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ORIGINAL ARTICLE Table of Contents   
Year : 2008  |  Volume : 51  |  Issue : 4  |  Page : 493-496
Mycological profile of fungal sinusitis: An audit of specimens over a 7-year period in a tertiary care hospital in Tamil Nadu


1 Department of ENT, Christian Medical College and Hospital, Vellore 632 004, Tamil Nadu, India
2 Department of Microbiology, Christian Medical College and Hospital, Vellore 632 004, Tamil Nadu, India

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   Abstract 

Background: Fungi are being increasingly implicated in the etiopathology of rhinosinusitis. Fungal sinusitis is frequently seen in diabetic or immunocompromised patients, although it has also been reported in immunocompetent individuals. Invasive fungal sinusitis, unless diagnosed early and treated aggressively, has a high mortality rate. Aim: Our aim was to look at the mycological and clinical aspects of fungal sinusitis in a tertiary referral center in Tamil Nadu. Design: This is a retrospective audit conducted on fungal culture positive sinus samples submitted to the Microbiology department from January 2000 to August 2007. Relevant clinical and histopathological details were analysed. Results: A total of 211 culture-positive fungal sinusitis samples were analysed. Of these, 63% had allergic fungal sinusitis and 34% had invasive fungal sinusitis. Aspergillus flavus was the most common causative agent of allergic fungal sinusitis and Rhizopus arrhizus was the most common causative agent of acute invasive sinusitis. A significant proportion of these patients did not have any known predisposing factors. Conclusion: In our study, the etiology of fungal sinusitis was different than that of western countries. Allergic fungal sinusitis was the most common type of fungal sinusitis in our community. Aspergillus sp was the most common causative agent in both allergic and chronic invasive forms of the disease.

Keywords: Aspergillus flavus, fungal sinusitis

How to cite this article:
Michael RC, Michael JS, Ashbee RH, Mathews MS. Mycological profile of fungal sinusitis: An audit of specimens over a 7-year period in a tertiary care hospital in Tamil Nadu. Indian J Pathol Microbiol 2008;51:493-6

How to cite this URL:
Michael RC, Michael JS, Ashbee RH, Mathews MS. Mycological profile of fungal sinusitis: An audit of specimens over a 7-year period in a tertiary care hospital in Tamil Nadu. Indian J Pathol Microbiol [serial online] 2008 [cited 2018 Aug 20];51:493-6. Available from: http://www.ijpmonline.org/text.asp?2008/51/4/493/43738



   Introduction Top


Fungi are uncommon causes of sinusitis, but the incidence of these infections is increasing. [1] Many fungi have been associated with fungal sinusitis, including the Aspergillus species, several of the dematiaceous fungi including Curvularia, Bipolaris, Exserohilum and also the zygomycetes. [2] The etiological agents of fungal sinusitis reported from India vary from those of the western countries, wherein dematiaceous fungi are more common. Aspergillus spp are more commonly isolated from the Indian subcontinent. [3]

Most fungal sinus infections are benign or non invasive, except when they occur in individuals who are immunocompromised, such as patients with diabetes mellitus, leukemia, acquired immunodeficiency disease syndrome (AIDS), or other conditions that impair the immune system. [4]

The diagnosis of invasive fungal sinusitis is based on a high index of clinical suspicion in immunocompromised patients with fever, nasal congestion and discharge and facial pain. If fungi are grown from nasal swabs, this adds weight to the diagnosis, but a biopsy is required for confirmation.

The classification of fungal sinusitis, however, remains controversial with no universally accepted criteria. [2] Fungal sinusitis can be divided into two main types: non invasive and invasive. [2] Non invasive can be further divided into two forms: allergic fungal sinusitis (AFS) and sinus mycetoma/fungal ball, which occurs in immunocompetent patients. AFS should be suspected in individuals with intractable sinusitis and recurrent nasal polyposis. These patients usually have atopy and have had multiple sinus surgeries by the time of diagnosis. Computerised tomography (CT) scans of the sinuses reveal opacification with concretions and/or calcifications. Fungal ball or sinus mycetoma is usually unilateral and involves the maxillary sinus.

