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ORIGINAL ARTICLE Table of Contents  
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Phaeohyphomycosis: A study from tertiary health care center in North India


1 Department of Microbiology, Government Medical College Hospital, Chandigarh, India
2 Department of Pathology, Government Medical College Hospital, Chandigarh, India
3 Department of General Surgery, Government Medical College Hospital, Chandigarh, India

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Date of Submission23-Feb-2021
Date of Decision22-Oct-2021
Date of Acceptance25-Oct-2021
Date of Web Publication06-Jun-2022
 

   Abstract 


Objectives: Phaeohyphomycosis refers to infections caused by phaeoid/dematiaceous or darkly pigmented fungi. This study was undertaken to further increase our knowledge about the incidence of phaeohyphomycosis and its causative agents. Methods: The present study was conducted over a period of one and a half years (January 2018–June 2019) on specimens received from patients with varied clinical manifestations ranging from superficial infections, subcutaneous cysts, pneumonia, brain abscess to a disseminated infection. These specimens were processed in the Department of Microbiology for potassium hydroxide (KOH) examination and culture and in Pathology for cytology/histopathological examination (HPE). All specimens positive on direct examination for dark grey, brown or black fungi were included in the study. Results: A total of 20 specimens were confirmed as phaeohyphomycosis. Most of the patients belonged to the age group of 41 to 50 years. Male: Female ratio was 2.3:1. Trauma was the most common risk factor. Spectra of the isolated fungal pathogens comprised of Bipolaris species, Exophiala species, Curvularia geniculata, Phialemonium species, Daldinia eschscholtzii, Hypoxylon anthochroum, Phaeoacremonium species, Leptosphaerulina australis, Medicopsis romeroi, Lasiodiplodia theobromae, Eutypella species, Chaetomium globosum, Alternaria species, Cladophialophora bantiana and 2 unidentified dematiaceous fungi. Recovery from phaeohyphomycosis was seen in 12 patients, 7 were lost to follow up and one patient succumbed to the illness. Conclusion: Infections caused by phaeoid fungi can no longer be viewed as rare. In fact, phaeohyphomycosis can have myriad of presentations spanning from mild cutaneous infections to fatal brain disease. Therefore, a high index of clinical suspicion is needed to diagnose such infections. The primary treatment modality remains surgical removal of the lesion in cutaneous or subcutaneous infections however disseminated disease with a guarded prognosis requires aggressive management.

Keywords: Dematiaceous fungi, fungal pathogens, India, phaeohyphomycosis


How to cite this URL:
Dhawan P, Singla N, Kundu R, Gulati N, Attri AK, Chander J. Phaeohyphomycosis: A study from tertiary health care center in North India. Indian J Pathol Microbiol [Epub ahead of print] [cited 2023 Jan 29]. Available from: https://www.ijpmonline.org/preprintarticle.asp?id=346688





   Introduction Top


Phaeohyphomycosis refers to infections caused by dematiaceous/phaeoid or darkly pigmented fungi that are different from others due to the presence of melanin in their cell wall.[1] The term phaeohyphomycosis refers to superficial, cutaneous, subcutaneous or systemic infections caused by phaeoid fungi in which tissue forms, both pigmented and filamentous are seen.[2] It needs to be distinguished from other conditions associated with dematiaceous fungi especially chromoblastomycosis, which is recognized by the presence of sclerotic bodies.[3] Over 150 species and 70 genera of dematiaceous fungi have been implicated to cause disease in humans and animals.[2] In tissue, they appear brown in unstained preparations and on Hematoxylin & eosin (H&E) staining. The Masson-Fontana stain (MF), which is specific for melanin stains the fungal profiles brownish-black.

