Abstract

To review invasive aspergillosis (IA) in developing countries, we included those countries, which are mentioned in the document of the International Monetary Fund (IMF), called the Emerging and Developing Economies List, 2009. A PubMed/Medline literature search was performed for studies concerning IA reported during 1970 through March 2010 from these countries. IA is an important cause of morbidity and mortality of hospitalized patients of developing countries, though the exact frequency of the disease is not known due to inadequate reporting and facilities to diagnose. Only a handful of centers from India, China, Thailand, Pakistan, Bangladesh, Sri Lanka, Malaysia, Iran, Iraq, Saudi Arabia, Egypt, Sudan, South Africa, Turkey, Hungary, Brazil, Chile, Colombia, and Argentina had reported case series of IA. As sub-optimum hospital care practice, hospital renovation work in the vicinity of immunocompromised patients, overuse or misuse of steroids and broad-spectrum antibiotics, use of contaminated infusion sets/fluid, and increase in intravenous drug abusers have been reported from those countries, it is expected to find a high rate of IA among patients with high risk, though hard data is missing in most situations. Besides classical risk factors for IA, liver failure, chronic obstructive pulmonary disease, diabetes, and tuberculosis are the newly recognized underlying diseases associated with IA. In Asia, Africa and Middle East sino-orbital or cerebral aspergillosis, and Aspergillus endophthalmitis are emerging diseases and Aspergillus flavus is the predominant species isolated from these infections. The high frequency of A. flavus isolation from these patients may be due to higher prevalence of the fungus in the environment. Cerebral aspergillosis cases are largely due to an extension of the lesion from invasive Aspergillus sinusitis. The majority of the centers rely on conventional techniques including direct microscopy, histopathology, and culture to diagnose IA. Galactomannan, β-D glucan test, and DNA detection in IA are available only in a few centers. Mortality of the patients with IA is very high due to delays in diagnosis and therapy. Antifungal use is largely restricted to amphotericin B deoxycholate and itraconazole, though other anti-Aspergillus antifungal agents are available in those countries. Clinicians are aware of good outcome after use of voriconazole/liposomal amphotericin B/caspofungin, but they are forced to use amphotericin B deoxycholate or itraconazole in public-sector hospitals due to economic reasons.

Introduction

Aspergillus species cause a wide spectrum of diseases including allergic syndrome, colonizing sinuses or cavities, acute or subacute and chronic invasive diseases. Invasive aspergillosis (IA) is a disease of concern, as it is a leading cause of death in patients with hematological malignancies and transplant recipients. With the use of broad-spectrum antifungal agents for prophylaxis in those high risk patients, the incidence and fatality rates of IA have declined in recent years, but new risk factors have emerged [1,2]. The incidence rates among patients at risk vary according to local epidemiology. Though the epidemiology of the disease and magnitude of the problem are well studied in the developed world, literature is scanty from developing countries.

Developing countries are home to around five-sixth of the world's population [3] and the countries are located in the tropical and sub-tropical regions of Asia, Africa, South and Central America where fungi thrive well in the hot and humid climate [4]. These countries have large numbers of poor people with few modern medical facilities at one end and rapidly developing prosperity and health care on the other end. Below-optimum hospital care practice in the economically deprived group, and modern medical intervention including transplantations in the prosperous group have led to an increase in number of invasive fungal diseases including IA in both groups [4]. Further, the large number of untrained health providers (quacks), the misuse of steroids, intravenous drug abuse, availability of spurious medical care infusion sets, are possible additional risk factors for IA in those countries [4,5]. As the number of persons at risk of IA in developing countries is huge, it is important to review the available literature on IA from these countries.

To identify the list of developing countries we followed the document of the International Monetary Fund database for the Emerging and Developing Economies, 2009 [6]. A PubMed/Medline literature search was performed for IA reported during 1970 through March 2010 from these countries. Articles were searched with the following Keywords: ‘Aspergillus’, ‘Aspergillosis’, ‘A. fumigatus’, ‘A. flavus’, ‘Leukemia’, ‘Bone Marrow Transplantation’, ‘Transplantation’, ‘Infections’. Reports with allergic Aspergillus-related disease and superficial Aspergillus infection were not considered. Published literatures on IA consist mainly of case series and case reports from a few tertiary care centers located in China [7–9], India [4,5, 10–12], Thailand [13–16], Pakistan [17–21], Iran [22–35], South Africa [36–40], Saudi Arabia [41–46], Sri Lanka [47–49], Egypt [50–56], Brazil [57–59], Argentina [60–65], Barbados [66], Bangladesh [67], Bolivia [68], Central African Republic [69], Chile [70–72], Colombia [73,74], Croatia [75,76], Estonia [77], Hungary [78,79], Iraq [80], Jamaica [81], Kuwait [82–84], Lebanon [85,86], Libya [87], Lithuania [88], Mexico [89–91], Morocco [92,93], Malaysia [94], Oman [95], Poland [96–98],Tunisia [99], Turkey [100–118], Sudan [40,119–122], Senegal [123], and Zimbabwe [124]. The present review was prepared after going through each article.

Epidemiology

In developing countries the risk factors for development of IA appear similar to the developed world, though certain differences are observed due to local epidemiology including patient characteristics, cultural habit, patient care practices [4,5,8,10,15,25,33,36,49,59,60,67,76,94,125–130]. The risk factors are outlined in Table 1. Few factors including hematological malignancies, various transplantations, chronic granulomatous disease, advanced AIDS, cytomegalovirus pneumonia are well documented [11,12,34,38,45,53,57,59,62,131,132]. In a systematic review of IA from a tertiary care hospital in Thailand, acute leukemia was the commonest underlying disease (30%); neutropenia (39%), chemotherapy (34%), and corticosteroid therapy (25%) were major predisposing factors [15]. Diabetes mellitus (17%) and systemic lupus erythematosus (15%) were found as the second and third common underlying conditions in that study.

Table 1

Risk factors for invasive aspergillosis in developing countries.

Classic factors Non-neutropenic factors 
Acquired neutrophil defect Chronic obstructive pulmonary disease 
Neoplastic disease with persistent neutropenia Chronic and acute liver disease 
 Intracranial surgery 
High dose of corticosteroids Reactive airway disease 
Immunosuppressants Rheumatoid arthritis 
Bone marrow and solid organ transplants ICU stay 
Aplastic anaemia/myelodysplastic syndrome/myelofibrosis  
AIDS — only when CD4 <50 cells  
Primary defect of neutrophils Newly recognized factors 
Chronic granulomatous disease Hyper-IgE syndrome (Job's)  
 Intravenous infusion/drug abuse 
 Diabetes mellitus 
 Burn wound 
 Application of tapes/ECG leads 
 Allergic broncho pulmonary aspergillosis/asthma 
Classic factors Non-neutropenic factors 
Acquired neutrophil defect Chronic obstructive pulmonary disease 
Neoplastic disease with persistent neutropenia Chronic and acute liver disease 
 Intracranial surgery 
High dose of corticosteroids Reactive airway disease 
Immunosuppressants Rheumatoid arthritis 
Bone marrow and solid organ transplants ICU stay 
Aplastic anaemia/myelodysplastic syndrome/myelofibrosis  
AIDS — only when CD4 <50 cells  
Primary defect of neutrophils Newly recognized factors 
Chronic granulomatous disease Hyper-IgE syndrome (Job's)  
 Intravenous infusion/drug abuse 
 Diabetes mellitus 
 Burn wound 
 Application of tapes/ECG leads 
 Allergic broncho pulmonary aspergillosis/asthma 

In haemato-oncological and haematopoietic allogenic stem cell transplant (HSCT) patients, IA is consistently the commonest fungal infection, though the incidence varied between different series [11,12,16,33,59,76,79]. The incidence of invasive candidiasis was invariably lower than IA in those patients, possibly due to routine use of fluconazole prophylaxis in such patients. The studies from Iran, India, and Tunisia reported IA in ∼15% patients with hematological malignancies [12,33,99]. In a hospital from Chile, IA was the commonest (63.4%) fungal infection among all fungal diseases in patients with haemato-oncological malignancy and HSCT [71]. In HSCT recipients the incidence of IA ranged between 3–15% in different studies [30,59]. In Brazil the number of patients with IA changed with structural change of a bone-marrow unit [59]. In a study from Hungary, IA was responsible for mortality in 40% of all deaths due to established infections in patients with HSCT [79]. The patients who acquire IA had a high (83%) mortality rate within 60 days of diagnosis. Indication of mortality included corticosteroid use, neutropenia at the time of diagnosis, change of antifungal agent due to toxicity, and disseminated disease [59].

IA occurs in ∼13% patients with lung transplantation and is always associated with either acute rejection episode or suture damage [70]. The incidence is consistent with the observations in the developed world [2]. In contrast IA was reported at a higher rate (2–4%) in patients with renal transplantation in developing countries [28,118] compared to <1% in developed countries [2]. This finding might be related to poor hygiene and sanitation in developing countries [118]. Due to inadequate cadaveric and living related organ supply, many patients with end-stage renal disease from the developed world go to the third-world countries for living unrelated (paid) kidney transplantation and acquire IA due to below optimum hospital care practices [133]. IA also complicates the patients undergoing liver transplantation in those countries. Multiple risk factors including hepatic failure, haemodialysis, and cytomegalovirus infection act in concert to wreck the immunity of patients with liver transplantation to Aspergillus species [7,22,26,27,96,134]. Heart transplantation is still rare in developing countries. Experience from a few centers reported IA cases, but the infection rate is not known [98,102].

Though IA is a common complication in patients with hematological malignancies [11,12,59], the reports of the IA in solid tumors are rare. In a study from China 45 (2.6%) of 1711 lung cancer patients had pulmonary aspergillosis [8]. On univariate analysis chemotherapy, steroid use, and stage IV diseases were found to be the significant risk factors; and on multivariate analysis only stage IV disease was the significant risk factor. Neutropenia and corticosteroid therapy correlated statistically with pulmonary aspergillosis in patients who died [8].

