• View in gallery

    (A) Multiple tense blisters and bullae filled with clear fluid and surrounded by erythema, and discrete nodules on the penile skin. (B) Papules and vesicles on the hand, especially the webs of the fingers.

  • View in gallery

    Scabies mites and eggs detected on the scraping from the papules.

  • View in gallery

    The age distribution of patients with bullous scabies shows that more than a half of patients are older than 70 years.

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Bullous Scabies

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  • 1 Department of Dermatology, The Eastern Hospital of The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.
  • 2 Department of Dermatology, The Fifth Affiliated Hospital, Guangzhou Medical University, Guangzhou, China.
  • 3 Department of Paediatrics, The Eastern Hospital of The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.
  • 4 Department of Dermatology, Maulana Azad Medical College–Lok Nayak Jai Prakash Narayan (LNJP) Hospital, New Delhi, India.

Scabies is a common contagious cutaneous disease and usually affects the young, characterized by polymorphous lesions that may present as burrows, pruritic papules, and inflammatory nodules. Bullous scabies (BS) is its rather rare subtype, mimicking bullous pemphigoid. We report a 15-year-old Chinese boy presenting with 1-month history of pruritic bullae on his penile skin, showing poor response to both topical steroids and systemic antihistamines, but cured by sulfur ointment alone. No recurrence occurred in the 5 years of follow-up. We also reviewed the published cases. Up to date, 44 cases, including the present, have been reported. Of them, 30 were male and 14 were female. The age range was from 1 to 89 years old, with a median age of 70.6 years. The bullous lesions may involve the arms, legs, trunk, genitals, feet, buttocks, thighs, neck, inguinal folds, and may even be generalized. Trunk and extremities are the most common involved locations. Facial or mucosa involvement had never been reported. The histological findings present as a subepidermal split with variable inflammatory infiltrate predominantly neutrophils, and eosinophilic spongiosis, or both. Eighteen of 32 patients showed positive deposition of linear-granular IgG or complement 3 alone or in various combinations, and five of 24 patients revealed circulating IgG. All the 40 cases with therapeutic details were cured by antiscabietic remedy. BS always involves the trunk and extremities. It has a predilection for elderlies and males. The treatments for BS are similar to those of classical scabies.

Introduction

Scabies is a common, worldwide, contagious cutaneous disease, which is caused by Sarcoptes scabiei and affects the individuals of all ages, races, and social classes in any climate.1 It has a preference for the young,24 but no gender difference and racial predominance have been described.3 The common risk factors for scabies include overcrowding, immigration, poor hygiene, poor nutritional status, homelessness, dementia, sexual or close contact,36 and immunocompromised individuals.7 The typical symptom is an intense, intractable, generalized pruritus that is worse at night36; but occasionally, patients may be asymptomatic.8 The most common presentations of scabies include classic burrows, pruritic papules, and inflammatory nodules.36 Occasionally, the lesions may resemble impetigo,9 psoriasis,9 contact dermatitis,9 urticaria,10 Darier's disease,11 or dermatitis herpetiformis.12 In 1974, Bean13 first described bullous scabies (BS): a rare subtype of scabies. To our knowledge, 43 cases1350 have been reported up to date. Herein, we report a Chinese boy with BS and review the literature including the clinical and pathological features.

Case Presentation

A 15-year-old Chinese boy presented with 1-month history of pruritic bullae on his penile skin, which had poor response to both topical steroids and systemic antihistamines. The symptoms preceded by abdominal, genital, and hand pruritus with nocturnal exacerbation of 3-month duration. Cutaneous examination showed that multiple tense blisters and bullae with diameter from 0.3 to 1.2 cm, which were filled with clear fluid and surrounded by erythema, were distributed over the penile skin (Figure 1A). The Nikolsky sign was negative over the lesions. There were discrete nodules (Figure 1A) and papules distributed over the penis and the scrotum. Papules and vesicles presented on his abdomen, hands, wrists, and especially on the webs of the fingers (Figure 1B). There was no mucosal and facial involvement. Several of his close classmates had nocturnal itching lesions but without bullae. No other family members were similarly affected. Direct microscopy of scraping from the papules of digital webs revealed S. scabiei mites and eggs (Figure 2). No biopsy was taken. The patient was treated with topical 10% sulfur ointment alone, resulting in rapid improvement for the itching and gradual disappearance for the bullae. No recurrence occurred during a 5-year follow-up.

