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 Table of Contents  
CASE REPORT
Year : 2015  |  Volume : 2  |  Issue : 3  |  Page : 257-261

Onychomycosis due to Aspergillus niger with concomitant multiple fungal infections in a human immunodeficiency virus infected person


Department of Microbiology, Indira Gandhi Medical College, Shimla, Himachal Pradesh, India

Date of Web Publication12-Jun-2015

Correspondence Address:
Dr. Sunite A Ganju
House No. 214/B, Sector 3, New Shimla, Shimla - 171 009, Himachal Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2348-3334.158710

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  Abstract 

Opportunistic fungal infections are common in human immunodeficiency virus (HIV) infected patients and commonly occur at some point during their illness. Though estimates show that these infections can occur in HIV patients with the same frequency as in the control group, their presentations are more severe and variable in HIV/acquired immunodeficiency syndrome. We present an HIV infected case with multiple fungal infections. This patient had onychomycosis due to Aspergillus niger, tinea cruris caused by Trichophyton rubrum, oral thrush and balanoposthitis due to Candida albicans.

Keywords: Aspergillus niger , candidiasis, human immunodeficiency virus, onychomycosis, tinea cruris


How to cite this article:
Ganju SA, Bhagra S, Kanga AK. Onychomycosis due to Aspergillus niger with concomitant multiple fungal infections in a human immunodeficiency virus infected person. CHRISMED J Health Res 2015;2:257-61

How to cite this URL:
Ganju SA, Bhagra S, Kanga AK. Onychomycosis due to Aspergillus niger with concomitant multiple fungal infections in a human immunodeficiency virus infected person. CHRISMED J Health Res [serial online] 2015 [cited 2019 Oct 23];2:257-61. Available from: http://www.cjhr.org/text.asp?2015/2/3/257/158710


  Introduction Top


Opportunistic fungal infections are commonly found in Human immunodeficiency virus (HIV) infected patients and are a major cause of mortality and morbidity. The spectrum of clinical presentations are atypical, varied and simultaneous multiple fungal infections can co-exist. Thus it is important to maintain a high index of clinical suspicion to establish early diagnosis and treatment.


  Case Report Top


A 43-year-old male patient was admitted in the Department of Dermatovenerology with complaints of erythematous rash and soreness in the penile region for the last 2 weeks. He had noticed raised itchy red colored patches and small papules in the groin extending to the medial aspect of both the thighs for last 6-8 months. He complained of loss of appetite and marked weight loss during the last 2 years. For the past 9 years, he had noted that the toe nails of both feet and finger nails of the left hand were disfigured and getting deformed.

On general physical examination patient was conscious, cooperative and well oriented. The vitals were stable; pulse rate 68/min, blood pressure 120/80 mmHg and respiratory rate 18/min. Examination of the chest, cardiovascular, central nervous system revealed no apparent abnormality. On local examination of the oral cavity curdy white plaques 2.5 × 2.5 cm on the anterior two-third of the tongue along with bilateral angular cheilitis [Figure 1] were observed. In the groin multiple well-defined hyperkeratotic erythematous plaques 2 × 2 cm [Figure 2] were noticed. On the glans penis 1 × 1 cm areas of erythrema were seen [Figure 3]. The nails of the left hand (index, middle and ring finger) showed discoloration, pitting and dystrophic changes. In both toe nails, coarse pitting and longitudinal ridges were noted [Figure 4]. The patient was detected to be positive for human immunodeficiency virus-1 (HIV-1) antibodies with a cluster of differentiation 4 (CD4) cell count of 186 cells/mm 3 . Other relevant laboratory investigations were within normal limits.
Figure 1: Oral candidiasis with angular cheilitis

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Figure 2: Tinea cruris

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Figure 3: Balanoposthitis

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Figure 4: Dystrophic onychomycosis of the finger nails