Apart from these classical risk factors, other factors like critically ill patients admitted in intensive care units, patients with pre-existing lung disease (emphysema, chronic obstructive pulmonary disease, healed tuberculosis cavity), and patients with liver failure are also claimed to be associated with IA in developing countries. IA in the intensive care unit patients have been reported infrequently [36,135]. However, the co-factors (multiple intravenous lines, tracheostomy, endotracheal intubation, other invasive procedures, prolonged corticosteroid and antibiotic therapy) in ICUs are either higher in numbers or misused more in developing countries due to sub-optimal protocol adherence by ICU staff [136]. Therefore, in all probability the incidence of IA is expected to be high in ICUs of developing countries. The association of liver failure and IA had been reported from centers in China [137,138]. De-compensated liver disease has been noted to be a cause of acquired immunodeficiency state, and malnourishment in hepatic failure adds to the severity of the condition. Further, frequent use of broad-spectrum antibiotics, steroids, and intensive monitoring make those patients susceptible to IA [139,140].

The elderly patients with chronic obstructive pulmonary disease are often colonized with Aspergillus species. They receive corticosteroids (oral or inhaled), are often critically ill and hospitalized, receive multiple antibiotics, and become susceptible to IA. Such patients were reported from China and India [125,141]. A rare case of Aspergillus endocarditis was reported in a patient with allergic bronchopulmonary aspergillosis (ABPA) [125]. Patients with structural lung-airway disease due to previous tuberculosis have been reported to acquire IA. Though developing countries have large number of patients with tuberculosis, IA is infrequently reported, except one autopsy series from Mumbai [126,142,143]. The autopsy series from Mumbai reported tuberculosis as a risk factor in 28% patients [126].

Recent studies reported the association of diabetes mellitus [143–146] and corticosteroid therapy [60,147,148] with IA in developing countries. Uncontrolled diabetes is a known risk factor for zygomycosis in India [149]. Possibly the decreased functional activity of macrophages in patients with diabetes predisposes the patients to IA also [143,146]. Intracranial surgery is an additional risk factor for isolated intracranial aspergillosis [61,150,151], and permanent pacemaker placement for Aspergillus endocarditis in immunocompetent hosts of developing countries [152]. From Argentina, a unique study reported Aspergillus osteomyelitis in 11% patients during childhood, which was significantly associated with chronic granulomatous disease [62].

A considerable number of IA cases in developing countries has been reported in immunocompetent host especially those with isolated cerebral aspergillosis and rhino-orbito-cerebral aspergillosis [15,21,37,41,42,75,85,87,94,111,123,150,153,154]. In a series from Thailand, 86% patients with cerebral aspergillosis had either diabetes or no known immunocompromised status [13]. This finding of interest may be due to the high spore count in the environment of tropical countries [73,99] or due to less investigation of host immunity status.

Aspergillus species

The commonest species implicated in IA is Aspergillus fumigatus. Other Aspergilli including A. flavus, A. terreus, A. niger, A. ustus, and A. alliaceus have been implicated as pathogens less commonly in patients with IA [43,45, 100,101,127,155–158]. However, in developing countries A. flavus has been isolated comparatively at higher frequency from sino-orbital aspergillosis or Aspergillus eye infections [21,121,122,127,154,159,160,166–168]. Few of those series reported A. flavus to be the exclusive agent or several times more common than A. fumigatus. Higher environmental contamination due to A. flavus may lead to increased frequency of A. flavus infections in developing countries [73,99]. A. niger has been reported as the etiological agent in patients with endophthalmitis [43,127,155], and endocarditis [23]. A. terreus [156,157] and A. ustus [100,107] have been isolated from patients with endophthalmitis. A. terreus was also isolated from a case of aortic root abscess and pseudoaneurysm post-cardiac surgery [161]. Rare cases of A. nidulans or A. glaucus isolation were reported from patients with brain abscess [85,162].

Pulmonary aspergillosis

Pulmonary aspergillosis is highly prevalent in developing countries [109,134,163]. In the series of IA reported from a tertiary care hospital in Thailand [15], the lung was involved in 68% of cases followed by sinuses (17%), eyes (8%), and brain (5%). Similarly pulmonary aspergillosis is by far the most common form of IA in transplant patients [11,59,71,79,103,118]. In an autopsy study of childhood pneumonia from Bangladesh, pulmonary aspergillosis was diagnosed in 3% of all pneumonias and 10% of necrotizing pneumonias [67]. The clinical course of pulmonary aspergillosis may be acute or chronic depending on host immune status and the amount of exposure of Aspergillus spore. Other than classical manifestations of pulmonary aspergillosis, certain uncommon clinical presentations have been observed in developing countries. Some of these observations include development of invasive pulmonary aspergillosis (IPA) in patients with colonizing aspergillosis (in tubercular cavity) [126,143], ABPA or aspergilloma [57,164], and bronchial asthma [8,126]. Possibly, the long period of steroid therapy allowed fungal hyphae from a cavitary lesion or localized mass lesion to invade the lung parenchyma. IPA was also found to be associated with anti neutrophilic cytoplasmic antibodies positive vasculitis [91,165]. In a series of 157 patients with vasculitis, seven (4.5%) developed IPA; two had Wegener's granulomatosis and five had microscopic polyangitis. IPA developed within 2–13 weeks of immunosuppressive therapy [165].

Isolated invasive Aspergillus tracheobronchitis is an uncommon clinical form of invasive aspergillosis and mostly reported in patients with severely immunocompromised status due to transplantation or haematological malignancies. Of note, 19 patients with isolated invasive Aspergillus tracheobronchitis were reported from China, who had impaired airway structures or defense functions rather than severely immunocompromised status. Only three (16%) patients had neutropenia. Malignancy (13 cases of solid tumor, one case of lymphoma) was the most common underlying disease. The disease could be classified into four different forms: superficial infiltrative, full layer involvement, occlusion, and mixed type [128].

Sino-orbital-cerebral aspergillosis

This clinical type is a highly prevalent disease in tropical countries, though much confusion exists regarding its categorization [92,93,109,119,121,159,160,166–168]. The most commonly accepted classification divides invasive fungal rhinosinusitis (FRS) into acute invasive FRS, granulomatous invasive FRS, and chronic invasive FRS [166]. The prevalence of acute invasive FRS is more or less similar in the developed and developing world. [168,169] However, in the developed world hematological malignancy is the commonly associated underlying disease in acute invasive FRS with higher isolation of A. fumigatus. In contrast uncontrolled diabetes is more commonly associated in developing countries with higher isolation of Zygomycetes in such a setting. This may be due to the high prevalence of uncontrolled diabetes in these countries [149]. Granulomatous invasive FRS is primarily seen in Sudan, India, Pakistan, and Saudi Arabia. The disease is described by a time course of >12 weeks with enlargement of mass in the cheek, nose, paranasal sinuses and the orbit in the immunocompetent host. Histopathologically it is characterized by granulomatous inflammation and considerable fibrosis, with presence of scanty hyphae, and A. flavus is the primary agent isolated [21,121,122,154,168]. In contrast, chronic invasive disease is seen in any part of the world and is characterized by dense accumulation of hyphae, presence of vascular invasion, sparse inflammatory reaction, and A. fumigatus isolation in patients with diabetes and on corticosteroid treatment [168,169]. It is noteworthy that A. flavus is the common etiological agent of all types of FRS except acute invasive type in Sudan and India [119,122,159,160,166–168].

Cerebral aspergillosis

Although Aspergillus spp. have a predilection for the central nervous system and many series of cerebral aspergillosis are reported from developing countries, the studies are limited by non-availability of relevant microbiological analysis. Most prevalence reports are based on surgical practice and postmortem data [144,147,150,154]. The reports of these series at least denoted high prevalence of cerebral aspergillosis in developing countries. The central nervous system involvement by Aspergillus species is either by haematogenous dissemination or direct inoculation of the agent during surgical procedure or spread from contiguous structures like paranasal sinuses, mastoid, and middle ear. The haematogenous dissemination leads to multiple acute necrotizing purulent lesions commonly in the parietal lobe involving the middle or anterior cerebral artery. Whereas contiguous spread occurs from granulomatous lesions in the paranasal sinuses and middle ear leading to the development of chronic granuloma with dense fibrosis in adjacent structures of the brain like the frontal (from paranasal sinuses) or temporal lobe (from middle ear or mastoid) [144]. As FRS is a highly prevalent disease in Asia, the Middle East, and Africa [119,159,160,166–169], the paranasal source of CNS involvement is common and often results in an orbital apex syndrome or granulomatous disease of the frontal lobe [24,104,144,147,150,154,170]. The two clinical conditions (rhinocerebral granulomas and intracranial abscess) have different presentations (Table 2). The former variety occurs commonly in immunocompetent hosts in contrast to intracerebral abscess. Rhinocerebral lesions are usually diagnosed early due to easier sampling from paranasal sinuses and have less mortality. In contrast intracerebral abscess developed by haematogenous dissemination have high mortality and are diagnosed late as a clinical surprise because of subtle clinical presentations and absence of any diagnostic characteristics [150].

Table 2

Differentiating features of rhinocerebral Aspergillus granuloma and intracerebral Aspergillus abscess (modified from Sharma et al.) [38].