Figure 1.
Figure 1.

(A) Multiple tense blisters and bullae filled with clear fluid and surrounded by erythema, and discrete nodules on the penile skin. (B) Papules and vesicles on the hand, especially the webs of the fingers.

Citation: The American Society of Tropical Medicine and Hygiene 95, 3; 10.4269/ajtmh.16-0273

Figure 2.
Figure 2.

Scabies mites and eggs detected on the scraping from the papules.

Citation: The American Society of Tropical Medicine and Hygiene 95, 3; 10.4269/ajtmh.16-0273

Literature Review

Using keywords “bullous scabies,” we searched MEDLINE and PubMed on March 25, 2016, for all articles published in English or published with English abstract details, and searched the China National Knowledge Infrastructure (http://cnki.net/) for content written in Chinese using the above term. We also selected the cases if the references had details. All the published cases diagnosed as BS were recruited for the review, including the following data: patient's age at discovery, gender, lesional location(s), clinical features, pathological changes, and treatment and its outcome.

Results

All the reported cases, including the present case, are summarized in Table 1. Among them, four were selected from reference 21 of which we lacked the full text, and there still included a dilemmatic case reported by Balighi and others.36 Of the 44 cases, 30 were male1319,21,2530,32,3437,39,4147 and 14 were female.16, ref-type="bibr">17,2024,29,31,33,38,40,4850 The age range was from 1 to 89 years, with a median age of 70.6 years; it also showed that only seven patients were under 30 years (Figure 3). Bullous locations were described in 36 cases, varying from arms,1420,22,24,27,3033,35,37,38,40,46 legs,1620,22,24,25,2730,35,3740,46 trunk,15,18,19,22,28,30,32,35,37,38 genitals,15,16 feet,31 buttocks,28 thighs,30,41 neck,15 inguinal folds,16,28 and even generalized13,16,18,23,29,36,50; but facial or mucosa involvement had never been reported. The blisters were preceded by pruritus, and may have occurred on immunosuppressed individuals.17,22 Recurrent BS was also described in a case.19 No other associations were described except for a case of bullous pemphigoid (BP) subsequent to BS.38