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Patient was evaluated to establish the etiological diagnosis. Scrapings from anterior two-third of the tongue were examined microscopically. In potassium hydroxide (KOH), wet mount budding yeast cells along with pseudohyphae were seen on microscopy. On culture on Sabouraud's dextrose agar (SDA), creamy white yeast like colonies suggestive of Candida species were obtained. The colonies were positive for germ tube formation, and the isolate was confirmed as Candida albicans. Skin scrapings from the groin were inoculated on SDA containing chloramphenicol 0.005% and incubated at 25°C. Growth of powdery white colonies on obverse and reddish brown pigment on the reverse was obtained after 8 days of incubation. On microscopic examination of the lactophenol cotton blue (LCB) mount, microconidia arranged in a bird on fence appearance along thin delicate hyphae 2-3 μm in diameter were seen. The findings were consistent with a diagnosis of tinea cruris caused by Trichophyton rubrum. Nail clippings and subungual debris collected from fingers and toe nails were subjected to KOH wet mount examination and culture on SDA containing 0.005% chloramphenicol. Septate hyphae were seen on direct KOH wet mount microscopic examination [Figure 5]. Black sporulating colonies were seen after 2-3 days of incubation of the culture. Examination of the LCB mount showed conidia arranged on the phialides covering the entire vesicle [Figure 6]. The culture characteristics resembled Aspergillus niger. The same species was re-isolated to rule out the possibility of laboratory contamination. Scrapings from the glans penis were collected aseptically and examined on KOH microscopy and culture on SDA. The findings were consistent with a diagnosis of C. albicans. The patient was diagnosed to have onychomycosis, oral thrush, balanoposthitis, and tinea cruris. Patient was grouped in WHO clinical stage 3. He was treated with antifungals and administered first line antiretroviral therapy with zidovudine, lamivudine, and nevirapine. The patient on follow up after 3 months showed clearing of fungal infection and his last CD4 count was 644 cell/mm 3 .
Figure 5: Direct microscopic examination of scrapings: Dichotomous septate hyphae (potassium hydroxide mount, ×400)

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Figure 6: Microscopy of Aspergillus niger in culture: Colony showing vesicles at the apex of the conidophore bearing phialides on upper two-third of its surface with chains of small phialoconidia with septate hyphae (lactophenol cotton blue mount, ×400)

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  Discussion Top


Multiple fungal species and unusual opportunistic fungi are frequently cultured from HIV infected patients and may correlate to their immunocompromised state. [1] This study case was a 43-year-old, male factory worker, HIV positive and diagnosed with onychomycosis left finger nails and both toe nails along with oral candidiasis, angular cheilitis, balanoposthitis, and taenia cruris.

Onychomycosis

Onychomycosis in HIV infected patients is reported to occur in 15-40%, four times more common in the HIV infected patients than in the general population. [1],[2] According to age and sex distribution, various studies report onychomycosis to be more common in males and in the age group of 31-40 years. [1],[3] In the present study, case occupational exposure to trauma, being a factory worker could have been a predisposing factor to onychomycosis. Finger nail onychomycosis associated with toe nail infections, typically described as one hand two feet syndrome has been described in literature. The involvement of fingernail as well as toenails has been noted by Cribier et al. in his study, where out of the 47 patients, 42 had toenail, 3 had fingernail and 2 had both fingernail and toenail involvement. [1] Though, the main causative fungus of onychomycosis is reported to be T. rubrum,[3] we repeatedly isolated A. niger. In HIV infected patients, differences both in the clinical type and in the causative organisms can be observed. [1] Several studies have been conducted with regard to onychomycosis caused by A. niger. Onychomycosis caused by Aspergillus species range from 2.6% to 6.1% world-wide. [4],[5] In a clinical and mycological study of onychomycosis in HIV infection, three cases A. niger out of 19 nondermatophytic cultures were identified. [6] Similarly, Tosti and Piraccini have reported two cases [7] and Grover has reported A. niger as a causative pathogen of onychomycosis in eight HIV patients. [8] Aspergillus species are common laboratory contaminants, and it is important to characterize whether these are true pathogens or not. A. niger, a nondermatophyte mold is found as an opportunistic fungus in the environment. As stated by English, nondermatophytic mold can be considered to be a causative agent of onychomycosis only when hyphae or spores are seen on microscopic examination and the same strain is identified through repeated cultures. [9] In A. niger, microscopic examination of KOH wet mount, dichotomous septate hyphae are visualized. The growth of colonies in culture is rapid, initially appearing whitish but turn black with time. On microscopic examination of LCB mount hyaline septate hyphae and biseriate phialides covering the entire vesicle with radiate conidial heads are seen. [9] In the present case, characteristic findings of A. niger were observed in repeated cultures on SDA, KOH wet mount and with LCB stain.