Sl. no. Characters Rhinocerebral Aspergillus granuloma Intracerebral Aspergillus abscess 
Duration of lesion >3 months <3 months 
Mode of spread Contiguous Haematogenous dissemination 
Site of brain lesion Commonly frontal lobe Commonly parietal lobe 
Clinical presentation Frontal lobe symptoms with sinusitis Raised intracranial pressure, seizures 
Dura involvement Common Uncommon 
Imaging Hyperdense with mild enhancement Mixed density with patchy or rim enhancement 
Pathology (gross) Tough — requires knife to cut Soft 
Pathology (microscopy) Granuloma with fibrosis Abscess with necrosis 
Diagnosis Early by samples from sinuses Delayed till craniotomy 
10 Differential diagnosis Malignancy Tubercular or pyogenic abscess 
11 Prognosis Low mortality though prolonged morbidity High mortality 
12 Recurrence Common Uncommon 
Sl. no. Characters Rhinocerebral Aspergillus granuloma Intracerebral Aspergillus abscess 
Duration of lesion >3 months <3 months 
Mode of spread Contiguous Haematogenous dissemination 
Site of brain lesion Commonly frontal lobe Commonly parietal lobe 
Clinical presentation Frontal lobe symptoms with sinusitis Raised intracranial pressure, seizures 
Dura involvement Common Uncommon 
Imaging Hyperdense with mild enhancement Mixed density with patchy or rim enhancement 
Pathology (gross) Tough — requires knife to cut Soft 
Pathology (microscopy) Granuloma with fibrosis Abscess with necrosis 
Diagnosis Early by samples from sinuses Delayed till craniotomy 
10 Differential diagnosis Malignancy Tubercular or pyogenic abscess 
11 Prognosis Low mortality though prolonged morbidity High mortality 
12 Recurrence Common Uncommon 

Although vascular invasion by Aspergillus species is a common finding, true mycotic aneurysm is rare. In developing countries occasionally such cases of intracranial mycotic aneurysms have been reported as a result of direct invasion of the wall of blood vessels either from the luminal or adventitial side [144,171,172]. Isolated meningitis due to Aspergillus spp. is a rare finding, as also is spinal cord involvement. The possibility of iatrogenic intrusion by Aspergillus spp. in the meninges through contaminated needles was suggested in some cases after performing spinal anaesthesia [48,49,171]. This was further supported in the outbreak of Aspergillus meningitis in Sri Lanka which was considered a post-tsunami effect. This outbreak occurred between 2 July and 25 July 2005, where five patients suffered from Aspergillus meningitis after administration of spinal anaesthesia for cesarean section. As the drug warehouses were full of donations for survivors of the tsunami, the regular supplies of the hospital were stored in a dirty and humid temporary warehouse, which possibly led to contamination of the syringes with A. fumigatus. After destruction of the unused syringes, the outbreak was controlled. This outbreak also proves that poor hospital practices in developing countries may lead to many cases of iatrogenic invasive aspergillosis [47].

Cardiac aspergillosis

Aspergillus endocarditis, an uncommon but life threatening entity, occurs mainly on prosthetic valves, but patients with native valve Aspergillus endocarditis have been described from India and Iran [1,23,54,125,152,154,173,174]. The disease has also been described as a part of disseminated aspergillosis [175]. Patients with Aspergillus endocarditis may present with fever, multiple embolic strokes, valve abnormalities, and arrhythmias [154,173]. The invading Aspergillus hyphae have a tendency to extend deep into the myocardium and pericardium producing multiple abscesses, necrosis, vasculitis, and areas of infarction [125]. The Aspergilli may further invade into the lungs [125], and even the reverse may occur where a mediastinal mass due to angioinvasive Aspergillus spp. may involve the pericardium and the heart [173].

Disseminated aspergillosis

Disseminated aspergillosis is a life threatening rapidly fulminant infection, involving two or more non-contiguous organs of the body, occurring in severely immunocompromised patients [7,13,57,94,154,175–178]. A rare case of disseminated aspergillosis was documented in an apparently immunocompetent host in Malaysia [94]. Lung is the common involved organ in all cases of dissemination [7,13,51,57,154,175–178]. Other involved organs include brain, heart, kidneys, liver, thyroid, and the gastrointestinal tract. Gastrointestinal aspergillosis, a rare entity, had been reported as a part of dissemination [176,177].

Aspergillus endophthalmitis

Aspergillus endophthalmitis is an emerging problem in developing countries [5,43,100,127,156,157,179–182]. In fact, the largest series of fungal endophthalmitis (including 31 patients with Aspergillus endophthalmitis) from a single center was reported from India [127]. Trauma (45%) and ocular surgery (48%) are the major predisposing factors for such infections. Postoperative Aspergillus endophthalmitis may be seen in clusters due to the use of contaminated irrigation solution, intraocular lenses, donor cornea, ventilation system, and hospital construction activities [107,127,183,184]. An outbreak of A. ustus endophthalmitis from Turkey confirmed the same fact [100]. Contamination of operation theatre due to less stringent infection control practices coupled with poor quality care in rural eye camp settings are responsible for unusually high number of cases of post-operative Aspergillus endophthalmitis in developing countries [127,182]. Post traumatic Aspergillus endophthalmitis usually occurs after injury due to contaminated wires, wooden sticks, and hypodermic needle [127]. Infection develops within 4 weeks of cataract surgery or trauma [127]. Endogenous Aspergillus endophthalmitis is reported rarely as a part of dissemination in IA. However, the unique outbreak of endogenous Aspergillus endophthalmitis in India after a single intravenous administration of presumably contaminated dextrose infusion fluid possibly highlights the unusual scenario prevailing in developing countries [5].

Invasive cutaneous aspergillosis

This is another emerging problem in developing countries especially in the tropical areas. Primary cutaneous aspergillosis is observed in special risk groups like burn victims, neonates, HIV-infected populations, and solid organ transplant recipients [65,185]. In contrast, the secondary cutaneous aspergillosis, a comparatively rare disease accounting for <5% of cases of disseminated aspergillosis, is confined to hematopoietic stem cell transplant (HSCT) recipients [17,186,187]. In developing countries poor intravascular catheter care, use of contaminated arm boards, adhesive tapes, and occlusive dressings are the possible reasons for higher incidence [185]. However, in a study from Iraq it was pointed out that fungal infections were more common in burn patients with open dressings (25.5%) than with occlusive dressings (16%) [80].

Uncommon presentations of invasive aspergillosis

The literature from developing countries has documented rare cases of Aspergillus myositis [177], Aspergillus polyarthritis [19], and primary renal aspergillosis [7,130], Aspergillus osteomyelitis (including those of the vertebral column) [45,131] and hepatic abscess [53,131].

Experience at our center

From our Institute, a tertiary care centre (∼1500 beds) in north India, systemic fungal infection was detected in 2.4% of all autopsies performed (15,040 deaths autopsied over 26 years) and IA was detected in 49% of those fungal positive cases (means 1.2% of all autopsy cases). Further, between 1994 and 2008, systemic fungal infection was demonstrated in 34 (9%) of 374 autopsies having liver failure (224 cirrhosis and 150 acute failure), and 59% of those cases had IA. Comparison of these two series (2.4% vs. 9% systemic fungal infections; 1.2% vs. 5.3% IA) indicates strong association of underlying liver failure with systemic fungal infections particularly with IA (unpublished observation by author AD).

ABPA is the most frequently recognized manifestation in allergic aspergillosis at our center [188]. In a rare case of ABPA from our Institute, the patient succumbed to his illness after the development of multilobular consolidation and multi-organ dysfunction. On autopsy invasive pulmonary aspergillosis with extensive dissemination to the thyroid, both kidneys and colon were observed (Fig. 1–3) (discussed at the Clinic-pathological Conference in September 2007 at our Institute).

Fig. 1

Both lungs with cavitary lesions present bilaterally and dilated bronchi filled with mucus in the lower lobes.

Fig. 1

Both lungs with cavitary lesions present bilaterally and dilated bronchi filled with mucus in the lower lobes.

Fig. 2

(a) Bronchiectatic cavities with Aspergillus balls (H & E × 100). (b) Grocott's stain highlighting the fungal hyphae invading the bronchiectatic airway wall (H & E ×100).

Fig. 2

(a) Bronchiectatic cavities with Aspergillus balls (H & E × 100). (b) Grocott's stain highlighting the fungal hyphae invading the bronchiectatic airway wall (H & E ×100).

Fig. 3

Grocott's stain highlighting the Aspergillus hyphae (H & E × 200).

Fig. 3

Grocott's stain highlighting the Aspergillus hyphae (H & E × 200).

The proportional higher isolation of A. flavus from patients with IA in developing countries led us to conduct an environmental surveillance of our hospital. Air samples were collected from the centrally air-conditioned portion of wards and non-air conditioned portion of the hospital every month for one year to evaluate the predominant Aspergillus spore in the air in those areas. In the air-conditioned wards A. flavus was the predominant agent isolated in all seasons except in the summer months, when A. niger outnumbered A. flavus. However, in non-air conditioned areas, A. flavus was the predominant species isolated only during winter and spring (January to March), A. fumigatus in summer and A. niger in autumn (unpublished observation).

Diagnosis of invasive aspergillosis

Many cases of IA remain undiagnosed until it is too late to save the patient [24] or diagnosed only at autopsy in developing countries [125,126,129]. Conventional direct microscopy, histopathology, and culture methods are the only available techniques in most centers to diagnose IA due to the non availability of galactomannan or beta-glucan tests assay. Therefore, most patients with IA reported from developing countries are proven cases, though few centers reported probable and possible aspergillosis cases as well [11,15,59,71,99,118]. A bone-marrow transplant center in Hungary had reported that despite the regular use of galactomannan antigen and imaging, antemortem diagnosis could be established in only 40% of cases with IA [79]. Polymerase chain reaction (PCR) has been successfully used to diagnose Aspergillus endophthalmitis in a few centers [51,189–191]. PCR technique had also been used to diagnose other forms of IA occasionally, but the test requires further validation [32].