Most common clinical presentation of these fungi is a subcutaneous infection following deep inoculation of fungus into the subcutaneous tissues. Lesions are primarily found on feet, legs, hands, arms, and back and appear as subcutaneous nodules, which are often palpable. Systemic infection occurring in the form of cerebral abscesses is rare but fatal if untreated and is mainly reported from immunocompetent individuals.[4] The preliminary diagnosis of phaeohyphomycosis is made via direct microscopic examination of clinical specimen with potassium hydroxide (KOH) wet mount, calcofluor white staining and fungal culture. Special stains like Masson-Fontana stain are used to elicit the presence of melanin in order to substantiate the diagnosis of phaeohyphomycosis.[5] Molecular tests hold the key to confirmation of genus and species involved. Recently, matrix-assisted laser desorption ionization––time of flight mass spectrometry (MALDI-TOF MS) has also been successfully used to establish etiological agents in phaeohyphomycosis.[6] Treatment mostly involves local excision especially in cases of subcutaneous phaeohyphomycosis while invasive infections warrant use of intravenous amphotericin B or azoles with or without surgical intervention.[3] Ulcerative lesions of skin and soft tissue without a cyst can be effectively managed with debridement.[7]

In our institution, as the awareness on phaeohyphomycosis is gradually increasing, more and more cases are being recognized. Therefore, the present study was undertaken to further enhance our knowledge about the incidence of phaeohyphomycosis and its causative agents in our geographic location.


   Material and Methods Top


The present prospective study was conducted in the Department of Microbiology, in collaboration with the Departments of Pathology and General Surgery during the time period January 2018–June 2019. The study protocol was duly approved by the Institutional ethics committee. All the patients with infection ranging from superficial infection, subcutaneous cyst, allergic disease, pneumonia, brain abscess to disseminated infection in whom dark yellow or brown colored septate, tortuous hyphae with irregular branching seen either on direct KOH mount or cytology/histopathology were taken as cases suspected of phaeohyphomycosis.

Various specimens received from these patients were in accordance to the site of lesion such as skin biopsy/fine needle aspirates from cutaneous lesions, nasal discharges, scrapings and aspirates from sinuses in patients with rhinocerebral lesions. Sputum, bronchoalveolar lavage (BAL) and transbronchial biopsy were received from patients having pulmonary lesions. In cases of ocular involvement specimens like corneal scraping, vitreous tap, aqueous tap, entire eye ball, eye discharge, pus/discharge from lacrimal sac, etc., were received. Varied samples were received in cases with disseminated disease. The biopsy material from clinically suspected cases of phaeohyphomycosis was collected in two sterile containers containing normal saline and 10% formalin and were processed in the Departments of Microbiology and Pathology, respectively. A detailed case history, examination and other relevant workup was done for all the positive cases. All the patients were followed up for the duration of study period.

The cytological/histopathological examination for all the specimens was carried out using May-Grünwald Giemsa (MGG)/hematoxylin and eosin (H&E) and periodic acid-Schiff (PAS). Grocott's methenamine silver (GMS) and Masson-Fontana (MF) stains were done wherever required. Specimens for direct examination and fungal culture were processed in Mycology laboratory, Department of Microbiology as per the standard mycological procedures. Direct examination as KOH mount was done for all the specimens followed by fungal culture on Sabouraud's dextrose agar (SDA). Two tubes of SDA with antibiotics (with chloramphenicol and gentamicin, without cycloheximide) and two tubes of SDA (with antibiotics and cycloheximide) were put up simultaneously. One tube of each type was incubated at 37°C and 25°C. Once the growth was obtained, lactophenol cotton blue (LCB) mount was made to identify the fungus. Slide cultures were put on cornmeal agar/oat meal agar to enhance sporulation of the fungal isolates whenever needed. Certain strains wherein identification was not possible by the above methods, were identified by molecular methods done at the National Culture Collection of Pathogenic Fungi (NCCPF), Mycology Division, Post Graduate Institute of Medical Education and Research (PGIMER), Chandigarh, India.