The more serious form of the disease, invasive fungal sinusitis, commonly occurs in patients with diabetes or in individuals who are immunocompromised and is characterized by its invasiveness, tissue destruction and rapid onset. It spreads rapidly, via vascular invasion, into the orbit and central nervous system (CNS). These patients require hospitalisation and urgent intervention. Early detection and treatment are vital for these infections because of the high mortality rate. [4]

The recommended therapies for invasive sinusitis are aggressive surgical removal of the fungal material along with necrotic or devitalised tissue and intravenous anti-fungal therapy. [4] Amphotericin B remains the treatment of choice for invasive fungal sinusitis due to the zygomycetes or Aspergillus. Surgery is important both in the diagnosis and debridement of necrotic tissue as well improving aeration and drainage within the sinuses. This is often done endoscopically to preserve the normal anatomy wherever possible.

The aim of this audit was to look at the spectrum of fungal sinusitis in patients in south India, specifically looking at the range of etiological agents and the associated predisposing factors.


   Materials and Methods Top


A total of 211 nasal and paranasal sinus tissue, exudates and allergic mucin specimens processed in the Mycology section of the Microbiology Department of a tertiary level teaching hospital in India from January 2000-August 2007 were analysed retrospectively. All the specimens were from patients attending the ENT outpatient department of the same hospital.

The relevant clinical details of the patients including the co-morbidities and histopathology reports as documented in the medical records were examined. Any factors indicating an immunocompromised status were noted.

All patients with a history and clinical examination suggestive of rhinosinusitis of fungal etiology underwent a thorough evaluation in the ENT outpatient department.

These patients underwent a rigid nasal endoscopy with swabs and biopsies from the middle meatus to assess the fungal etiology. CT scans of the paranasal sinuses were performed to look for bone erosion and heterogenous soft tissue opacity. Blood investigations were carried out for the presence of hematological, biochemical and metabolic abnormalities that could predispose to invasive forms of the disease.

Clinical presentations

Diagnosis of the type of fungal sinusitis was based on the criteria described below.

Allergic fungal sinusitis (AFS)

Patients with a combination of the following findings were diagnosed as having AFS as per the diagnostic criteria described by Bent and Kuhn. [5]

  • Radiologically-proven sinusitis.
  • Presence of allergic mucin within the nasal cavity or sinuses (degenerated eosinophils with Charcot-Leyden crystals and segmented branching fungal forms).
  • Demonstration of fungal hyphae in the allergic mucin.
  • Absence of fungal invasion of tissue on histopathology.
  • Absence of diabetes, immunodeficiency disease, or recent treatment with immunosuppressants.


Invasive fungal sinusitis

Diagnostic criteria for invasive fungal sinusitis as defined by deShazo: [6]

  • Mucosal thickenings or air fluid levels compatible with sinusitis on radiological imaging.
  • Histopathological evidence of hyphal forms within the sinus mucosa, submucosa, blood vessel, or bone.
  • To diagnose granulomatous invasive sinusitis, histopathological evidence of hyphal forms within the sinus mucosa, submucosa, blood vessel, or bone in association with granuloma consisting of giant cells.


Patients with invasive fungal sinusitis were further divided into two groups:

  1. Patients with acute fulminant invasive fungal sinusitis who presented with the following:

    1. Immunocompromised status or diabetes mellitus
    2. Dark-colored nasal lesions/ulcers, fever, headache, facial pain, epistaxis and changes in sensorium.


  2. Chronic invasive fungal sinusitis was further divided into nongranulomatous and granulomatous (indolent) depending on the histopathological examination.

    1. Patients with the non granulomatous chronic invasive form were commonly diabetics whereas those with the granulomatous form were immunocompetent.
    2. All patients had symptoms and signs of chronic sinusitis lasting longer than 4 weeks.
    3. When orbital extension was present, decreased vision and proptosis were the presenting symptoms.


Fungal ball

Patients were diagnosed as having a fungal ball if they had one of the following findings according to the criteria by deShazo, et al. [7] (most patients presented with non specific symptoms)

  • Radiologic studies showing sinus opacification often associated with floccular calcifications.
  • Mucopurulent; a cheesy or clay-like material presenting a single sinus at the time of surgery.
  • Histopathological evaluation showing dense agglomeration of hyphae separate from adjacent respiratory mucosa and the absence of allergic mucin.
  • No fungal invasion of tissue/mucosa.


Laboratory diagnosis

The samples received in the laboratory for diagnosis of fungal sinusitis were allergic mucin, exudate from the nasal mucosa, tissue biopsy from nasal polyps and sinus mucosa removed during paranasal surgery. They were all received in sterile containers.