Treatment of invasive aspergillosis

Despite the recommendation of Infectious Disease Society of America to use voriconazole as the primary therapy of IA [192], and better outcome reported while using voriconazole as compared to amphotericin B [1], amphotericin B or itraconazole is the first line therapy in the majority of patients with IA in developing countries possibly due to the higher cost of other anti-Aspergillus effective drugs [11,13,15,47,57,59,118,128,131,146–148,150,193]. The scenario is comprehensively reviewed in the study of a tertiary care hospital in Thailand where amphotericin B deoxycholate was prescribed as the first line therapy in 59% patients with IA, followed by itraconazole (39%), liposomal amphotericin B (10%), caspofungin (5%), and voriconazole (2%) [15]. The authors in that study summed up the use of amphotericin B followed by itraconazole as the mainstay of treatment due to the higher cost of other antifungal agents. Similarly, in the Brazilian study, 91.6% HSCT recipients with IA received amphotericin B due to economic reasons, though 37.5% of them needed to change this first choice, principally because of nephrotoxicity (55.6%) and failure (33%) [59]. The cost of the drug is an important hurdle in the management of IA in those countries, as patients may be unable to complete the therapy despite the initial good response using voriconazole [146]. Only a few studies could evaluate the response to voriconazole or liposomal amphotericin B or caspofungin in IA, when patients could afford such therapy [13,15,82,118,146]. Nebulized amphotericin B has also been successfully used with voriconazole for treatment of Aspergillus tracheobronchitis [14]. The response to amphotericin B or itraconazole is good in immunocompetent patients [128,194]. However, the response in immunosuppressed or neutropenic patients is not encouraging (mortality up to 87.5%) [13,15,59,118]. Delay in admission to the hospital, diagnosis, and start of antifungal therapy are the other possible reasons of high mortality in those patients. In a study on patients with cerebral aspergillosis, it was observed that the median duration of symptoms prior to hospital admission was 60 days (range 8–180 days) and the median time taken to get the clinical diagnosis and treatment after admission was 8 days (range 5–30 days). High mortality (87.5%) was reported in that study in spite of extensive surgery and antifungal therapy in the majority of the patients [13]. During management of invasive fungal sinusitis, therapy with an amphotericin B formulation (active against both Aspergillus and Zygomycetes) is desirable until confirmation of etiology on culture or histopathology [1,42,153,160]. To manage Aspergillus endophthalmitis, the combination of parsplana vitreoctomy and intra-vitreal amphotericin B with or without itraconazole was recommended [127].

Conclusion

The frequency of IA in developing countries is expected to be high, though the disease is under-reported or reported late. Besides usual presentations of IA, certain peculiarities have been observed in those countries regarding risk factors, clinical presentations, and the Aspergillus spp. isolation. Apart from the classical risk factors, patients with pre-existing lung diseases, liver failure and diabetes are associated with IA. Sino-orbital or cerebral aspergillosis and Aspergillus endophthalmitis are highly prevalent diseases and A. flavus is isolated at a higher frequency compared to A. fumigatus from these patients. Though early diagnosis and therapy is desirable to manage IA, antifungal medication is frequently delayed leading to high mortality. Amphotericin B deoxycholate followed by itraconazole are the most commonly prescribed drugs to treat IA in developing countries due to economic constraints.

Acknowledgements

We acknowledge the help of Dr Kirti Gupta, Histopathology Department for the histopathology photographs, and Ms Manpreet Dhaliwal, Microbiology Department, PGI, for reference management.

Declaration of interest: The authors report no conflict of interest. The authors alone are responsible for the content and writing of the paper.

References

1.
Segal
BH
Aspergillosis
N Engl J Med
 , 
2009
, vol. 
360
 (pg. 
1870
-
1884
)
2.
Singh
N
Paterson
DL
Aspergillus infections in transplant recipients
Clin Microbiol Rev
 , 
2005
, vol. 
18
 (pg. 
44
-
69
)
3.
Population reference bureau [homepage on Internet]
World population highlights
 , 
2008
, vol. 
63
  
September Available from:
 
http://www.prb.org/Publications/PopulationBulletins/2008/worldpopulationhighlights2008.aspx. Key findings from PRB's world population data sheet. In: Population Bulletin;
4.
Chakrabarti
A
Chatterjee
SS
Shivaprakash
MR
Overview of opportunistic fungal infections in India
Nippon Ishinkin Gakkai Zasshi
 , 
2008
, vol. 
49
 (pg. 
165
-
172
)
5.
Gupta
A
Gupta
V
Dogra
MR
, et al.  . 
Fungal endophthalmitis after a single intravenous administration of presumably contaminated dextrose infusion fluid
Retina
 , 
2000
, vol. 
20
 (pg. 
262
-
268
)
6.
International Monetary fund [homepage on Internet]
IMF Emerging and Developing Economies List
 , 
2009
 
