Prevalence of co-existent COVID-19-associated pulmonary aspergillosis (CAPA) and its impact on early mortality in patients with COVID-19-associated pulmonary mucormycosis (CAPM).

BACKGROUND: Data on mixed mould infection with COVID-19-associated pulmonary aspergillosis (CAPA) and COVID-19-associated pulmonary mucormycosis (CAPM) are sparse. OBJECTIVES: To ascertain the prevalence of co-existent CAPA in CAPM (mixed mould infection) and whether mixed mould infection is associated with early mortality (≤7 days of diagnosis). METHODS: We retrospectively analysed the data collected from 25 centres across India on COVID-19-associated mucormycosis. We included only CAPM and excluded subjects with disseminated or rhino-orbital mucormycosis. We defined co-existent CAPA if a respiratory specimen showed septate hyphae on smear, histopathology or culture grew Aspergillus spp. We also compare the demography, predisposing factors, severity of COVID-19, and management of CAPM patients with and without CAPA. Using a case-control design, we assess whether mixed mould infection (primary exposure) were associated with early mortality in CAPM. RESULTS: We included 105 patients with CAPM. The prevalence of mixed mould infection was 20% (21/105). Patients with mixed mould infection experienced early mortality (9/21 [42.9%] vs. 15/84 [17.9%]; p = 0.02) and poorer survival at 6 weeks (7/21 [33.3] vs. 46/77 [59.7%]; p = 0.03) than CAPM alone. On imaging, consolidation was more commonly encountered with mixed mould infections than CAPM. Co-existent CAPA (odds ratio [95% confidence interval], 19.1 [2.62-139.1]) was independently associated with early mortality in CAPM after adjusting for hypoxemia during COVID-19 and other factors. CONCLUSION: Coinfection of CAPA and CAPM was not uncommon in our CAPM patients and portends a worse prognosis. Prospective studies from different countries are required to know the impact of mixed mould infection.

Risk factors, mortality, and predictors of survival in COVID-19-associated pulmonary mucormycosis: a multicentre retrospective study from India.

OBJECTIVES: To compare COVID-19-associated pulmonary mucormycosis (CAPM) with COVID-19-associated rhino-orbital mucormycosis (CAROM), ascertain factors associated with CAPM among patients with COVID-19, and identify factors associated with 12-week mortality in CAPM. METHODS: We performed a retrospective multicentre cohort study. All study participants had COVID-19. We enrolled CAPM, CAROM, and COVID-19 subjects without mucormycosis (controls; age-matched). We collected information on demography, predisposing factors, and details of COVID-19 illness. Univariable analysis was used to compare CAPM and CAROM. We used multivariable logistic regression to evaluate factors associated with CAPM (with hypoxemia during COVID-19 as the primary exposure) and at 12-week mortality. RESULTS: We included 1724 cases (CAPM [n = 122], CAROM [n = 1602]) and 3911 controls. Male sex, renal transplantation, multimorbidity, neutrophil-lymphocyte ratio, intensive care admission, and cumulative glucocorticoid dose for COVID-19 were significantly higher in CAPM than in CAROM. On multivariable analysis, COVID-19-related hypoxemia (aOR, 2.384; 95% CI, 1.209-4.700), male sex, rural residence, diabetes mellitus, serum C-reactive protein, glucocorticoid, and zinc use during COVID-19 were independently associated with CAPM. CAPM reported a higher 12-week mortality than CAROM (56 of the 107 [52.3%] vs. 413 of the 1356 [30.5%]; p = 0.0001). Hypoxemia during COVID-19 (aOR [95% CI], 3.70 [1.34-10.25]) and Aspergillus co-infection (aOR [95% CI], 5.40 [1.23-23.64]) were independently associated with mortality in CAPM, whereas surgery was associated with better survival. DISCUSSION: CAPM is a distinct entity with a higher mortality than CAROM. Hypoxemia during COVID-19 illness is associated with CAPM. COVID-19 hypoxemia and Aspergillus co-infection were associated with higher mortality in CAPM.

Mucormycosis in Human Immunodeficiency Virus-Infected Individuals: A Systematic Review of Case Reports.