Table 1

Summaries of the published bullous scabies

No.Published yearAgeGenderLocation of bullous lesionsIIF/DIF resultTherapyAuthorReference
119741MGeneralizedND/ND1% GBHBean13
219819FGeneralizedND/ND10% Benzyl benzoatePonce-Navarez and others50
3198113FGeneralizedND/ND10% Benzyl benzoatePonce-Navarez and others50
4198934FGeneralized−/−10% Benzyl benzoateViraben and Dupre23
5199167MArms, abdomen, genitals−/Granular IgG1% GBHBhawan and others15
6199176MNeck, back, arms−/Linear IgG, C31% GBHBhawan and others15
7199276FLDND/ND1% GBHKurosawa and others49
8199336FArms and legsIgG/Linear C31% MalathionOstlere and others24
9199369MLegs−/Linear IgM, C31% GBHParodi and others25
10199374MLDND/–LDShirlene-Jay and others42
11199374MChest−/ND1% GBH, 1% lindaneSaid and others26
12199484FLDIgG/Linear IgG, C3LDEzaki and others48
13199566FArms and legs−/Granular C325% Benzyl benzoateVeraldi and others20
14199573MArms and legs−/Granular C35% PermethrinHaustein27
15199676MTrunk, legs, inguinal folds, and buttocks−/Linear IgG, C35% Permethrin,Slawsky and others28
1% GBH, 6% sulfur
16199773MLegsND/−25% Benzyl benzoateClyti and others46
17199789FArms and legsND/−25% Benzyl benzoateClyti and others46
18199964MLDIgG/Linear IgG, C3LDKambara and others43
19200081MLDIgG/Linear IgG, C3LDInoue and others44
20200070FLegsND/−5% Permethrin/oral ivermectinBosch-Garcia and others29
21200072MGeneralizedND/−5% Permethrin/oral ivermectinBosch-Garcia and others29
22200176MTrunk and thighs−/Granular IgG, C3, and C41% GBHBornhovd and others30
23200189MTrunk and extremitiesIgG/linear IgG and C31% GBHBornhovd and others30
24200352MLD−/−5% PermethrinBrar and others45
2520034MLeft handND/ND5% PermethrinShahab and Loo17
26200334MTrunk and limbsND/−5% Permethrin lotionKaur and Thami19
27200530FTrunk, arms, and legsND/ND5% PermethrinJena and others22
28200642MLower trunk, arms, and legsND/−1% LindaneAnsarin and others18
29200371MArms, legs, and trunk−/Linear IgG, C3Oral ivermectinNakamura and others21
30200672MLD−/Linear IgG and C3Oral ivermectinGalvany and others47
31200652MGeneralized−/Linear IgG and C3Oral ivermectin and prednisoloneBalighi and others*36
32200865MTrunk and arms−/−Sulfur 20% in yellow soft paraffinWozniacka and others32
33200970FArms−/−10% Sulfur ointment, and hydrocortisoneMarciniak and others33
34201087FArms and feet−/−Topical lindaneSerra and others31
35201072MGenitals and inguinal folds−/Linear IgG and C3Oral ivermectin, topical compounds (permethrin, triamcinolone acetonide, gentamycin)Rossell and others16
36201179MLDND/−Benzyl benzoate 20%Roxana Stan and others34
37201354MTrunk and limbsND/linear IgG and C310% Sulfur ointmentChen and Luo35
38201326MBoth handsND5% Permethrin lotion and a single 12-mg dose of oral ivermectin along with oral antihistaminesGutte14
39201465MTrunk and extremities−/−20% Sulfur ointmentZhang and others37
40201578FTrunk and extremitiesND10% Sulfur ointmentHuang and others38
41201523MRight foot 5% PermethrinMaan and others39
42201587MArms and legsND/Linear IgG, IgM, and C312.5% Sulfur and 5% permethrinAkin Belli and others40
43201573FThighs−/−10% Sulfur creamSu and others41
44201015MGenital foldsND/NDTopical sulfur ointmentPresentPresent

DIF = direct immunofluorescence; F = female; GBH = gamma benzene hexachloride; IIF = indirect immunofluorescence; LD = lack data; M = male; ND = not done; − = negative.

The case is dilemmatic whether it is a bullous scabies or scabies-induced bullous pemphigoid.

We do not understand the text clearly except the gender and age.

The case was diagnosed on 2006 and the article was published on 2010.

Figure 3.
Figure 3.

The age distribution of patients with bullous scabies shows that more than a half of patients are older than 70 years.

Citation: The American Society of Tropical Medicine and Hygiene 95, 3; 10.4269/ajtmh.16-0273

The pathological findings included a subepidermal split with variable inflammatory infiltrate predominantly neutrophils, and eosinophilic spongiosis, or both17; which mimic the pathological features of BP.18 However, intraepidermal blister was also reported.14 The scabies mites or eggs could be found in the bullae occasionally.19,33 Thirty-two patients had been studied by direct immunofluorescence (DIF); among them, 18 were positive and 14 negative. The most frequent presentations for DIF were linear IgG combined with complement 3 (C3) deposit (11/18), the rare conditions included combinative deposit of granular IgG, C3, and complement 4 (C4) (1/18); linear IgM combined with C3 (1/18); linear deposit of IgG, IgM, and C3 (1/18), or only a single component deposition including granular IgG (1/18), linear C3 (1/18), or granular C3 (2/18). Nineteen of 24 patients showed negative results for indirect immunofluorescence (IIF), whereas five revealed circulating IgG binding to the dermoepidermal junction.24,30,43,44,48 Seven of 23 patients showed negative results for both DIF and IIF.23,3133,37,41,45