All the mycelia samples sent to NCCPF were subcultured on to SDA. Any growth obtained was identified both macroscopically and microscopically. The conidia were then inoculated into Sabouraud dextrose broth and incubated at 37°C in an incubator shaker with shaking at 150 rotations per minute. Fungal balls generated were used for deoxy-ribonucleic acid (DNA) extraction by manual phenol chloroform isoamyl alcohol method. Extracted DNA was quantified using Nanodrop 2000 spectrophotometer (Thermo Fischer Scientific, Wilmington, DE, USA). Internal transcribed spacer region (ITS) of ribosomal DNA was amplified using ITS-5 (5'- GGAAGTAAAAGTCGTAACAAGG-3') and ITS-4 (5'-TCCTCCGCTTATTGATATGC- 3') primers. For a reaction volume of 25 μl, 2.5 μl of the 1:10 diluted genomic DNA, and 0.5 mM of each primer were added. Polymerase chain reaction (PCR) product were amplified with the following temperature profiles; denaturation for 5 minutes at 94°C, followed by 35 cycles of 30 seconds at 95°C, 1 minute at the annealing temperature of 56°C followed by final extension for 5 minutes at 72°C. Sequencing PCR was carried out using Big Dye Terminator Cycle Sequencing Kit Version 1.1 (Applied Biosystem, Foster city, CA, USA) as per the manufacturer's protocol. For each gene fragment, both the positive strand and the negative strand were sequenced using both forward and reverse primer respectively. Amplicons were subjected to sequencing using 3500 ABI sequencers using the respective primers. The sequences were subjected to BLAST analysis in the GenBank online portal (https://blast.ncbi.nlm.nih.gov/). A total of seven isolates where no sporulation could be induced/not identified phenotypically even to genus level, were identified by molecular methods. It was not possible to send all isolates for molecular identification due to logistic reasons.


   Results and Observations Top


A total of 10541 specimens were received in the mycology laboratory during the study period of which 20 specimens were finally concluded to be from patients of phaeohyphomycosis. The overall incidence of phaeohyphomycosis in the present study was 0.2% or 2 cases per 1000 patients. The age distribution of cases shows age group 41-50 years to be the most affected. The mean age of the patients was 46.6 years and the median age was 50 years. The minimum age of presentation was 18 years while the maximum was 75 years. Fourteen (70%) male and 6 (30%) female patients were diagnosed as having phaeohyphomycosis. Among these patients maximum were housewives 5 (25%) followed by clerks 5 (25%), farmers 3 (15%), students 3 (15%) and 4 (20%) were engaged in other occupations. The clinical manifestations were of a cyst/abscess/nodule involving subcutaneous tissue in 9 (45%) cases, rhinosinusitis in 3 (15%) cases, nasal stuffiness in 2 (10%) cases while cutaneous ulceration with subcutaneous tissue involvement was seen in 3 (15%) cases. Headache, corneal ulcer and shortness of breath & cough were observed in one case each. History of trauma was forthcoming in 9 (45%) cases while 5 cases (25%) had diabetes mellitus.

Amongst the specimens received, 8 (40%) were tissue specimens, 5 (25%) were pus, 5 (25%) were Ear Nose Throat (ENT) specimens like nasal crust, fungal muck from maxillary sinus, infected polyp and one each of corneal scrapping and bronchoalveolar lavage. All the specimens were examined using KOH wet mount. Out of these 16 (80%) were KOH positive [Figure 1], all of which showed septate hyphae and 4 (20%) specimens negative on KOH were positive on histopathology. Masson-Fontana stain was performed on 11 specimens as other specimens were not adequate in quantity. It was positive in 7 (63.6%) cases and negative in 4 (36.4%). Among the 20 specimens that were found to be positive for fungal etiology, 19 (95%) were culture positive. Mycelial isolates grew after 7-14 days of incubation.
Figure 1: a Magnetic resonance imaging scan showing large heterogeneous space occupying lesion in the right frontal lobe. b. Subcutaneous nodule on the left medial malleolus in a patient with subcutaneous phaeohyphomycosis. C. Non contrast computed tomography scan showing deviation of nasal septum to the left and a soft tissue density in the left maxillary sinus with air fluid level. d. Section from brain abscess tissue showing brown septate hyphae (MF × 400). e. Tortuous and pigmented septate hyphae in wet mounts of pus specimens (KOH × 400). f. Tortuous septate hyphae seen in the smear from pus aspirated from subcutaneous nodule on the foot (MGG × 1000). g. Tortuous septate hyphae seen in tissue section from brain abscess (PAS × 400). h. Growth on SDA showing black mycelial colonies of Bipolaris spp. on obverse view. i. Reverse view of growth of Bipolaris spp. on SDA showing distinctive blackish pigment diffusing into medium. j. Alternaria spp. showing muriform conidia with horizontal and transverse septae (LCB × 400). k. Curvularia spp showing sympodially-arranged conidia with curving of the third cell from the base (LCB × 400). l. Growth on SDA showing black mycelial colonies of Cladophialophora bantiana on obverse view. m. Bipolaris spp. showing sympodially-arranged conidia (LCB × 400). n. Chaetomium globosum showing densely hairy, egg shaped fruiting body (perithecium) (LCB × 400)