Mucormycosis in human immunodeficiency virus (HIV) infection is uncommon; notably, many cases have additional predisposing factors. Whether mucormycosis differs in HIV-affected individuals with and without additional risk factors (e.g., neutropenia, diabetes mellitus, and transplantation) remains unclear. In this systematic review, we identified 94 cases of HIV and mucormycosis classifiable into three groups: (1) HIV with additional risk factors (n = 50), (2) intravenous drug users (IVDU, n = 24), and (3) no other risk factor (n = 19) for mucormycosis. The most common presentation in IVDU was renal (41.7%) and cerebral mucormycosis (39.2%), whereas rhino-orbital mucormycosis (ROM, 4.2%) was uncommon. In the other two groups, ROM was the most common presentation. Rhizopus was the most frequently isolated Mucorales; however, in IVDU, Lichtheimia was the most common. The overall mortality was 53% and not significantly different in the three groups. Mucormycosis in HIV-infected individuals is rare without additional risk factors or IVDU.

Ibrutinib and tracheal mucormycosis: A case report and systematic review of literature.

Ibrutinib, a Bruton tyrosine kinase (BTK) inhibitor, has been approved for various hematological malignancies. Invasive aspergillosis is a known complication of ibrutinib, but mucormycosis is rare. We describe the case of a 70-year-old man with mantle cell lymphoma infiltrating the trachea, managed with a tracheobronchial stent and ibrutinib. He had improved one month after treatment, and we removed the airway stent. Four months later, he developed tracheal nodules confirmed to be tracheal mucormycosis and responded to liposomal amphotericin B (3.5 g) followed by posaconazole. After transient improvement, the tracheal lesions recurred, the biopsy showed lymphoma (with no evidence of mucormycosis), and he died. A systematic review of the literature identified 20 additional cases of ibrutinib-associated mucormycosis. Most of the 21 patients included were men (95%), and ibrutinib was the only risk factor in 15.7%. The reported mortality was 31.6% (6/19), attributable to mucormycosis in half the cases.

Risk factors for pulmonary mucormycosis in subjects with diabetes mellitus-A case-control study.

BACKGROUND: Factors associated with pulmonary mucormycosis (PM) among subjects with diabetes mellitus (DM) remain unclear. Following the coronavirus disease (COVID-19)-associated mucormycosis outbreak in India, specific environmental exposures (especially cattle dung exposure) were proposed as possible aetiology. We hypothesized that environmental factors are associated with PM. We compared subjects with DM with (cases) and without PM (controls). METHODS: In this case-control study, for each PM case, we included five unmatched diabetic controls (hospital [n = 2], community [n = 3]) without PM. We collected information on demography, COVID-19 infection, glycated haemoglobin% (HbA1c), the type of house (pucca vs. kutcha) where the participants reside, and other environmental factors. The primary exposure tested was cattle dung exposure (CDE; using cattle dung cakes as fuel or cattle handling). We performed a multivariate logistic regression to explore factors associated with PM and report the association as an adjusted odds ratio (OR) with 95% confidence intervals (CI). RESULTS: We enrolled 39 PM cases and 199 controls (hospital [n = 80], community [n = 119]). CDE (OR 0.68, 95% CI [0.14-3.31]; p = 0.63) was not associated with increased PM in DM. We found male sex (OR 4.07, 95% CI [1.16-14.31]), higher HbA1c (OR 1.51, 95% CI [1.18-16.32]), COVID-19 (OR 28.25, 95% CI [7.02-113.6]) and residence at kutcha house (OR 4.84, 95% CI [1.33-17.52]) associated with PM. CONCLUSION: Cattle dung exposure was not associated with PM in subjects with DM. Instead, male sex, poor glycaemic control, COVID-19 and the type of housing were associated with pulmonary mucormycosis.

Treatment of pulmonary mucormycosis with adjunctive nebulized amphotericin B (MUCONAB trial): Results of an open-label randomized controlled trial.