According to Baran et al. [10] onychomycosis is classified into five clinical types: (1) Distal lateral subungual onychomycosis (DLSO), (2) superficial white onychomycosis, (3) proximal subungual onychomycosis (PSO), (4) endonyx onychomycosis, and (5) total dystrophic onychomycosis. DLSO is the most common type, and PSO is the rarest form of onychomycosis in the general population. PSO is associated with HIV/acquired immunodeficiency syndrome (AIDS) and is considered to be an early marker of HIV infection. [11] Clinically, our patient presented with subungual hyperkeratosis and proximal onycholysis and the nail plate had a consistency of a plaster, clinically presenting as PSO. In our patient, both the toe nails and fingers of the left hand were affected, characteristic of HIV infection. HIV patients with onychomycosis frequently have involvement of not one, but can infect all of their toenails. [1] Onychomycosis is more common when the CD4 count is <450 cells/mm 3 . [11] In the present patient, the CD4 count was 186 cell/mm 3 . Onychomycosis can resemble psoriasis, and it is important to differentiate the two, as treatment of psoriasis can worsen onychomycosis. Psoriasis usually involves other skin sites and culture is the diagnostic tool for onychomycosis. However, the two conditions can also coexist.

Tinea cruris

Trichophyton rubrum is the most common cause of tinea cruris world-wide, regardless of HIV status. [12] In severely immunosuppressed patients with AIDS, the lesions have a little inflammation, and often the elevated border and central clearing is lacking, typical of tinea (Anergic tinea). [12] In our case, the lesion in the inguinal region had sharply marginated areas of hyperkeratosis resembling dry skin. Several authors have studied HIV infected patients having dermatophytosis. In a study from south India conducted by Kumarasamy et al., [13] 8.0% had dermatophytosis and Singh et al. [14] observed in 32.9% cases. The wide range variations could be explained on the category of HIV infected cases and climatic conditions. Extensive form of tinea may occur in hot, humid climates and can be seen at all levels of immunosuppression.

Oral candidiasis

Oral candidiasis is the most common HIV-related oral disorder occurring in 17-43% cases with HIV infection and in more than 90% of cases with AIDS. [15] In a study on microbial flora in HIV seropositive patients with angular cheilitis, C. albicans was isolated in 65% of cases. [16] Another study from South India on oral lesions and conditions associated with HIV patients a total of 217 (72%) out of the 300 patients had some oral lesion. Pseudo membranous candidiasis was noted in 33% and angular cheilitis in 8% cases. [17] The authors have also reported that the prevalence of oral candidiasis was higher in males. [17] Also, oral candidiasis has been very frequently associated with the CD4 cell count <200. [16] Our study case was a male patient with the CD4 count of 186 cells/mm 3 .

Candida balanoposthitis

Candida albicans is also a common cause of balanitis. Inflamation of the glans and prepuce may also provide a route for the acquisition of HIV infection. In a study conducted in Assam, candidal balanitis/balanoposthitis was found to be the most common sexually transmitted disease being present in 21.5% men. [18] In another study carried over a 3 years period, Candida was isolated from 35% of 450 men with balano-posthitis. [19] Thus, candida infection can be commonly associated with, and HIV sexually transmitted infections.


  Conclusion Top


Onychomycosis due to A. niger in HIV infected patients is an emerging isolate. HIV infected patients can present with multiple fungal infections, and hence it is essential to have in depth knowledge of the varied cutaneous fungal manifestation to avoid misdiagnosis.