Forty patients were reported with therapeutic options, whom were cured by antiscabietic remedy, including topical gamma benzene hexachloride, sulfur ointment or cream, malathion, benzyl benzoate, permethrin or systemic ivermectin, or topical ointment combined with systemic ivermectin. Antihistamines, topical or systemic steroids, immunoglobulin, or cyclophosphamide alone, or in different combinations have been tried, showing poor response to BS besides palliative improvement of itching and/or lesions.14,16,35,36,40,41 Interestingly, oral prednisolone was reported worsening the lesions in a case.21

Discussion

BS, also called BP-like eruption,15 is an atypical manifestation of scabies, which may develop concurrently with, or after, the occurrence of scabietic lesions.2628,51 Despite the lack of histopathological examination for the present case, scabies mites were detected, and both the lesions and symptoms disappeared after antiscabietic therapy alone without recurrence during a 5-year follow-up; all these suggested that the diagnosis was BS.

The present results showed that BS has male predilection and mainly afflicts the elderly, especially patients older than 70 years; such an age group is the same in which BP mainly occurs. The reasons for elderly predominance, we speculate, are that older individuals have increased likelihood of bedridden status and stay in nursing homes, resulting in increased risk of scabies infection.52,53 The exact mechanisms are not fully understood yet. The lesions may involve, except the mucosa and face, the whole body including arms, legs, trunk, genitals, feet, buttocks, thighs, neck, inguinal folds, and may even be generalized; but the trunk and extremities are the most commonly involved areas. Scabies mites and/or eggs may be detected from the lesions of BS, but not always. The pathological features of BS are similar to those of BP; however, true BP subsequent to BS had indeed occurred.38 We considered that the case described by Balighi and others36 was BS rather than BP, because of the positive detection of the scabies mites from the vesiculobullous lesion, and the excellent response to medications. Although China has about 20% of the world population and is a developing country, only five cases of BS, including the present one, had been reported up to date,35,37,38,41 and three were described by our group,35,38 we considered that BS may have been largely misdiagnosed or neglected as a diagnosis in China before.

The mechanisms of bullae formation for BS remain unknown. Superinfection was considered to play an important role in some patients with a positive culture of Staphylococcus aureus.18 In patients with positive deposition of C3 and various immunoglobulins, it was considered that the bullae may result from the direct injury or secretion of lytic enzymes by the scabies mites, which alters the basement membrane zone (BMZ) antigen resulting in autoantibody formation and inducing inflammatory reaction18; or mite proteins may have cross-reactivity with BMZ antigens and lead to the production of the autoantibodies, activating immunoreaction and producing the bullae.20 In patients with negative DIF, id reaction, also called autoeczematization, to scabietic mite was considered as the mechanism of bullae.18 Bornhovd and others30 considered that persistence of scabies led to a specific immune response with activation of Th2 cells, resulting in increase of interleukin-5 and eosinophilia, and causing BS. However, the present results found that 18 of 32 BS patients had positive finding of DIF with linear-granular IgG and/or C3 alone or in various combinations, whereas only five of 23 revealed circulating IgG on IIF study. The previous study demonstrated that positive epidermal immunofluorescent staining does not indicate absolutely an autoimmune bullous disease54; the value of positive immunofluorescent staining in BS needs further studies. Because of the deposition of immunoglobulin and C3 in the BMZ, the detection of circulating IgG in some patients, and the excellent response to antiscabietic treatments, BS can be considered a scabies-induced immune response.35 But, it is still hard to understand why the lesions of BS had poor response to immunosuppressants, and the lesions could occur on the immunosuppressed individuals,17,22 or even progressed after treatment with prednisolone.21 It is also unclear why BS does not occur more often although scabies is a common disease, and why it has male predilection.