BACKGROUND: The role of nebulized amphotericin B (NAB) in managing pulmonary mucormycosis (PM) is unknown. METHODS: In this open-label trial, we randomized PM subjects to receive either intravenous liposomal amphotericin B (control arm, 3-5 mg/kg/day) alone or along with nebulized amphotericin B deoxycholate (NAB, 10 mg twice a day, every alternate day). The primary outcomes were: (1) overall response ('success' [complete or partial response] or 'failure' [stable disease, progressive disease, or death]) at 6 weeks; and (2) the proportion of subjects with adverse events (AE). The key secondary outcome was 90-day mortality. We performed a modified intention-to-treat (mITT) analysis where we included only subjects receiving at least a single dose of NAB. RESULTS: Fifteen and 17 subjects were randomized to the control and NAB arms; two died before the first dose of NAB. Finally, we included 30 subjects (15 in each arm; mean age 49.8 years; 80% men) for the mITT analysis. Diabetes mellitus (n = 27; 16/27 were COVID-19-associated PM) was the most common predisposing factor. The overall treatment success was not significantly different between the control and the NAB arms (71.4% vs. 53.3%; p = .45). Twenty-nine subjects experienced any AE, but none discontinued treatment. The 90-day mortality was not significantly different between the control (28.6%) and NAB arm (53.3%; p = .26). CONCLUSION: Adjunctive NAB was safe but did not improve overall response at 6 weeks. A different dosing schedule or nebulized liposomal amphotericin B may still need evaluation. More research is needed to explore other treatment options for PM.

Prevalence of Aspergillus Sensitization and Allergic Bronchopulmonary Aspergillosis in Adults With Bronchial Asthma: A Systematic Review of Global Data.

BACKGROUND: The prevalence of allergic bronchopulmonary aspergillosis (ABPA) in asthmatic patients remains unclear and is likely different across geographic locales. OBJECTIVE: To systematically review the literature for estimating the prevalence of Aspergillus sensitization (AS) and ABPA in adults with bronchial asthma. METHODS: We searched the PubMed and Embase databases for studies reporting the prevalence of AS or ABPA in at least 50 asthmatic subjects. The primary outcome was to assess the prevalence of ABPA. The secondary outcome was to evaluate the prevalence of AS in asthma and that of ABPA in asthma with AS. We pooled the prevalence estimates using a random-effects model and examined the factors influencing the prevalence using multivariate meta-regression. RESULTS: Of the 11,801 records retrieved, 86 studies with 25,770 asthmatic subjects met the inclusion criteria. Most of the studies were from tertiary care centers. The pooled prevalence of ABPA in asthma (47 studies; 9822 asthmatic subjects) was 11.3% (95% CI, 8.7-14.2). The pooled prevalence of AS in asthma (73 studies; 23,003 asthmatic subjects) was 25.1% (95% CI, 20.5-30.0), whereas the prevalence of ABPA in AS (36 studies; 2954 asthmatic subjects) was 37.0% (95% CI, 27.9-46.6). Multivariate meta-regression identified studies published from India (odds ratio, 1.11; 95% CI, 1.01-1.23) as the only factor associated with higher ABPA prevalence. There was presence of significant statistical heterogeneity and publication bias. CONCLUSIONS: We found a high prevalence of ABPA in adult asthmatic subjects, underscoring the need for screening for ABPA in all asthmatic subjects seeking tertiary care.

Aspergillus Sensitization and Allergic Bronchopulmonary Aspergillosis in Asthmatic Children: A Systematic Review and Meta-Analysis.

Background: The prevalence of aspergillus sensitization (AS) and allergic bronchopulmonary aspergillosis (ABPA) in asthmatic children remains unclear. Objective: To systematically review the literature to estimate the prevalence of AS and ABPA in children with bronchial asthma. Methods: We searched the PubMed and Embase databases for studies reporting the prevalence of AS or ABPA in pediatric asthma. The primary outcome was to assess the prevalence of AS, while the secondary outcome was to evaluate the prevalence of ABPA. We pooled the prevalence estimates using a random effects model. We also calculated the heterogeneity and publication bias. Results: Of the 11,695 records retrieved, 16 studies with 2468 asthmatic children met the inclusion criteria. Most studies were published from tertiary centers. The pooled prevalence of AS in asthma (15 studies; 2361 subjects) was 16.1% (95% confidence intervals [CI], 9.3-24.3). The prevalence of AS was significantly higher in prospective studies, studies from India, and those from developing countries. The pooled prevalence of ABPA in asthma (5 studies; 505 children) was 9.9% (95% CI, 0.81-27.6). There was significant heterogeneity and publication bias for both outcomes. Conclusions: We found a high prevalence of AS and ABPA in asthmatic children. There is a need for community-based studies from different ethnicities using a standard methodology to ascertain the true prevalence of AS and ABPA in pediatric asthma.