 
  References Top

1.
Cribier B, Mena ML, Rey D, Partisani M, Fabien V, Lang JM, et al. Nail changes in patients infected with human immunodeficiency virus. A prospective controlled study. Arch Dermatol 1998;134:1216-20.  Back to cited text no. 1
    
2.
Goodman DS, Teplitz ED, Wishner A, Klein RS, Burk PG, Hershenbaum E. Prevalence of cutaneous disease in patients with acquired immunodeficiency syndrome (AIDS) or AIDS-related complex. J Am Acad Dermatol 1987;17:210-20.  Back to cited text no. 2
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Kaur R, Kashyap B, Bhalla P. Onychomycosis - Epidemiology, diagnosis and management. Indian J Med Microbiol 2008;26:108-16.  Back to cited text no. 3
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Gupta M, Sharma NL, Kanga AK, Mahajan VK, Tegta GR. Onychomycosis: Clinico-mycologic study of 130 patients from Himachal Pradesh, India. Indian J Dermatol Venereol Leprol 2007;73:389-92.  Back to cited text no. 4
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Gianni C, Romano C. Clinical and histological aspects of toenail onychomycosis caused by Aspergillus spp.: 34 cases treated with weekly intermittent terbinafine. Dermatology 2004;209:104-10.  Back to cited text no. 5
    
6.
Surjushe A, Kamath R, Oberai C, Saple D, Thakre M, Dharmshale S, et al. A clinical and mycological study of onychomycosis in HIV infection. Indian J Dermatol Venereol Leprol 2007;73:397-401.  Back to cited text no. 6
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Tosti A, Piraccini BM, Lorenzi S. Onychomycosis caused by nondermatophytic molds: Clinical features and response to treatment of 59 cases. J Am Acad Dermatol 2000;42:217-24.  Back to cited text no. 7
    
8.
Grover S. Clinico-mycological evaluation of onychomycosis at Bangalore and Jorhat. Indian J Dermatol Venereol Leprol 2003;69:284-6.  Back to cited text no. 8
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English MP. Nails and fungi. Br J Dermatol 1976;94:697-701.  Back to cited text no. 9
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Baran R, Hay RJ, Tosti A, Haneke E. A new classification of onychomycosis. Br J Dermatol 1998;139:567-71.  Back to cited text no. 10
    
11.
Vander Straten MR, Hossain MA, Ghannoum MA. Cutaneous infections dermatophytosis, onychomycosis, and tinea versicolor. Infect Dis Clin North Am 2003;17:87-112.  Back to cited text no. 11
    
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Kwon-Chung KJ, Bennet JE. Medical Mycology. Philadelphia: Lea and Febiger; 1992. p. 201-47.  Back to cited text no. 12
    
13.
Kumarasamy N, Solomon S, Madhivanan P, Ravikumar B, Thyagarajan SP, Yesudian P. Dermatologic manifestations among human immunodeficiency virus patients in south India. Int J Dermatol 2000;39:192-5.  Back to cited text no. 13
    
14.
Singh A, Thappa DM, Hamide A. The spectrum of mucocutaneous manifestations during the evolutionary phases of HIV disease: An emerging Indian scenario. J Dermatol 1999;26:294-304.  Back to cited text no. 14
    
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Lamster IB, Begg MD, Mitchell-Lewis D, Fine JB, Grbic JT, Todak GG, et al. Oral manifestations of HIV infection in homosexual men and intravenous drug users. Study design and relationship of epidemiologic, clinical, and immunologic parameters to oral lesions. Oral Surg Oral Med Oral Pathol 1994;78:163-74.  Back to cited text no. 15
    
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Krishnan PA, Kannan R. Comparative study on the microbiological features of angular cheilitis in HIV seropositive and HIV seronegative patients from South India. J Oral Maxillofac Pathol 2013;17:346-50.  Back to cited text no. 16
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Ranganathan K, Reddy BV, Kumarasamy N, Solomon S, Viswanathan R, Johnson NW. Oral lesions and conditions associated with human immunodeficiency virus infection in 300 south Indian patients. Oral Dis 2000;6:152-7.  Back to cited text no. 17
    
18.
Saikia L, Nath R, Deuori T, Mahanta J. Sexually transmitted diseases in Assam: An experience in a tertiary care referral hospital. Indian J Dermatol Venereol Leprol 2009;75:329.  Back to cited text no. 18
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Dockerty WG, Sonnex C. Candidal balano-posthitis: A study of diagnostic methods. Genitourin Med 1995;71:407-9.  Back to cited text no. 19
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]


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