar histopathology on tissue biopsy along with a lack of rapid and sensitive detection methods for CSIG, its diagnosis is often challenging. Mistaken or uncertain diagnoses can lead to inappropriate treatment and drug resistance. It is therefore important to recognize the clinical, pathological, microorganism, and epidemiological correlations of skin and soft tissue granulomatous diseases in local regions. However, the prevalence and the characteristics of CSIG are poorly documented.

    Here, we conducted a retrospective analysis of the patients diagnosed with CSIG at the Hospital for Skin Diseases (Institute of Dermatology), Chinese Academy of Medical Sciences and Peking Union Medical College from 2011 to 2015 with the aim of determining the patterns of CSIG with the main coverage of southeastern China.

    Materials and methods

    Data collection

    The protocol for diagnosing CSIG is presented in Figure 1.We collected the data of patients diagnosed as CSIG from January 1,2011 to December 31,2015 in the Hospital for Skin Diseases (Institute of Dermatology), Chinese Academy of Medical Sciences, which is a national specialized hospital of dermatology with its main coverage on southeastern China.

    All patients diagnosed as CSIG met the following criteria:(1)the clinical manifestations and histopathology conform to cutaneous or subcutaneous infectious granuloma, and (2) have positive results from etiological examination.All cases had positive culture or polymerase chain reaction results combined with DNA sequencing of a single pathogen.Clinical specimens(tissue)were collected for pathological examination, which showed granulomatous inflammation and fungal hyphae, spores, acid-fast bacillus, or other characteristic findings, such as sulfur granules.

    All available data were collected and analyzed for clinical and pathological characteristics. The medical records were independently reviewed by two dermatologists (Dr ZZ Yan and Dr MH Fu).

    Statistical analysis

    The data were described by the number, ratio, and mean value according to the pathogen type.All the analyses were performed using the software program Microsoft Office Excel.

    Results

    A total of 256 cases of CSIG over the five years were included. The male/female ratio among the patients was 1.51 (137/119). The age distribution of the 256 CSIG patients ranged from 4 to 90 years old(Table 1).The mean age of the patients was 52±18.49 years. Infections were more common in those aged over 40 years (195/256,76.17%).

    Figure 1. Diagnosis flowchart of cutaneous and subcutaneous infectious granuloma.

    Clinical features

    The frequency of specific lesion sites varied(Table 1).The distal extremities were the most common lesion site(32.03%), followed by the face (27.34%) and the upper limbs (22.27%). Among the 186 cutaneous cases, the predominant clinical forms were plaque (42.96%) and nodule (28.87%) (Table 2). Among 182 patients with complete medical history records, 11 were in an immunosuppressive state: 1 had a solid organ transplant,1 had chronic kidney disease and took an oral immunosuppressant, 2 systemic lupus erythematosus and 3 rheumatoid arthritis with a long history of oral corticosteroid use,and the other 4 suffered from hepatitis B virus infection,tuberculosis,or human immunodeficiency virus infection. The cause of CSIG was documented in a few cases, with injury (26/48, 54.17%) caused by trauma,medical operation, or aquatic animal as the major cause.Another risk factor was a history of water contact (9/48,18.75%), including contact with environmental or reserved water or with an aquatic animal (swimming or working in a fishery, in aquaculture, or as a mariner).

    Pathogen distribution

    A total of 28 pathogens involving 153 patients were identified from the 256 patients, and mycobacteria infection constituted the major infection of CSIG group.

    Mycobacterium leprae (M. leprate,68/256,26.56%)wasthe most frequent cause of CSIG, followed by Sporothrix schenckii(S.schenckii,61/256,23.83%),Mycobacterium tuberculosis (M. tuberculosis, 40/256, 15.63%), and dematiaceous fungi (25/256, 9.7%). Mycobacterium marinum (M. marinum, 23/153, 8.98%) was the most common nontuberculous mycobacteria (NTM). A generally steady constituent ratio of each species was isolated from the CSIG cases during the five-year observation period.The causative pathogens from each study year are presented in Table 2.

    Table 1 Characteristics of cutaneous and subcutaneous infectious granuloma cases

    Pathological features

    Pathological examinations of the patients were conducted.In the fungal group,47 of 103 patients(45.63%)showed hyphae or spores after acid–Schiff or Gomori’s methenamine silver staining within the granulomas.Dematiaceous fungi exhibited high positive rates (17/25, 68.00%) after special staining compared with S. schenckii (22/61,36.07%). In the mycobacterium group, all 153 patients underwent acid-fast staining, and 48 cases (31.37%)showed acid-fast bacilli after Ziehl–Neelsen staining. Of the 68 leprosy patients, 37 (54.41%) manifested positive staining results. In contrast, only 6 of the 40 M.tuberculosis infections (15.00%) and 5 of the 23 M.marinum infections (21.74%) exhibited positive staining results.The other 161(62.89%)patients had granulomatous inflammation but did not exhibit characteristic evidence of any specific pathogens following special staining.

    Treatment and prognosis

    Among the 182 patients with available treatment records,116 underwent drug susceptibility testing and/or drugresistant gene detection. For the mycobacterium group, 2 of the 40 cutaneous tuberculosis(CTB)cases were resistant to streptomycin, 1 was resistant to rifampin, and 1 was resistant to isoniazid. For the cases of cutaneous sporotrichosis, only 1 out of the 35 patients who did not respond to itraconazole, terbinafine, or ketoconazole for at least 10 months exhibited sensitivity to a saturated solution of potassium iodide. Although a few of the M.marinum infections were treated with clarithromycin or levofloxacin monotherapy, most patients received combined antibiotic therapy. The improved treatment results were observed through visible scarring or recovery of the lesions, with or without the negative conversion of etiological examination,such as slit-skin smears of leprosy patients and the culture of pathogenic microorganisms from clinical specimens.In this group,97.80%of patients responded well to treatment with classical or sensitive antibiotic therapy (178/182).