Could cattle dung burning have contributed to the epidemic of COVID-19-associated mucormycosis in India? Results of an experimental aero-mycological study.

BACKGROUND: Several hypotheses have been proposed for explaining the outbreak of coronavirus disease 2019 (COVID-19)-associated mucormycosis in India, including the burning of cattle dung cakes, though no study has yet been conducted to support this claim. METHODS: We conducted an aero-mycological study to evaluate whether Mucorales in the air increased during or after burning cattle dung cakes. We further compared the growth of Mucorales in the indoor air samples from houses with and without cattle. We also cultured fresh and dried cattle dung and soil samples for Mucorales. RESULTS: We noted no significant difference in the proportion of air samples growing Mucorales during (4/22 [18.2%]) and after (3/2 [13.6%]) cattle dung burning than that collected immediately before (4/22 [18.2%]). Mucorales were isolated in 15.4% of the indoor air samples obtained from different houses (both rural and urban); the proportion of samples growing Mucorales was not significantly different in households with and without cattle. We also observed growth of Mucorales in 6 of the 8 [75%] fresh and 3 of the 6 [50%] dried dung samples. The most common Mucorales isolated from soil and dung samples was Lichtheimia corymbifera, while Rhizopus arrhizus was the most common species isolated from indoor air samples. CONCLUSIONS: We found no significant increase in the proportion of air samples growing Mucorales during or after burning cattle dung cake than that before. It seems unlikely that cattle dung burning contributes to the occurrence of mucormycosis.

Definition, diagnosis, and management of COVID-19-associated pulmonary mucormycosis: Delphi consensus statement from the Fungal Infection Study Forum and Academy of Pulmonary Sciences, India.

COVID-19-associated pulmonary mucormycosis (CAPM) remains an underdiagnosed entity. Using a modified Delphi method, we have formulated a consensus statement for the diagnosis and management of CAPM. We selected 26 experts from various disciplines who are involved in managing CAPM. Three rounds of the Delphi process were held to reach consensus (≥70% agreement or disagreement) or dissensus. A consensus was achieved for 84 of the 89 statements. Pulmonary mucormycosis occurring within 3 months of COVID-19 diagnosis was labelled CAPM and classified further as proven, probable, and possible. We recommend flexible bronchoscopy to enable early diagnosis. The experts proposed definitions to categorise dual infections with aspergillosis and mucormycosis in patients with COVID-19. We recommend liposomal amphotericin B (5 mg/kg per day) and early surgery as central to the management of mucormycosis in patients with COVID-19. We recommend response assessment at 4-6 weeks using clinical and imaging parameters. Posaconazole or isavuconazole was recommended as maintenance therapy following initial response, but no consensus was reached for the duration of treatment. In patients with stable or progressive disease, the experts recommended salvage therapy with posaconazole or isavuconazole. CAPM is a rare but under-reported complication of COVID-19. Although we have proposed recommendations for defining, diagnosing, and managing CAPM, more extensive research is required.

As the virus sowed, the fungus reaped! A comparative analysis of the clinico-epidemiological characteristics of rhino-orbital mucormycosis before and during COVID-19 pandemic.

BACKGROUND: The sudden surge of mucormycosis cases which happened during the second wave of COVID-19 pandemic was a significant public health problem in India. OBJECTIVES: The aim of this study was to analyse the clinico-epidemicological characteristics of the mucormycosis cases to determine the changes that had occurred due to COVID-19 pandemic. METHODOLOGY: A retrospective cross-sectional study was conducted at the Department of Otolaryngology Head and Neck Surgery, PGIMER, Chandigarh, India. Patients diagnosed with rhino-orbital mucormycosis were categorised into the following groups: Pre-pandemic(May 2019 to April 2020), Pandemic Pre-epidemic (May 2020 to April 2021) and Epidemic (1 May 2021 to 12 July 2021). The epidemiological, clinical and surgical data of all the patients were retrieved from the hospital records and analysed. RESULTS: The epidemic period had 370 cases, compared with 65 during pandemic period and 42 in the pre-pandemic period. Diabetes mellitus was seen in 87% of cases during epidemic period, 92.9% in the pre-pandemic period and 90.8% in the pre-pandemic pre-epidemic period. The proportion of patients suffering from vision loss, restricted extra-ocular movements, palatal ulcer and nasal obstruction was higher in the pre-epidemic groups, and the difference was significant (p, <.01). There was no history of oxygen use in 85.9% of patients and no steroid use in 76.5%. The death rates were the lowest during epidemic (10%). CONCLUSION: COVID-19 has caused a statistically significant increase in the number of mucormycosis infections. The mortality and morbidity which showed an increase during the first wave of COVID-19 decreased significantly during the epidemic period.