World Economic Outlook Database, October Available from: http://www.imf.org/external/pubs/ft/weo/2009/02/weodata/index.aspx.
7.
Shi
SH
Lu
AW
Shen
Y
, et al.  . 
Spectrum and risk factors for invasive candidiasis and non-Candida fungal infections after liver transplantation
Chin Med J (Engl)
 , 
2008
, vol. 
121
 (pg. 
625
-
630
)
8.
Yan
X
Li
M
Jiang
M
, et al.  . 
Clinical characteristics of 45 patients with invasive pulmonary aspergillosis: retrospective analysis of 1711 lung cancer cases
Cancer
 , 
2009
, vol. 
115
 (pg. 
5018
-
5025
)
9.
Chan
CM
Woo
PC
Leung
AS
, et al.  . 
Detection of antibodies specific to an antigenic cell wall galactomannoprotein for serodiagnosis of Aspergillus fumigatus aspergillosis
J Clin Microbiol
 , 
2002
, vol. 
40
 (pg. 
2041
-
2045
)
10.
Sridhar
H
Jayshree
RS
Bapsy
PP
, et al.  . 
Invasive aspergillosis in cancer
Mycoses
 , 
2002
, vol. 
45
 (pg. 
358
-
363
)
11.
George
B
Mathews
V
Srivastava
A
Chandy
M
Infections among allogeneic bone marrow transplant recipients in India
Bone Marrow Transplant
 , 
2004
, vol. 
33
 (pg. 
311
-
315
)
12.
Srivastava
VM
Krishnaswami
H
Srivastava
A
Dennison
D
Chandy
M
Infections in haematological malignancies: an autopsy study of 72 cases
Trans R Soc Trop Med Hyg
 , 
1996
, vol. 
90
 (pg. 
406
-
408
)
13.
Pongbhaesaj
P
Dejthevaporn
C
Tunlayadechanont
S
, et al.  . 
Aspergillosis of the central nervous system: a catastrophic opportunistic infection
Southeast Asian J Trop Med Public Health
 , 
2004
, vol. 
35
 (pg. 
119
-
125
)
14.
Pornsuriyasak
P
Murgu
S
Colt
H
Pseudomembranous Aspergillus tracheobronchitis superimposed on post-tuberculosis tracheal stenosis
Respirology
 , 
2009
, vol. 
14
 (pg. 
144
-
147
)
15.
Kiertiburanakul
S
Thibbadee
C
Santanirand
P
Invasive aspergillosis in a tertiary-care hospital in Thailand
J Med Assoc Thai
 , 
2007
, vol. 
90
 (pg. 
895
-
902
)
16.
Suankratay
C
Kanitcharaskul
P
Arunyingmongkol
K
Galactomannan antigenemia for the diagnosis of invasive aspergillosis in neutropenic patients with hematological disorders
J Med Assoc Thai
 , 
2006
, vol. 
89
 (pg. 
1851
-
1858
)
17.
Hashmi
KU
Ahmed
P
Satti
TM
, et al.  . 
Cutaneous aspergillosis as a first manifestation of systemic infection in allogeneic haematopoietic stem cell transplantation
J Pak Med Assoc
 , 
2007
, vol. 
57
 (pg. 
324
-
326
)
18.
Wasay
M
Patel
J
Azam
I
Khan
MA
Smego
RA
Jr
Preoperative antifungal therapy may improve survival in patients with Aspergillus brain abscess
Clin Neurol Neurosurg
 , 
2009
, vol. 
111
 (pg. 
565
-
567
)
19.
Mekan
SF
Saeed
O
Khan
JA
Invasive aspergillosis with polyarthritis
Mycoses
 , 
2004
, vol. 
47
 (pg. 
518
-
520
)
20.
Ur-Rahman
N
Jamjoom
ZA
Jamjoom
A
Spinal aspergillosis in nonimmunocompromised host mimicking Pott's paraplegia
Neurosurg Rev
 , 
2000
, vol. 
23
 (pg. 
107
-
111
)
21.
Hussain
S
Salahuddin
N
Ahmad
I
Salahuddin
I
Jooma
R
Rhinocerebral invasive mycosis: occurrence in immunocompetent individuals
Eur J Radiol
 , 
1995
, vol. 
20
 (pg. 
151
-
155
)
22.
Badiee
P
Kordbacheh
P
Alborzi
A
, et al.  . 
Prospective screening in liver transplant recipients by panfungal PCR-ELISA for early diagnosis of invasive fungal infections
Liver Transpl
 , 
2007
, vol. 
13
 (pg. 
1011
-
1016
)
23.
Badiee
P
Alborzi
A
Shakiba
E
Ziyaeyan
M
Pourabbas
B
Molecular diagnosis of Aspergillus endocarditis after cardiac surgery
J Med Microbiol
 , 
2009
, vol. 
58
 (pg. 
192
-
195
)
24.
Azarpira
N
Esfandiari
M
Bagheri
MH
Rakei
S
Salari
S
Cerebral aspergillosis presenting as a mass lesion
Braz J Infect Dis
 , 
2008
, vol. 
12
 (pg. 
349
-
351
)
25.
Nikeghbalian
S
Salahi
R
Salahi
H
, et al.  . 
Hepatic abscesses after liver transplant: 1997-2008
Exp Clin Transplant
 , 
2009
, vol. 
7
 (pg. 
256
-
260
)
26.
Hashemi
SB
Shishegar
M
Nikeghbalian
S
, et al.  . 
Endogenous Aspergillus endophthalmitis occurring after liver transplantation: a case report
Transplant Proc
 , 
2009
, vol. 
41
 (pg. 
2933
-
2935
)
27.
Hosseini
H
Saki
S
Saki
N
Eghtedari
M
Aspergillus endophthalmitis in orthotopic liver transplantation
Indian J Med Sci
 , 
2009
, vol. 
63
 (pg. 
253
-
256
)
28.
Sharifipour
F
Rezaeetalab
F
Naghibi
M
Pulmonary fungal infections in kidney transplant recipients: an 8-year study
Transplant Proc
 , 
2009
, vol. 
41
 (pg. 
1654
-
1656
)
29.
Najafizadeh
K
Daneshvar
A
Dezfouli
AA
, et al.  . 
Pulmonary artery stenosis shortly after lung transplantation: successful balloon dilation and stent insertion in one case
Ann Transplant
 , 
2009
, vol. 
14
 (pg. 
52
-
55
)
30.
Ghotaslou
R
Parvizi
R
Safaei
N
Yousefi
S
A case of Aspergillus fumigatus mediastinitis after heart surgery in Madani Heart Center, Tabriz, Iran
Prog Cardiovasc Nurs
 , 
2008
, vol. 
23
 (pg. 
133
-
135
)
31.
Badiee
P
Kordbacheh
P
Alborzi
A
, et al.  . 
Study on invasive fungal infections in immunocompromised patients to present a suitable early diagnostic procedure
Int J Infect Dis
 , 
2009
, vol. 
13
 (pg. 
97
-
102
)
32.
Badiee
P
Kordbacheh
P
Alborzi
A
Malekhoseini
SA
Invasive fungal infection in renal transplant recipients demonstrated by panfungal polymerase chain reaction
Exp Clin Transplant
 , 
2007
, vol. 
5
 (pg. 
624
-
629
)
33.
Bassiri Jahromi
S
Khaksar
AA
Deep-seated fungal infections in immunocompromised patients in iran
Iran J Allergy Asthma Immunol
 , 
2005
, vol. 
4
 (pg. 
27
-
32
)
34.
Farhoudi
A
Siadati
A
Atarod
L
, et al.  . 
Para vertebral abscess and rib osteomyelitis due to Aspergillus fumigatus in a patient with chronic granulomatous disease
Iran J Allergy Asthma Immunol
 , 
2003
, vol. 
2
 (pg. 
13
-
15
)
35.
Navabi
MA
Ajami
H
Amirghofran
A
Peyravian
F
Aspergillus endocarditis: rare but serious Aspergillus ball obstructing the pulmonary artery
Eur J Cardiothorac Surg
 , 
1998
, vol. 
14
 (pg. 
530
-
532
)
36.
Kallenbach
J
Dusheiko
J
Block
CS
, et al.  . 
Aspergillus pneumonia—a cluster of four cases in an intensive care unit
S Afr Med J
 , 
1977
, vol. 
52
 (pg. 
919
-
923
)
37.
Govender
S
Kumar
KP
Aspergillus spondylitis in immunocompetent patients
Int Orthop
 , 
2001
, vol. 
25
 (pg. 
74
-
76
)
38.
Stemmet
F
Davies
JQ
von Oppell
UO
Postpneumonectomy aortic arch mycotic aneurysm
Ann Thorac Surg
 , 
2001
, vol. 
71
 (pg. 
1030
-
1032
)
39.
Govender
S
Rajoo
R
Goga
IE
Charles
RW
Aspergillus osteomyelitis of the spine
Spine (Phila Pa 1976)
 , 
1991
, vol. 
16
 (pg. 
746
-
749
)
40.
Lowe
J
Bradley
J
Cerebral and orbital Aspergillus infection due to invasive aspergillosis of ethmoid sinus
J Clin Pathol
 , 
1986
, vol. 
39
 (pg. 
774
-
778
)
41.
Chamsi-Pasha
H
Abdulmoneim
A
Ahmed
WH
, et al.  . 
Biatrial aspergillosis in a patient with immunocompetency
J Am Soc Echocardiogr
 , 
2004
, vol. 
17
 (pg. 
70
-
72
)
42.
Alrajhi
AA
Enani
M
Mahasin
Z
Al-Omran
K
Chronic invasive aspergillosis of the paranasal sinuses in immunocompetent hosts from Saudi Arabia
Am J Trop Med Hyg
 , 
2001
, vol. 
65
 (pg. 
83
-
86
)
43.
Abu el-Asrar
AM
al-Amro
SA
al-Mosallam
AA
al-Obeidan
S
Post-traumatic endophthalmitis: causative organisms and visual outcome
Eur J Ophthalmol
 , 
1999
, vol. 
9
 (pg. 
21
-
31
)
44.
Jamjoom
AB
al-Hedaithy
SA
Jamjoom
ZA
, et al.  . 
Intracranial mycotic infections in neurosurgical practice
Acta Neurochir (Wien)
 , 
1995
, vol. 
137
 (pg. 
78
-
84
)
45.
Al-Tawfiq
JA
Al-Abdely
HM
Vertebral osteomyelitis due to Aspergillus fumigatus in a patient with chronic granulomatous disease successfully treated with antifungal agents and interferon-gamma
Med Mycol
 , 
2010
, vol. 
48
 (pg. 
537
-
541
)
46.
Bukhari
E
Alrabiaah
A
First case of extensive spinal cord infection with Aspergillus nidulans in a child with chronic granulomatous disease
J Infect Dev Ctries
 , 
2009
, vol. 
3
 (pg. 
321
-
323
)
47.
Gunaratne
PS
Wijeyaratne
CN
Seneviratne
HR
Aspergillus meningitis in Sri Lanka — a post-tsunami effect?
N Engl J Med
 , 
2007
, vol. 
356
 (pg. 
754
-
756
)
48.
Lokuhetty
MD
Wijesinghe
HD
Weerasundera
B
Dayapala
A
Iatrogenic Aspergillus infection of the central nervous system in a pregnant woman
Indian J Pathol Microbiol
 , 
2009
, vol. 
52
 (pg. 
427
-
429
)
49.
Rodrigo
N
Perera
KN
Ranwala
R
, et al.  . 
Aspergillus meningitis following spinal anaesthesia for caesarean section in Colombo, Sri Lanka
Int J Obstet Anesth
 , 
2007
, vol. 
16
 (pg. 
256
-
260
)
50.
El-Mahallawy
HA
Shaker
HH
Ali Helmy
H
Mostafa
T
Razak Abo-Sedah
A
Evaluation of pan-fungal PCR assay and Aspergillus antigen detection in the diagnosis of invasive fungal infections in high risk paediatric cancer patients
Med Mycol
 , 
2006
, vol. 
44
 (pg. 
733
-
739
)
51.
Salman
AG
Mansour
DE
Radwan
AA
Mansour
LE
Polymerase chain reaction in pediatric post-traumatic fungal endophthalmitis among Egyptian children
Ocul Immunol Inflamm
 , 
2010
, vol. 
18
 (pg. 
127
-
132
)
52.
Selim
HS
Hammouda
AF
Sadek
NA
Ahmed
MA
Al-Kadassy
AM
Fungal Infection among Patients with Some Hematopoietic Disorders
J Egypt Public Health Assoc
 , 
2006
, vol. 
81
 (pg. 
321
-
336
)
53.
Mamishi
S
Zomorodian
K
Saadat
F
, et al.  . 
A case of invasive aspergillosis in CGD patient successfully treated with Amphotericin B and INF-gamma
Ann Clin Microbiol Antimicrob
 , 
2005
, vol. 
4
 pg. 
4
 
54.
Shoar
MG
Zomorodian
K
Saadat
F
Hashemi
MJ
Tarazoei
B
Fatal endocarditis due to Aspergillus flavus in Iran
J Pak Med Assoc
 , 
2004
, vol. 
54
 (pg. 
485
-
486
)
55.
Nikeghbalian
S
Malek-Hosseini
SA
Salahi
H
, et al.  . 
Pancreas transplantation in Shiraz organ transplant center; the first Iranian experience
Arch Iran Med
 , 
2008
, vol. 
11
 (pg. 
490
-
496
)
56.
Geramizadeh
B
Kheirandish
P
Fatheezadeh
P
Jannesar
R
Fine needle aspiration of subcutaneous masses caused by Aspergillus: a report of 2 cases
Acta Cytol
 , 
2005
, vol. 
49
 (pg. 
666
-
668
)
57.
Martinez
R
Castro
G
Machado
AA
Moya
MJ
Primary aspergilloma and subacute invasive aspergillosis in two AIDS patients
Rev Inst Med Trop Sao Paulo
 , 
2009
, vol. 
51
 (pg. 
49
-
52
)
58.
Orzechowski Xavier
M
Pasqualotto
AC
Uchoa Sales Mda
P
, et al.  . 
Invasive pulmonary aspergillosis due to a mixed infection caused by Aspergillus flavus and Aspergillus fumigatus
Rev Iberoam Micol
 , 
2008
, vol. 
25
 (pg. 
176
-
178
)
59.
Carvalho-Dias
VM
Sola
CB
Cunha
CA
, et al.  . 
Invasive aspergillosis in hematopoietic stem cell transplant recipients: a retrospective analysis
Braz J Infect Dis
 , 
2008
, vol. 
12
 (pg. 
385
-
389
)
60.
Quadrelli
SA
Alvarez
C
Arce
SC
, et al.  . 
Pulmonary involvement of systemic lupus erythematosus: analysis of 90 necropsies
Lupus
 , 
2009
, vol. 
18
 (pg. 
1053
-
1060
)
61.
Cuccia
V
Galarza
M
Monges
J
Cerebral aspergillosis in children. Report of three cases
Pediatr Neurosurg
 , 
2000
, vol. 
33
 (pg. 
43
-
48
)
62.
Galluzzo
ML
Hernandez
C
Davila
MT
, et al.  . 
Clinical and histopathological features and a unique spectrum of organisms significantly associated with chronic granulomatous disease osteomyelitis during childhood
Clin Infect Dis
 , 
2008
, vol. 
46
 (pg. 
745
-
749
)
63.
Stalldecker
G
Molina
HA
Antelo
N
, et al.  . 
Hypopituitarism caused by colonic carcinoma metastasis associated with hypophysial aspergillosis
Medicina (B Aires)
 , 
1994
, vol. 
54
 (pg. 
248
-
252
)
64.
Metta
H
Corti
M
Redini
L
, et al.  . 
Renal abscess due to Aspergillus fumigatus as the only sign of disseminated aspergillosis in a patient with AIDS
Rev Iberoam Micol
 , 
2010
 