Tissue samples were cut into small pieces using sterile scissors. For each of the samples, a portion was examined using light microscopy after digestion with 10% potassium hydroxide (KOH) and using fluorescence microscopy after digestion with a mixture of KOH and calcofluor white. The presence of hyaline or dematiaceous, septate or aseptate filamentous hyphae in direct microscopy was indicative of fungal infection.

The remaining portions of the samples were inoculated onto Sabouraud's dextrose agar and Sabouraud's dextrose agar with chloramphenicol and gentamicin. They were incubated at 27şC and 37şC for 4 weeks. Resultant fungal isolates were identified by the colony morphology and microscopic morphology observed on lactophenol cotton blue preparations. Only samples that were positive by both microscopy and culture were included in this analysis.


   Results Top


Over the 7-year period of the study, 211 patients were diagnosed with fungal sinusitis on the basis of positive microscopy and fungal culture. Of these, 115 were women and 96 were men; the mean age at presentation was 45.7 years (range = 11-79 years).

Among the 211 patients, 133 (63%) had the allergic form of the disease, with 51 (24%) presenting with acute invasive disease and 21 (10%) presenting with chronic invasive sinusitis, of whom only one had histopathological evidence of chronic granulomatous invasive sinusitis. Fungal granuloma was seen in only 6 patients (3%). All patients had histopathological evidence, which supported the diagnostic classification of these forms.

As shown in [Table 1], the range of organisms causing sinusitis varied with the different forms of the disease. For AFS, Aspergillus flavus was the most common etiological agent, with Aspergillus fumigatus being the next most common cause; together they were responsible for 88% of the cases. In contrast, in patients with acute invasive sinusitis, the most common etiological agent was the Rhizopus species belonging to the zygomycota division.

As shown in [Table 2], the majority of patients (62.7%) with acute invasive form of sinusitis were diabetics, whereas 43% of the patients with chronic invasive fungal sinusitis did not have any documented underlying co-morbidities or immunosuppressive condition.


   Discussion Top


The aim of this audit was to examine the etiology of fungal sinusitis and the associated predisposing factors in patients from south India. Other studies have been published from northern India. [8],[9]

This is the first large study from south India, although a more limited study has previously been published from our institution. [10] Over a 7-year period, 211 patients presented with fungal sinusitis and the most common form seen was allergic disease (63%). This contrasts with the findings of Chakrabarti, et al. [8] and Panda, et al. [9] who reported only small numbers of patients with allergic disease in their patient groups.

The exact definitions used for allergic disease are controversial and have changed over time so this difference may be more reflective of this change in diagnostic criteria rather than a genuine difference in the incidence of the different forms of disease between different regions in the country. [11],[12]

Aspergillus flavus was the most common etiological agent in allergic disease, as has been previously reported from north India with A. fumigatus the next most common species. [8],[9] In North America, dematiaceous fungi, such as Bipolaris spp and Curvularia spp were found to predominate in allergic sinusitis. [3] The reasons for this difference are a matter of speculation, but several factors may be involved. In India, a large proportion of the population live in rural or semi-rural areas and so their exposure to certain fungi will differ from arguably a more urban population in developed countries. Another contributory factor may be related to the type of housing in the two countries. In India, houses are often open to the environment and have an open-plan style and this may lead to prolonged exposure to fungi that occur in the outside environment. Houses in developed countries are more likely to be closed to the outside environment and hence the fungal population within the home may be different to that found outside and so exposure will be to those fungi colonising indoors, rather than outdoor fungi.

A third of the patients (34%) in this series had invasive fungal sinusitis. Among them, the most common form was acute invasive fungal sinusitis (24%), which has increased morbidity and mortality when compared with other forms of the disease. [1] The increased index of suspicion coupled with good mycological laboratory facilities for laboratory diagnosis and the increase in the incidence of diabetes with poor overall control of disease are likely to be important contributing factors toward this increased incidence. Another reason for the large number of patients with invasive disease is that the ENT department in our institution serves as a tertiary care referral center for local practitioners and for other parts of the country, as well as neighbouring countries.

The most frequent fungal isolate encountered in patients with acute invasive sinusitis was Rhizopus arrhizus . This belongs to the Zygomycete division of the order mucorales, which are angioinvasive and hence can cause rapid deterioration in the patient's condition. Patients who present with acute invasive fungal sinusitis typically have a compromised immune system, such as post chemotherapy or with uncontrolled diabetes [13] and this was found for 63% of the patients in this group.