Pediatric case of conidiobolomycosis: A rare entity.

Conidiobolomycosis caused by Conidiobolus species is an uncommon infection restricted to tropical and subtropical regions, usually affecting immunocompetent individuals. More than half of pediatric cases of conidiobolomycosis across the globe are from India. We report a case of subcutaneous conidiobolomycosis in an adolescent with development delay who responded to combined therapy with itraconazole and saturated solution of potassium iodide.

Connecting the Dots: Interplay of Pathogenic Mechanisms between COVID-19 Disease and Mucormycosis.

Coronavirus disease (COVID-19)-associated mucormycosis (CAM) is an emerging threat globally, especially in India. More than 40,000 CAM cases have been reported in India. The emergence of CAM cases in India has been attributed to environmental, host, and iatrogenic factors. Mucorales spore burden has been reported globally; however, their presence is higher in tropical countries such as India, contributing to the emergence of CAM. Before the COVID-19 pandemic, patients with diabetes mellitus, haematological malignancies, solid organ transplants, corticosteroid therapy and neutropenia were more prone to mucormycosis, whereas in COVID-19 patients, virus-induced endothelial dysfunction, hyperglycaemia, and immune dysfunction following corticosteroid use increase the risk of acquiring mucormycosis. The interaction of Mucorales spores with the epithelial cells, followed by endothelial invasion, is a crucial step in the pathogenesis of mucormycosis. Endothelial damage and increased endothelial receptor expression induced by COVID-19 infection may predispose patients to CAM. COVID-19 infection may directly induce hyperglycaemia by damaging beta cells of the pancreas or by corticosteroid therapy, which may contribute to CAM pathogenesis. Iron acquisition from the host, especially in diabetic ketoacidosis (DKA) or deferoxamine therapy, is an important virulence trait of Mucorales. Similarly, the hyperferritinaemia caused by COVID-19 may act as a source of iron for Mucorales growth and invasion. In addition, corticosteroid treatment reduces or abolishes the innate immune functions of phagocytic cells contributing to the pathogenesis of CAM. This review aims to discuss primarily the host and iatrogenic factors shared between COVID-19 and mucormycosis that could explain the emergence of CAM.

Cunninghamella arunalokei a New Species of Cunninghamella from India Causing Disease in an Immunocompetent Individual.

Mucormycosis due to Cunninghamella spp. is a rare disease, especially in immunocompetent individuals. Here, we describe the isolation and characterization of a new species of Cunninghamella, causing chronic rhino-orbital-cerebral disease, and review cases of mucormycosis due to Cunninghamella spp. in immunocompetent individuals. The Basic Local Alignment Search Tool (BLAST) analysis of the internal transcribed spacer region (ITS) sequence of isolate NCCPF 890012 showed 90% similarity with Cunninghamella bigelovii, while the large ribosomal subunit (28S) and translation elongation factor-1 alpha (EF-1 alpha) gene sequences showed 98% identity. Further, the phylogenetic analysis with concatenated sequences clustered isolate (NCCPF 890012) closely with C. bigelovii. The ITS sequence showed the maximum variation among three genes analyzed and helped in the new species' delineation. Comparison of the assembled whole genome of NCCPF 890012 with other Mucorales using 123 single-copy orthologous genes showed clustering within the genus Cunninghamella. Based on these findings, the isolate is considered to be a new species of Cunninghamella and designated as Cunninghamella arunalokei sp. nov. Despite repeated debridement and antifungal treatment, the patient had multiple recurrences with intracranial extension and succumbed to the illness.

Clinical profile, antifungal susceptibility, and molecular characterization of Candida auris isolated from patients in a South Indian surgical ICU.