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The spectra of fungal pathogens isolated comprised of Bipolaris species 4 (20%), Exophiala species 1 (5%), Curvularia geniculata 1 (5%), Phialemonium species 1 (5%), Daldinia eschscholtzii 1 (5%), Hypoxylon anthochroum 1 (5%), Phaeoacremonium species 1 (5%), Leptosphaerulina australis 1 (5%), Medicopsis romeroi 1 (5%), Lasiodiplodia theobromae 1 (5%), Eutypella species 1 (5%), Chaetomium globosum 1 (5%), Alternaria species 1 (5%), Cladophialophora bantiana 1 (5%) and 2 (10%) unidentified dematiaceous fungi. Of these various species of dematiaceous fungi isolated in this study, 7 species namely, D. eschscholtzii, H. anthochroum, L. australis, M. romeroi, L. theobromae, Eutypella species and C. globosum were identified by genetic sequencing.

In this study, most of the patients 14 (70%) were treated surgically [Table 1] (Surgical excision in 10 and Functional endoscopic sinus surgery, FESS in 4 cases) and no subsequent antifungals were given in them. Three were treated both medically (antifungal agents) and surgically. One patient with C. bantiana infection was treated surgically followed by oral voriconazole 200 mg twice a day for 2 weeks and another patient with corneal ulcer underwent debridement followed by topical natamycin eye drops 5% prescribed 6 times a day for 2 weeks. In patient with necrotizing infection lower limb, debridement with oral itraconazole were prescribed. A patient with pulmonary infection was treated with antifungal agents alone (liposomal amphotericin B). Two other patients were given treatment other than antifungal agents. One was with testicular malignancy on anticancer drugs. Other patient had electric burns in whom antibiotics were given. Overall, 12 (60%) patients recovered, one patient died and 7 were lost to follow up.
Table 1: Details of patients presenting with Phaeohyphomycosis (n=20)

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   Discussion Top


Phaeohyphomycosis constitutes infections with a diverse clinical spectrum. There are many isolated case reports of phaeohyphomycosis all over the world but handful of literature focusing on epidemiology and the disease pattern.[4],[8] In the present study, we tried to look for the incidence of phaeohyphomycosis in our geographic region and found it to be 0.2% or 2 cases per 1000 patients over a period of one and a half years. Phaeohyphomycosis may be reported at any age and in the present study, the age of the patients ranged from 18 years to 75 years. Maximum number of patients, 6 (30%) were in the age group of 41-50 years. This is comparable to other studies reported in the literature.[9],[10],[11] However, recently phaeohyphomycosis in pediatric patients has been described.[12] Hence it can be inferred that people at the age of maximum activity are affected the most, no age is debarred from getting the infection. We observed a male predilection with a male: female ratio of 2.3:1 which parallels other studies.[9],[10] On the contrary Ritter et al.[13] reported infections with a female predonderance. Generally, men are more exposed to outdoor activities, thereby increasing their vulnerability to the disease. Diabetes mellitus as a risk factor was seen in 5 (25%) cases in the current study.

The present study had 16 (80%) KOH positive specimens showing dark colored septate hyphae suggesting phaeophyphomycosis. Masson-Fontana stain was positive in 7 (7/11, 63.6%) cases, negative in 4 (4/11, 36.4%) cases and not performed in the rest 9 cases due to inadequate specimen quantity. In one case of allergic fungal rhinosinusitis, Masson-Fontana stain and other histopathological stains were positive for phaeoid hyphae and hyaline hyphae confirming a mixed infection. The utility of Masson-Fontana stain which is specific for melanin in confirming dematiaceous fungi has been highlighted earlier.[5] Our work proves the diagnostic usefulness of Masson-Fontana stain for dematiaceous fungi in cases of mixed infection and where the presentation is vague and confusing, leading to an inability to clinch an accurate diagnosis otherwise.