However, it was also of interest to note that in 45% of patients with chronic invasive fungal sinusitis, there was no significant cause of immunocompromise or known co-morbidity. There are several possible reasons for these findings. A significant proportion of the Indian population lives below the poverty line and hence may be malnourished. Although they are not "immunocompromised" in the classical sense their poor nutritional status may render them more susceptible to invasive disease. The second reason may be that diabetes mellitus is known to be extremely common in India [14] and some of the patients with invasive sinusitis may have had undiagnosed diabetes mellitus, predisposing them to this form of disease.

In conclusion, this is the first large audit of fungal sinusitis from south India. The etiological agents involved in the different forms of disease seem to be common throughout the country, but differ from Western countries. Although allergic fungal sinusitis was the most common form of disease seen, invasive sinusitis was seen in a third of the patients surveyed and in a large proportion of the chronic invasive form there was no predisposing factor that could be found.

 
   References Top

1.Chakrabarti A, Sharma SC. Paranasal sinus mycoses. Indian J Chest Dis Allied Sci 2000;42:293-304.  Back to cited text no. 1  [PUBMED]  
2.deShazo RD, Chapin K, Swain RE. Fungal sinusitis. N Engl J Med 1997;337:254-9.   Back to cited text no. 2  [PUBMED]  [FULLTEXT]
3.deShazo RD, Swain RE. Diagnostic criteria for allergic fungal sinusitis. J Allergy Clin Immunol 1995;96:24-35.  Back to cited text no. 3  [PUBMED]  [FULLTEXT]
4.Thrasher RD, Kingdom TT. Fungal infections of the head and neck: An update. Otolaryngol Clin North Am 2003;36:577-94.   Back to cited text no. 4  [PUBMED]  
5.Bent JP 3 rd . Kuhn FA. Diagnosis of allergic fungal sinusitis. Otolaryngol Head Neck Surg 1994;111:580-8.  Back to cited text no. 5    
6.deShazo RD. Fungal sinusitis. Am J Med Sci 1998;316:39-45.  Back to cited text no. 6  [PUBMED]  [FULLTEXT]
7.deShazo RD, O'Brien M, Chapin K, Soto-Aguilar M, Swain R, Lyons M, et al Criteria for diagnosis of sinus mycetoma. J Allergy Clin Immunol 1997;99:475-85.  Back to cited text no. 7    
8.Chakrabarti A, Sharma SC, Chandler J. Epidemiology and pathogenesis of paranasal sinus mycoses. Otolaryngol Head Neck Surg 1992;107:745-50.  Back to cited text no. 8  [PUBMED]  
9.Panda NK, Sharma SC, Chakrabarti A, Mann SB. Paranasal sinus mycoses in north India. Mycoses 1998;41:281-6.  Back to cited text no. 9  [PUBMED]  
10.Rupa V, Jacob M, Mathews MS, Job A, Kurien M, Chandi SM. Clinicopathological and mycological spectrum of allergic fungal sinusitis in South India. Mycoses 2002;45:364-7.  Back to cited text no. 10  [PUBMED]  [FULLTEXT]
11.Schubert MS. Allergic fungal sinusitis. Clin Rev Allergy Immunol 2006;30:205-16.  Back to cited text no. 11  [PUBMED]  [FULLTEXT]
12.Saravanan K, Panda NK, Chakrabarti A, Das A, Bapuraj RJ. Allergic fungal rhinosinusitis: An attempt to resolve the diagnostic dilemma. Arch Otolaryngol Head Neck Surg 2006;132:173-8.  Back to cited text no. 12  [PUBMED]  [FULLTEXT]
13.Chopra H, Dua K, Malhotra V, Gupta RP, Puri H. Invasive fungal sinusitis of isolated sphenoid sinus in immunocompetent subjects. Mycoses 2006;49:30-6.  Back to cited text no. 13  [PUBMED]  [FULLTEXT]
14.Pradeepa R, Mohan V. The changing scenario of the diabetes epidemic: Implications for India. Indian J Med Res 2002;116:121-32.  Back to cited text no. 14  [PUBMED]  

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Correspondence Address:
Joy S Michael
Department of Microbiology, Christian Medical College and Hospital, Vellore 632 004, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.43738

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    Tables

  [Table 1], [Table 2]

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