[Epub ahead of print] PubMed PMID: 20346298.
65.
Galimberti
R
Kowalczuk
A
Hidalgo Parra
I
Gonzalez Ramos
M
Flores
V
Cutaneous aspergillosis: a report of six cases
Br J Dermatol
 , 
1998
, vol. 
139
 (pg. 
522
-
526
)
66.
Lashley
PM
Callender
DP
Graham
AC
Gopwani
H
Garriques
S
Aspergillosis in a patient with acute lymphoblastic leukaemia
West Indian Med J
 , 
1991
, vol. 
40
 (pg. 
37
-
40
)
67.
Tomashefski
JF
Jr.
Butler
T
Islam
M
Histopathology and etiology of childhood pneumonia: an autopsy study of 93 patients in Bangladesh
Pathology
 , 
1989
, vol. 
21
 (pg. 
71
-
78
)
68.
Casal
RF
Adachi
R
Jimenez
CA
, et al.  . 
Diagnosis of invasive Aspergillus tracheobronchitis facilitated by endobronchial ultrasound-guided transbronchial needle aspiration: a case report
J Med Case Reports
 , 
2009
, vol. 
3
 pg. 
9290
 
69.
Spasova
MI
Grudeva-Popova
JG
Genev
ED
, et al.  . 
Pseudomembranous necrotizing tracheobronchitis caused by Aspergillus spp. — contribution of one case with acute myeloid leukemia
Folia Med (Plovdiv)
 , 
2006
, vol. 
48
 (pg. 
93
-
97
)
70.
Parada
MT
Alba
A
Sepulveda
C
Early and late infections in lung transplantation patients
Transplant Proc
 , 
2010
, vol. 
42
 (pg. 
333
-
335
)
71.
Rabagliati
BR
Fuentes
LG
Guzman
DA
, et al.  . 
Invasive fungal disease in hemato-oncological and hematopoietic stem cell transplantation patients from Hospital Clinico Universidad Catolica, Santiago-Chile using revised EORTC/MSG diagnostic criteria
Rev Chilena Infectol
 , 
2009
, vol. 
26
 (pg. 
212
-
219
)
72.
Pilleux
L
Ponticas
M
Carrasco
C
, et al.  . 
Invasive hepatosplenic hyalohyphomycosis. Report of a case
Rev Med Chil
 , 
2000
, vol. 
128
 (pg. 
641
-
646
)
73.
Cardenas
MX
Cortes
JA
Parra
CM
Aspergillus spp. in risk areas of transplant patients in a university hospital
Rev Iberoam Micol
 , 
2008
, vol. 
25
 (pg. 
232
-
236
)
74.
Blazicevich-Carrillo
L
Cabrales-Camacho
LM
Carrizosa
J
Cornejo
W
Clinical and radiological findings in two cases of aspergillosis of the central nervous system in children
Rev Neurol
 , 
2003
, vol. 
36
 (pg. 
632
-
635
)
75.
Marinovic
T
Skrlin
J
Vilendecic
M
Rotim
K
Grahovac
G
Multiple Aspergillus brain abscesses in immuno-competent patient with severe cranio-facial trauma
Acta Neurochir (Wien)
 , 
2007
, vol. 
149
 (pg. 
629
-
632
)
76.
Jandrlic
M
Kalenic
S
Labar
B
, et al.  . 
An autopsy study of systemic fungal infections in patients with hematologic malignancies
Eur J Clin Microbiol Infect Dis
 , 
1995
, vol. 
14
 (pg. 
768
-
774
)
77.
Jarv
H
Lehtmaa
J
Summerbell
RC
, et al.  . 
Isolation of Neosartorya pseudofischeri from blood: first hint of pulmonary Aspergillosis
J Clin Microbiol
 , 
2004
, vol. 
42
 (pg. 
925
-
928
)
78.
Krivan
G
Sinko
J
Nagy
IZ
, et al.  . 
Successful combined antifungal salvage therapy with liposomal amphothericin B and caspofungin for invasive Aspergillus flavus infection in a child following allogeneic bone marrow transplantation
Acta Biomed
 , 
2006
, vol. 
77
 
(Suppl. 2)
(pg. 
17
-
21
)
79.
Sinko
J
Csomor
J
Nikolova
R
, et al.  . 
Invasive fungal disease in allogeneic hematopoietic stem cell transplant recipients: an autopsy-driven survey
Transpl Infect Dis
 , 
2008
, vol. 
10
 (pg. 
106
-
109
)
80.
Mousa
HA
Fungal infection of burn wounds in patients with open and occlusive treatment methods
East Mediterr Health J
 , 
1999
, vol. 
5
 (pg. 
333
-
336
)
81.
Ramos-Gabatin
A
Jordan
RM
Primary pituitary aspergillosis responding to transsphenoidal surgery and combined therapy with amphotericin-B and 5-fluorocytosine: case report
J Neurosurg
 , 
1981
, vol. 
54
 (pg. 
839
-
841
)
82.
Said
T
Nampoory
MR
Nair
MP
, et al.  . 
Safety of caspofungin for treating invasive nasal sinus aspergillosis in a kidney transplant recipient
Transplant Proc
 , 
2005
, vol. 
37
 (pg. 
3038
-
3040
)
83.
Khan
ZU
Chugh
TD
Invasive fungal infections in Kuwait: A retrospective study
Indian J Chest Dis Allied Sci
 , 
2000
, vol. 
42
 (pg. 
279
-
287
)
84.
Khan
ZU
Sanyal
SC
Mokaddas
E
, et al.  . 
Endocarditis due to Aspergillus flavus
Mycoses
 , 
1997
, vol. 
40
 (pg. 
213
-
217
)
85.
Traboulsi
RS
Kattar
MM
Dbouni
O
Araj
GF
Kanj
SS
Fatal brain infection caused by Aspergillus glaucus in an immunocompetent patient identified by sequencing of the ribosomal 18S-28S internal transcribed spacer
Eur J Clin Microbiol Infect Dis
 , 
2007
, vol. 
26
 (pg. 
747
-
750
)
86.
Abu Jawdeh
L
Haidar
R
Bitar
F
, et al.  . 
Aspergillus vertebral osteomyelitis in a child with a primary monocyte killing defect: response to GM-CSF therapy
J Infect
 , 
2000
, vol. 
41
 (pg. 
97
-
100
)
87.
Khatri
ML
Stefanato
CM
Benghazeil
M
, et al.  . 
Cutaneous and paranasal aspergillosis in an immunocompetent patient
Int J Dermatol
 , 
2000
, vol. 
39
 (pg. 
853
-
856
)
88.
Kaltenis
P
Mudeniene
V
Maknavicius
S
Seinin
D
Renal amyloidosis in a child with chronic granulomatous disease and invasive aspergillosis
Pediatr Nephrol
 , 
2008
, vol. 
23
 (pg. 
831
-
834
)
89.
Vivas
C
Endocarditis caused by Aspergillus niger: case report
Clin Infect Dis
 , 
1998
, vol. 
27
 (pg. 
1322
-
1323
)
90.
Gaytan-Martinez
J
Mateos-Garcia
E
Sanchez-Cortes
E
, et al.  . 
Microbiological findings in febrile neutropenia
Arch Med Res
 , 
2000
, vol. 
31
 (pg. 
388
-
392
)
91.
Rojas-Serrano
J
Pedroza
J
Regalado
J
, et al.  . 
High prevalence of infections in patients with systemic lupus erythematosus and pulmonary haemorrhage
Lupus
 , 
2008
, vol. 
17
 (pg. 
295
-
299
)
92.
Boutarbouch
M
Arkha
Y
El Ouahabi
A
Derraz
S
El Khamlichi
A
Sphenoid sinus aspergillosis simulating pituitary tumor in immunocompetent patient
J Clin Neurosci
 , 
2009
, vol. 
16
 (pg. 
840
-
841
)
93.
Akhaddar
A
Gazzaz
M
Albouzidi
A
, et al.  . 
Invasive Aspergillus terreus sinusitis with orbitocranial extension: case report
Surg Neurol
 , 
2008
, vol. 
69
 (pg. 
490
-
495
)
94.
Raja
NS
Singh
NN
Disseminated invasive aspergillosis in an apparently immunocompetent host
J Microbiol Immunol Infect
 , 
2006
, vol. 
39
 (pg. 
73
-
77
)
95.
Gupta
PK
Mahapatra
AK
Gaind
R
, et al.  . 
Aspergillus spinal epidural abscess
Pediatr Neurosurg
 , 
2001
, vol. 
35
 (pg. 
18
-
23
)
96.
Teisseyre
J
Kalicinski
P
Markiewicz-Kijewska
M
, et al.  . 
Aspergillosis in children after liver transplantation: Single center experience
Pediatr Transplant
 , 
2007
, vol. 
11
 (pg. 
868
-
875
)
97.
Stodulski
D
Kowalska
B
Stankiewicz
C
Otogenic skull base osteomyelitis caused by invasive fungal infection. Case report and literature review
Eur Arch Otorhinolaryngol
 , 
2006
, vol. 
263
 (pg. 
1070
-
1076
)
98.
Konduracka
E
Opportunistic fungal infections in patients treated with heart transplantation — own centre experiences
Ann Transplant
 , 
1998
, vol. 
3
 (pg. 
21
-
24
)
99.
Hadrich
I
Makni
F
Sellami
H
, et al.  . 
Invasive aspergillosis: epidemiology and environmental study in haematology patients (Sfax, Tunisia)
Mycoses
 , 
2009
 
[Epub ahead of print] PubMed PMID: 19500260.
100.
Saracli
MA
Mutlu
FM
Yildiran
ST
, et al.  . 
Clustering of invasive Aspergillus ustus eye infections in a tertiary care hospital: a molecular epidemiologic study of an uncommon species
Med Mycol
 , 
2007
, vol. 
45
 (pg. 
377
-
384
)
101.
Ozhak-Baysan
B
Alastruey-Izquierdo
A
Saba
R
, et al.  . 
Aspergillus alliaceus and Aspergillus flavus co-infection in an acute myeloid leukemia patient
Med Mycol
 , 
2010
 