BACKGROUND: Candida auris is an emerging multidrug resistant yeast which causes blood stream infection especially among critically ill patients. This yeast can also colonize patients and are isolated from hospital environment causing outbreaks in hospital settings. OBJECTIVE: To describe possible outbreak of C. auris infection in surgical ICU and characterize the isolates by molecular typing and azole resistance mechanism. METHODS: After isolation of Candida auris from cluster of patients from surgical ICU, environment survey was done to identify the source in the hospital. The identity of the isolates was confirmed by Matrix Assisted Laser Desorption Ionisation Time of Flight mass spectroscopy and sequencing 26S and ITS region of rDNA. Molecular typing was done by fluorescent amplified fragment length polymorphism technique. Antifungal susceptibility testing was performed by CLSI broth dilution technique. ERG11 gene was sequenced to screen for mutations responsible for azole resistance. RESULTS AND CONCLUSION: A total of eight C. auris was isolated during the four months (December 2018-March 2019) suggesting possible of outbreak in surgical ICU of tertiary care center in South India. C. auris (n = 8) was isolated from urine (n = 4), blood (n = 3) and ear discharge (n = 1) samples. Based on 26S sequence analysis all our isolates belonged to South Asian clade. All the isolates had minimum inhibitory concentration (MIC) of ≥16 µg/ml to fluconazole. ERG11 sequence exhibited amino acid substitution Y132F in all the isolates. The two environmental isolates clustered closely with an isolate from urine sample. Adherence to strict infection control practices prevented further spread of infection.

Fungaemia due to rare yeasts in paediatric intensive care units: A prospective study.

BACKGROUND: Considering the emergence of fungaemia due to rare yeasts at our centre, we performed a systematic epidemiologic study on fungaemia due to rare yeast. OBJECTIVES: We undertook the present prospective observational study to explore the epidemiological features and clinical characteristics of fungaemia due to rare yeasts in paediatric ICUs at our centre. METHODS: The successive yeasts isolated from blood at our PICUs during December 2017 through March 2019 were identified by molecular methods. Fungaemia due to yeasts other than C. albicans, C. tropicalis, C. glabrata, C. krusei and C. parapsilosis was categorised as rare yeasts. Antifungal susceptibility testing of the yeast isolates was performed as per clinical and laboratory standards institute (CLSI) guidelines. We also compared different clinical parameters of fungaemia due to common versus rare yeasts, and rare yeasts in neonates versus non-neonates. RESULTS: During the study period, 212 yeast isolates were obtained from 159 patients at PICUs of our hospital, and 127 isolates from 98 patients (61.6%) were categorised as rare yeasts. Neonates acquired fungaemia significantly earlier after ICU admission than non-neonates (median:4 vs 6 days; p = .005). Regarding epidemiology study of rare yeast fungaemia, Wickerhamomyces anomalus (43.8%) and Candida utilis (40.8%) were common isolates; surgical intervention and gastrointestinal disease were significantly associated; overall, azole, echinocandin and amphotericin B resistance was at 9.1%, 1.02% and 1.02%, respectively; overall mortality was 65.3%. CONCLUSIONS: The emergence of rare yeasts especially W. anomalus and C. utilis causing fungaemia in our children demands urgent attention to control the spread.

Mycosis of the Plantar Surface of Foot Owing to Nondermatophyte Mold Nodulisporium griseobrunneum Mimicking a Tinea Pedis.

Nondermatophyte molds (NDM) and dematiaceous molds are less frequently implicated as the etiological agents of tinea-like infections of the foot. Among the etiological agents, Hendersonula toruloidea (now, Nattrassia mangiferae), Scytalidium hyalinum, Alternaria species (spp.), and Fusarium spp. are infrequently associated with foot mycoses. Nodulisporium (N.) spp. is a mitosporic NDM, which has been implicated in human infections like cerebral phaeohyphomycosis and allergic fungal sinusitis. Here, we report N. griseobrunneum in a 9-year-old female with mycosis of the plantar surface of foot mimicking a tinea pedis. Potassium hydroxide mount of skin specimen demonstrated dichotomous branching septate hyphae. Fungal culture and molecular sequencing established N. griseobrunneum as the etiological agent. Antifungal susceptibility testing revealed lower MICs to all seven drugs tested including itraconazole (ITR). The patient was treated with ITR and topical terbinafine. To the best of our knowledge, this is the first communication depicting molecular confirmation of the etiologic agent and antifungal susceptibility data of the mycosis of the plantar surface of foot owing to N. griseobrunneum from India.