The clinical presentation of phaeohyphomycosis can be varied ranging from subcutaneous nodules to serious systemic infections like brain abscesses.[3] In this study most of the cases, 12 (60%) presented with cutaneous and/or subcutaneous involvement either as cyst, nodules or necrotizing infection. Researchers have reported cases of cutaneous and subcutaneous phaeohyphomycosis wherein trauma was the main source of infection.[14],[15] This infers that there might be inoculation of dematiaceous fungi following trauma leading to phaeohyphomycosis. Although a history of trauma may not always be elicited.[16] Many diverse genera have been identified to be causing infection in such patients. In the present study, although two of the isolates (could not be effectively revived to undergo genetic sequencing and identification) could not be identified, others causing infection were Bipolaris species, Exophiala species, Curvularia geniculata, Daldinia eschscholtzii, Phaeoacremonium species, Leptosphaerulina australis, Medicopsis romeroi, Phialemonium species, and Lasiodiplodia theobromae. These have been demonstrated in previous reports.[11],[17],[18] Cases of subcutaneous phaeohyphomycosis caused by L. theobromae and M. romeroi are on record.[19],[20] D. eschscholtzii, which is a wood-inhabiting fungus, has also been isolated from human specimens recently and identified using genome sequencing.[21]

Now-a-days fungal rhinosinusitis and paranasal sinus phaeohyphomycosis is being reported although the primary etiological agent in fungal rhinosinusitis is various Aspergillus species.[22],[23] We had 5 patients with ENT involvement. It is an indolent disease that may remain confined to the sinus cavity or spread to the adjoining structures. This process takes months to years. Another isolate Hypoxylon anthochroum on genetic sequencing was identified in a case with corneal ulcer. Human infections due to it have not been reported earlier.[24] In the present study, Alternaria was isolated from the BAL specimen in one case. Bipolaris, Curvularia have also been reported previously as agents causing allergic bronchopulmonary mycosis.[25] We isolated Cladophialophora bantiana from pus obtained in a case of cerebral abscess. Chakrabarti et al.[10] reported 124 cases of brain abscess due to C. bantiana mainly from Asian countries and almost 50% of these patients were from the Indian subcontinent. There have also been isolated case reports of cerebral phaeohyphomycosis caused by Fonsecaea monophora and Thielavia subthermophila.[26],[27]

In this study, most of the patients 14 (70%) were treated surgically in whom surgical excision (10 patients) and FESS (4 patients) was done. Three patients (15%) were treated both medically (antifungals) and surgically while medical treatment other than antifungals was given in 2 (10%) patients. One patient received antifungals alone. Overall, 12 (60%) patients recovered. One patient died (cerebral phaeohyphomycosis case) and 7 (35%) were lost to follow up due to various reasons. However, it will be prudent to mention here that the patients were followed up for the study period only and all those who are considered recovered actually means that they didn't have any recurrence in this particular period. Primary modality of treatment in subcutaneous phaeohyphomycosis is complete surgical excision. Successful treatment with surgical excision in subcutaneous phaeohyphomycosis without antifungals has been reported.[16] Incomplete removal or incision of involved tissues may result in recurrence. Treatment of choice for systemic phaeohyphomycosis includes both surgical resection and antifungals.

In conclusion, there is a need to lookout for more cases of phaeohyphomycosis. The incidence is increasing with diverse range of genera involved in causing infections. Cutaneous involvement is invariably mistaken for malignancy which can be extremely worrisome for the patient. Disseminated infections portend a bad prognosis being potentially life threatening. A high index of clinical suspicion, accurate diagnosis and prompt treatment are quintessential for favorable outcomes.

Acknowledgements

In this study, 7 species namely, Daldinia eschscholtzii, Hypoxylon anthochroum, Leptosphaerulina australis, Medicopsis romeroi, Lasiodiplodia theobromae, Eutypella species and Chaetomium globosum were identified by genetic sequencing done at the National Culture Collection of Pathogenic Fungi (NCCPF), Mycology Division, Post Graduate Institute of Medical Education and Research (PGIMER), Chandigarh, India for which we are thankful to Dr. Arunaloke Chakrabarti, Professor and Head, Department of Medical Microbiology, PGIMER, Chandigarh, India.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Correspondence Address:
Nidhi Singla,
Professor, Department of Microbiology, Government Medical College Hospital, Chandigarh 160 030
India
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijpm.ijpm_204_21



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