Because of the lack of defined diagnostic criteria, the diagnosis of BS should be considered for any bullous eruptions accompanied by papules and nocturnal itching, and the itching responds well to antiscabietics, but resists immunosuppressants, regardless of the histopathology and scraping findings. We suggest that the patient diagnosed as BS may have a follow-up as long as possible so that true BP can be excluded. The doctors also should pay attention to the possibility of recurrent BS.19 Moreover, as circulating antibodies against BP180 and/or BP230 had been detected in some of the scabietic patients with bullous eruptions,38,51 and persistent circulating antibodies against scabies antigens have been identified in dogs and foxes by enzyme-linked immunosorbent assays,54 we support the opinion that some of the bullous lesions occurring in scabies are true BP.38,51

The differential diagnoses include BP, pemphigus, arthropod bite reaction, acute contact dermatitis, and bullous impetigo,17 as well as epidermolysis bullosa acquisita. As both clinical and pathological features of BS resemble those of BP,17 even when the skin scrapings are positive for scabies, it is still hard to differ true BP from BS,16,21 and to exclude the possibility of scabies and concomitant BP.21 It is also reported that patients suffering from scabies have an increased risk for BP.52 In fact, true BP subsequent to scabies or to BS have been reported.9,38,51,55 Usually, the facts that the detection of scabies mites and/or its eggs from scraping, good response to antiscabietic treatment, and/or the patients with either negative or low values of circulating IgG,16,21 are important clues for the diagnosis of BS. Nakamura and others21 considered that IIF study is more important than DIF to distinguish BS from BP. We considered, if possible, that circulating antibodies against either BP180 or BP180 and BP230 might be tested, for which the positive results support the diagnosis of BP. On the basis of the clinical manifestations and pathological changes, other differential diagnoses are not difficult to exclude.

The therapies of BS are similar to those of classical scabies including systemic and topical treatments. In patients with poor response or allergic reaction to topical treatment, systemic ivermectin is an option. Because resistance of common scabies to permethrin and lindane has been reported,3,4,6 the doctors should pay more attention to the patients of BS with poor response to the medications, although such a condition has never been reported before. For recurrent BS, multiple applications must be administered.19 Immunosuppressants seem to be of no benefit to BS. In rare conditions, oral prednisolone may worsen the lesions.21 As a matter of fact, doctors always select drugs based on their personal predilection, local availability, and the cost.3,5

Conclusions

BS is a rare subtype of scabies that commonly afflicts the elderly with a median age of 70.6 years. The lesions may involve the whole body except the mucosa and face. Its clinical and histopathological features mimic those of BP. No defined diagnostic criteria for BS have been proposed. A diagnosis of BS should be considered for any bullous eruptions accompanied by papules and nocturnal itching that respond well to antiscabietics but are resistant to immunosuppressants, regardless of the histopathology and scraping findings. The treatments for BS are similar to those of classical scabies.

Consent

Written informed consent was obtained from the patient for publication of this case report and any accompanying images.

ACKNOWLEDGMENT

We sincerely thank the patient who participated in the present study.

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Author Notes

* Address correspondence to Di-Qing Luo, Department of Dermatology, The Eastern Hospital of The First Affiliated Hospital, Sun Yat-sen University, 183 Huangpu Road East, Guangzhou 510700, China. E-mail: luodq@mail.sysu.edu.cn† These authors contributed equally to this work.

Authors' addresses: Di-Qing Luo, Juan-Hua Liu, and Yu-Kun Zhao, Department of Dermatology, The Eastern Hospital of The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China, E-mails: luodq@mail.sysu.edu.cn, liujuanhua@medmail.com.cn, and zhaoyukun7288569@sina.com. Mei-Xing Huang, Department of Dermatology, The Fifth Affiliated Hospital, Guangzhou Medical University, Guangzhou, China, E-mail: gygyhmx@126.com. Wen Tang, Department of Paediatrics, The Eastern Hospital of The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, People's Republic of China, E-mail: tangwen@mail.sysu.edu.cn. Rashmi Sarkar, Department of Dermatology, Maulana Azad Medical College–Lok Nayak Jai Prakash Narayan (LNJP) Hospital, New Delhi, India, E-mail: rashmisarkar@yahoo.com.

Reprint requests: Di-Qing Luo, Department of Dermatology, The Eastern Hospital of The First Affiliated Hospital, Sun Yat-sen University, 183 Huangpu Road East, Guangzhou 510700, China, E-mail: luodq@mail.sysu.edu.cn, Tel: 862082379516, Fax: 862082398840.

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