[Epub ahead of print] PubMed PMID: 20392148.
102.
Tigen
E
Tigen
K
Karaahmet
T
Odabasi
Z
Korten
V
Concomitant Aspergillus and cytomegalovirus infection in heart transplant: early diagnosis is the key to successful treatment
Exp Clin Transplant
 , 
2009
, vol. 
7
 (pg. 
168
-
172
)
103.
Ozcan
D
Gulec
AT
Haberal
M
Multiple subcutaneous nodules leading to the diagnosis of pulmonary aspergillosis in a renal transplant recipient
Clin Transplant
 , 
2008
, vol. 
22
 (pg. 
120
-
123
)
104.
Turgut
M
Ozsunar
Y
Oncu
S
, et al.  . 
Invasive fungal granuloma of the brain caused by Aspergillus fumigatus: a case report and review of the literature
Surg Neurol
 , 
2008
, vol. 
69
 (pg. 
169
-
174
)
105.
Ersoy
A
Akdag
I
Akalin
H
Sarisozen
B
Ener
B
Aspergillosis osteomyelitis and joint infection in a renal transplant recipient
Transplant Proc
 , 
2007
, vol. 
39
 (pg. 
1662
-
1663
)
106.
Alioglu
B
Avci
Z
Canan
O
, et al.  . 
Invasive esophageal aspergillosis associated with acute myelogenous leukemia: successful therapy with combination caspofungin and liposomal amphotericin B
Pediatr Hematol Oncol
 , 
2007
, vol. 
24
 (pg. 
63
-
68
)
107.
Yildiran
ST
Mutlu
FM
Saracli
MA
, et al.  . 
Fungal endophthalmitis caused by Aspergillus ustus in a patient following cataract surgery
Med Mycol
 , 
2006
, vol. 
44
 (pg. 
665
-
669
)
108.
Ali
R
Ozkalemkas
F
Ozcelik
T
, et al.  . 
Invasive pulmonary aspergillosis: role of early diagnosis and surgical treatment in patients with acute leukemia
Ann Clin Microbiol Antimicrob
 , 
2006
, vol. 
5
 pg. 
17
 
109.
Gulen
H
Erbay
A
Gulen
F
, et al.  . 
Sinopulmonary aspergillosis in children with hematological malignancy
Minerva Pediatr
 , 
2006
, vol. 
58
 (pg. 
319
-
324
)
110.
Oner
AY
Celik
H
Akpek
S
Tokgoz
N
Central nervous system aspergillosis: magnetic resonance imaging, diffusion-weighted imaging, and magnetic resonance spectroscopy features
Acta Radiol
 , 
2006
, vol. 
47
 (pg. 
408
-
412
)
111.
Polat
G
Urpek
G
Yilmaz
U
, et al.  . 
Successful treatment of invasive pulmonary aspergillosis in an immunocompetent host
Respirology
 , 
2005
, vol. 
10
 (pg. 
393
-
395
)
112.
Usta
M
Kahvecioglu
S
Akdag
I
, et al.  . 
Aspergillus pneumonia in renal transplant recipients at a medical center in Turkey
Transplant Proc
 , 
2004
, vol. 
36
 (pg. 
2703
-
2707
)
113.
Iplikcioglu
AC
Bek
S
Bikmaz
K
Ceylan
D
Gokduman
CA
Aspergillus pituitary abscess
Acta Neurochir (Wien)
 , 
2004
, vol. 
146
 (pg. 
521
-
524
)
114.
Dogan
M
Pabuccuoglu
U
Sarioglu
S
Yucesoy
M
Isolated nasopharyngeal aspergillosis caused by A. flavus and associated with oxalosis
Ear Nose Throat J
 , 
2004
, vol. 
83
 (pg. 
331
-
333
)
115.
Davutoglu
V
Soydinc
S
Aydin
A
Karakok
M
Rapidly advancing invasive endomyocardial aspergillosis
J Am Soc Echocardiogr
 , 
2005
, vol. 
18
 (pg. 
185
-
187
)
116.
Bozbuga
N
Erentug
V
Erdogan
HB
, et al.  . 
Surgical treatment of aortic abscess and fistula
Tex Heart Inst J
 , 
2004
, vol. 
31
 (pg. 
382
-
386
)
117.
Kocazeybek
B
Sonmez
B
Sarman
K
, et al.  . 
Diagnosis at first glance: hairy black colonies in resected prosthetic aortic valve
Clin Microbiol Infect
 , 
2000
, vol. 
6
 (pg. 
617
-
618
)
118.
Altiparmak
MR
Apaydin
S
Trablus
S
, et al.  . 
Systemic fungal infections after renal transplantation
Scand J Infect Dis
 , 
2002
, vol. 
34
 (pg. 
284
-
288
)
119.
Veress
B
Malik
OA
el-Tayeb
AA
, et al.  . 
Further observations on the primary paranasal Aspergillus granuloma in the Sudan: a morphological study of 46 cases
Am J Trop Med Hyg
 , 
1973
, vol. 
22
 (pg. 
765
-
772
)
120.
Dufour
X
Kauffmann-Lacroix
C
Roblot
F
, et al.  . 
Chronic invasive fungal rhinosinusitis: two new cases and review of the literature
Am J Rhinol
 , 
2004
, vol. 
18
 (pg. 
221
-
226
)
121.
Kameswaran
M
al-Wadei
A
Khurana
P
Okafor
BC
Rhinocerebral aspergillosis
J Laryngol Otol
 , 
1992
, vol. 
106
 (pg. 
981
-
985
)
122.
Yagi
HI
Gumaa
SA
Shumo
AI
Abdalla
N
Gadir
AA
Nasosinus aspergillosis in Sudanese patients: clinical features, pathology, diagnosis, and treatment
J Otolaryngol
 , 
1999
, vol. 
28
 (pg. 
90
-
94
)
123.
Brun
S
Fekkar
A
Busse
A
, et al.  . 
Aspergillus flavus brain abscesses associated with hepatic amebiasis in a non-neutropenic man in Senegal
Am J Trop Med Hyg
 , 
2009
, vol. 
81
 (pg. 
583
-
586
)
124.
McLeod
DT
Neill
P
Robertson
VJ
, et al.  . 
Pulmonary diseases in patients infected with the human immunodeficiency virus in Zimbabwe, Central Africa
Trans R Soc Trop Med Hyg
 , 
1989
, vol. 
83
 (pg. 
694
-
697
)
125.
Gupta
K
Das
A
Joshi
K
, et al.  . 
Aspergillus endocarditis in a known case of allergic bronchopulmonary aspergillosis: an autopsy report
Cardiovasc Pathol
 , 
2009
 
[Epub ahead of print] PubMed PMID: 19211274.
126.
Vaideeswar
P
Prasad
S
Deshpande
JR
Pandit
SP
Invasive pulmonary aspergillosis: a study of 39 cases at autopsy
J Postgrad Med
 , 
2004
, vol. 
50
 (pg. 
21
-
26
)
127.
Chakrabarti
A
Shivaprakash
MR
Singh
R
, et al.  . 
Fungal endophthalmitis: fourteen years' experience from a center in India
Retina
 , 
2008
, vol. 
28
 (pg. 
1400
-
1407
)
128.
Wu
N
Huang
Y
Li
Q
, et al.  . 
Isolated invasive Aspergillus tracheobronchitis: a clinical study of 19 cases
Clin Microbiol Infect
 , 
2009
 
[Epub ahead of print] PubMed PMID: 19689467.
129.
Shek
WH
Chan
KL
Luk
IS
Experience of invasive aspergillosis in Hong Kong
J Clin Pathol
 , 
1992
, vol. 
45
 pg. 
183
 
130.
de Medeiros
CR
Dantas da Cunha
A
Jr.
Pasquini
R
Arns da Cunha
C
Primary renal aspergillosis: extremely uncommon presentation in patients treated with bone marrow transplantation
Bone Marrow Transplant
 , 
1999
, vol. 
24
 (pg. 
113
-
114
)
131.
Mamishi
S
Parvaneh
N
Salavati
A
Abdollahzadeh
S
Yeganeh
M
Invasive aspergillosis in chronic granulomatous disease: report of 7 cases
Eur J Pediatr
 , 
2007
, vol. 
166
 (pg. 
83
-
84
)
132.
Siu
YP
Leung
KT
Tong
MK
, et al.  . 
Fatal case of Aspergillus coinfection in a renal transplant recipient suffering from cytomegalovirus pneumonitis
Nephrology
 , 
2005
, vol. 
10
 (pg. 
619
-
622
)
133.
Sever
MS
Ecder
T
Aydin
AE
, et al.  . 
Living unrelated (paid) kidney transplantation in Third-World countries: high risk of complications besides the ethical problem
Nephrol Dial Transplant
 , 
1994
, vol. 
9
 (pg. 
350
-
354
)
134.
Boon
AP
Adams
DH
Buckels
J
McMaster
P
Cerebral aspergillosis in liver transplantation
J Clin Pathol
 , 
1990
, vol. 
43
 (pg. 
114
-
118
)
135.
Kohli
U
Sahu
J
Lodha
R
Agarwal
N
Ray
R
Invasive nosocomial aspergillosis associated with heart failure and complete heart block following recovery from dengue shock syndrome
Pediatr Crit Care Med
 , 
2007
, vol. 
8
 (pg. 
389
-
391
)
136.
Singh
N
Pruett
TL
Houston
S
, et al.  . 
Invasive aspergillosis in the recipients of liver retransplantation
Liver Transpl
 , 
2006
, vol. 
12
 (pg. 
1205
-
1209
)
137.
Hu
YR
Hu
AR
Analysis of risk factors of patients with chronic liver failure complicated invasive fungal infections
Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi
 , 
2009
, vol. 
23
 (pg. 
214
-
217
)
138.
Su
HB
Wang
HF
Lin
F
, et al.  . 
Retrospective study of liver failure complicated with bacterium and fungus infection
Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi
 , 
2007
, vol. 
21
 (pg. 
229
-
231
)
139.
El-Serag
HB
Anand
B
Richardson
P
Rabeneck
L
Association between hepatitis C infection and other infectious diseases: a case for targeted screening?
Am J Gastroenterol
 , 
2003
, vol. 
98
 (pg. 
167
-
174
)
140.
Walsh
TJ
Hamilton
SR
Disseminated aspergillosis complicating hepatic failure
Arch Intern Med
 , 
1983
, vol. 
143
 (pg. 
1189
-
1191
)
141.
Zhan
QY
He
HY
Tong
ZH
, et al.  . 
Clinical features of invasive pulmonary aspergillosis in critically ill patients with chronic respiratory diseases
Zhonghua Jie He He Hu Xi Za Zhi
 , 
2008
, vol. 
31
 (pg. 
282
-
286
)
142.
Cabral
FC
Marchiori
E
Zanetti
G
Takayassu
TC
Mano
CM
Semi-invasive pulmonary aspergillosis in an immunosuppressed patient: a case report
Cases J
 , 
2009
, vol. 
2
 pg. 
40
 