    Discussion

    Here, we report the pattern of CSIG at a national skin disease hospital in Jiangsu, China. We found that themycobacterium group involved more cases than did the fungal group,which is consistent with a previous study in Egypt.2The predominance pathogen is of mycobacterial infections in our CSIG case study,particularly leprosy and M. tuberculosis, which may indicate a health hazard in China.Meanwhile,M.marinum accounted for 51.11%of NTM infection, and this result is comparable with other reports.3

    Table 2 Annual distribution of cutaneous and subcutaneous infectious granuloma isolates (2011–2015) (n)

    One group analyzed the reported cases and other domestic studies of CSIG since the 1980s and determined that the most common causative species was S.schenckii in Northeastern China, Cladosporium carrionii in Shandong province, which is located in Eastern China,and Fonsecaea pedrosoi in Guangdong/Guangxi province, which is located in South China.4Most sporotrichosis cases in Northeast China were caused by trauma and are more common in the spring and winter.5The majority of reported cases occurred in individuals who used reed and corn straw to get warm during the cold season, mainly because S. schenckii is commonly isolated from reeds, corn straw, and soil, and minor trauma may facilitate the spread of the disease.However,the most frequently found fungal strain in our patient was S. schenckii, followed by Fonsecaea pedrosoi and Cladosporium carrionii. The possible explanation is the different sources of patients.

    In our patients, the clinical manifestations were comparable with those from previous work, and plaque is the most common lesion, followed by nodules and erythema, and ulceration.2In one previous study, ulcerations (42%) and papules (34%) were the most frequent lesion morphologies, although macules, vesicles, and/or pustules, which were occasionally hemorrhagic, often preceded ulcerations.6Therefore, all skin lesions that are considered as highly suspicious should be biopsied for pathological examination and microorganism culture.

    The distal extremities were the most common location of skin lesions, followed by the face and upper limbs. S.schenckii affected the face in more than half of the cases,which is consistent with previous research conducted in children in an endemic area of China.7Furthermore, a large sample survey revealed that the upper limbs are still the most common site of infection for this species.5

    CSIG is difficult to diagnose because of its varied and nonspecific manifestations, but histopathology can be helpful in confirming the diagnosis. The most common type of S.schenckii and dematiaceous fungi infection was hyperplastic epidermis with granulomatous inflammation(48/86, 55.81%). The suppurative granuloma type(4/25,16.00%) showed a high frequency in the dematiaceous fungal group, whereas the characteristic “sporotrichoid”suppurative granuloma was presented in less than 20%of the patients.Asteroid bodies were observed at the center of the granuloma of one patient,although they were not the pathognomonic evidence of the disease.These frequencies are considerably lower than those reported by some previous studies.8-9Out of the 40 CTB cases in our study,22 had epithelioid cell granulomas, and caseous necrosis was present in three cases. The rest of the CTB patients showed a diffuse infiltration of mixed inflammatory cells,which has been observed previously in most NTM patients,along with small vessel proliferation.10However,this finding is not specific for mycobacteria infection and is also observed in other inflammatory diseases. The alternate manifestations of acanthosis or pseudoepitheliomatous hyperplasia of the epidermis,subcutis,and deep soft tissue were observed in 43.3% and 10% of patients,respectively. The depth of biopsy may account for the lower rate observed here compared with the rates obtained in related studies.2,11Additionally,suppurative granuloma and intradermal cyst lined by squamous epithelium and surrounded by inflammation, which are usually observed in rapidly growing mycobacterium infection,2were found at a lower rate in our study.

    For the fungal group, the dematiaceous fungi exhibited high positive rates after special staining in our study compared with S.schenckii;this finding agrees with other related work.A previous report ascribed the difference to the more obvious fungi and more severe inflammation caused by dematiaceous fungi compared with S.schenckii.12In the mycobacterium group, the sensitivity of acid-fast bacillus detection (48/153, 31.37%) was higher than that of other series,3,13partly because multibacillary leprosy is the most common pathogen in this group.

    In accordance with other publications,13–15a history of injury or water contact history increased the chance of exposure to the normal environmental inhabitants that are considered as risk factors correlated with CSIG. Several studies have related the increase in fungal and mycobacterium cutaneous infections to the growing population of immunosuppressed patients.15However, few of our patients were in an immunosuppressive state,a trend that is comparable with other reports.12Most of our patients were sensitive to standard or empirical therapy and had a benign course, partly because the subset of patients who attend a specialized hospital like ours are more likely to be in good physical condition and lack prior treatment history.

    In conclusion, we preliminarily present the pattern of CSIG from 2011 to 2015 at a national skin diseases hospital in China. The most common pathogen was M.leprae, followed by S.schenckii and M. tuberculosis. The disease appeared to be associated with advanced age and occurred more frequently in males than in females. The appearance of a plaque or nodule on exposed parts with a history of injury should be highly suspected as cases of CSIG.The present study promotes awareness of CSIG and may help dermatologists confirm clinical suspicion of CSIG.

    Acknowledgements

    This study was supported by grants from Chinese Academy of Medical Sciences Innovation Fund for Medical Sciences(CIFMS-2016-I2M-1–005), National Natural Science Foundation of China (81371751), and Natural Science Foundation of Jiangsu Province of China (BK20141065).

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