143.
Kumar
AA
Shantha
GP
Jeyachandran
V
, et al.  . 
Multidrug resistant tuberculosis co-existing with aspergilloma and invasive aspergillosis in a 50 year old diabetic woman: a case report
Cases J
 , 
2008
, vol. 
1
 pg. 
303
 
144.
Shankar
SK
Mahadevan
A
Sundaram
C
, et al.  . 
Pathobiology of fungal infections of the central nervous system with special reference to the Indian scenario
Neurol India
 , 
2007
, vol. 
55
 (pg. 
198
-
215
)
145.
Norlinah
MI
Ngow
HA
Hamidon
BB
Angioinvasive cerebral aspergillosis presenting as acute ischaemic stroke in a patient with diabetes mellitus
Singapore Med J
 , 
2007
, vol. 
48
 (pg. 
e1
-
4
)
146.
Balasubramaniam
P
Madakira
PB
Ninan
A
Swaminathan
A
Response of central nervous system aspergillosis to voriconazole
Neurol India
 , 
2007
, vol. 
55
 (pg. 
301
-
303
)
147.
Nadkarni
T
Goel
A
Aspergilloma of the brain: an overview
J Postgrad Med
 , 
2005
, vol. 
51
 
(Suppl. 1)
(pg. 
S37
-
41
)
148.
Feng
Q
Ma
L
Gabrielle
G
Yu
GW
Use of video-assisted thoracoscopy surgery for the treatment of Aspergillus empyema with bronchopleural fistula
Thorac Cardiovasc Surg
 , 
2008
, vol. 
56
 (pg. 
370
-
372
)
149.
Chakrabarti
A
Das
A
Mandal
J
, et al.  . 
The rising trend of invasive zygomycosis in patients with uncontrolled diabetes mellitus
Med Mycol
 , 
2006
, vol. 
44
 (pg. 
335
-
342
)
150.
Sharma
BS
Khosla
VK
Kak
VK
, et al.  . 
Intracranial fungal granuloma
Surg Neurol
 , 
1997
, vol. 
47
 (pg. 
489
-
497
)
151.
Viriyavejakul
P
Phudhichareonrat
S
Boonpasat
Y
, et al.  . 
Intracerebral hemorrhage due to nosocomial aspergillosis following neurosurgery
Southeast Asian J Trop Med Public Health
 , 
1999
, vol. 
30
 (pg. 
154
-
156
)
152.
Kothari
A
Pillai
BS
Bhan
A
Pacing lead endocarditis due to Aspergillus fumigatus
Indian J Med Microbiol
 , 
2010
, vol. 
28
 (pg. 
72
-
73
)
153.
Panda
NK
Saravanan
K
Chakrabarti
A
Combination antifungal therapy for invasive aspergillosis: can it replace high-risk surgery at the skull base?
Am J Otolaryngol
 , 
2008
, vol. 
29
 (pg. 
24
-
30
)
154.
Murthy
JM
Sundaram
C
Prasad
VS
, et al.  . 
Aspergillosis of central nervous system: a study of 21 patients seen in a university hospital in south India
J Assoc Physicians India
 , 
2000
, vol. 
48
 (pg. 
677
-
681
)
155.
Brar
GS
Ram
J
Kaushik
S
, et al.  . 
Aspergillus niger endophthalmitis after cataract surgery
J Cataract Refract Surg
 , 
2002
, vol. 
28
 (pg. 
1882
-
1883
)
156.
Das
T
Vyas
P
Sharma
S
Aspergillus terreus postoperative endophthalmitis
Br J Ophthalmol
 , 
1993
, vol. 
77
 (pg. 
386
-
387
)
157.
Agarwal
M
Biswas
J
Mathur
U
Sijwali
MS
Singh
AK
Aspergillus iris granuloma in a young male: a case report with review of literature
Indian J Ophthalmol
 , 
2007
, vol. 
55
 (pg. 
73
-
74
)
158.
Balajee
SA
Lindsley
MD
Iqbal
N
, et al.  . 
Nonsporulating clinical isolate identified as Petromyces alliaceus (anamorph Aspergillus alliaceus) by morphological and sequence-based methods
J Clin Microbiol
 , 
2007
, vol. 
45
 (pg. 
2701
-
2703
)
159.
Mahgoub el
S
Mycological and serological studies on Aspergillus flavus isolated from paranasal aspergilloma in Sudan
J Trop Med Hyg
 , 
1971
, vol. 
74
 (pg. 
162
-
165
)
160.
Chakrabarti
A
Sharma
SC
Chandler
J
Epidemiology and pathogenesis of paranasal sinus mycoses
Otolaryngol Head Neck Surg
 , 
1992
, vol. 
107
 (pg. 
745
-
750
)
161.
Koshi
G
Cherian
KM
Aspergillus terreus, an uncommon fungus causing aortic root abscess and pseudoaneurysm
Indian Heart J
 , 
1995
, vol. 
47
 (pg. 
265
-
267
)
162.
Chakrabarti
A
Marak
RSK
Singhi
S
, et al.  . 
Brain Abscess due to Aspergillus nidulans
J de Mycol Medicale
 , 
2006
, vol. 
16
 (pg. 
100
-
104
)
163.
Warren
RE
Calne
RY
Bacterial and fungal infections
Liver Transplantation
 , 
1987
2nd
London
Grune and Stratton
(pg. 
331
-
364
)
164.
Kuruvilla
S
Saldanha
R
Joseph
LD
Recurrent respiratory papillomatosis complicated by aspergillosis: a case report with review of literature
J Postgrad Med
 , 
2008
, vol. 
54
 (pg. 
32
-
34
)
165.
Su
T
Li
HC
Chen
M
, et al.  . 
Invasive pulmonary aspergillosis in patients with antineutrophil cytoplasmic antibody associated vasculitis
J Clin Rheumatol
 , 
2009
, vol. 
15
 (pg. 
380
-
382
)
166.
deShazo
RD
Chapin
K
Swain
RE
Fungal sinusitis
N Engl J Med
 , 
1997
, vol. 
337
 (pg. 
254
-
259
)
167.
Chakrabarti
A
Sharma
SC
Paranasal sinus mycoses
Indian J Chest Dis Allied Sci
 , 
2000
, vol. 
42
 (pg. 
293
-
304
)
168.
Chakrabarti
A
Das
A
Panda
NK
Controversies surrounding the categorization of fungal sinusitis
Med Mycol
 , 
2009
, vol. 
47
 
(Suppl. 1)
(pg. 
S299
-
308
)
169.
Chakrabarti
A
Denning
DW
Ferguson
BJ
, et al.  . 
Fungal rhinosinusitis: a categorization and definitional schema addressing current controversies
Laryngoscope
 , 
2009
, vol. 
119
 (pg. 
1809
-
1818
)
170.
Murthy
JM
Sundaram
C
Prasad
VS
, et al.  . 
Sinocranial aspergillosis: a form of central nervous system aspergillosis in south India
Mycoses
 , 
2001
, vol. 
44
 (pg. 
141
-
145
)
171.
Sundaram
C
Goel
D
Uppin
SG
Seethajayalakshmi
S
Borgohain
R
Intracranial mycotic aneurysm due to Aspergillus species
J Clin Neurosci
 , 
2007
, vol. 
14
 (pg. 
882
-
886
)
172.
Radhakrishnan
VV
Saraswathy
A
Rout
D
Mohan
PK
Mycotic aneurysms of the intracranial vessels
Indian J Med Res
 , 
1994
, vol. 
100
 (pg. 
228
-
231
)
173.
Satish
OS
Alfred
JM
Sundaram
C
Rao
DS
Images in cardiovascular medicine. Extensive invasive cardiothoracic aspergillosis
Circulation
 , 
2006
, vol. 
114
 (pg. 
e562
-
563
)
174.
Challa
S
Prayaga
AK
Vemu
L
, et al.  . 
Fungal endocarditis: an autopsy study
Asian Cardiovasc Thorac Ann
 , 
2004
, vol. 
12
 (pg. 
95
-
98
)
175.
Radotra
BD
Chakrabarti
A
Clinicopathological discussion. Disseminated aspergillosis with ABPA
SIHAM Mycoses Newsletter
 , 
2008
, vol. 
8
 (pg. 
2
-
3
)
176.
Chaudhary
A
Jain
V
Dwivedi
RS
Misra
S
Invasive aspergillosis causing small bowel infarction in a patient of carcinoma breast undergoing chemotherapy
J Carcinog
 , 
2006
, vol. 
5
 pg. 
18
 
177.
Muda
Z
Ibrahim
H
Abdulrahman
EJ
, et al.  . 
Invasive aspergillosis in paediatric oncology patients
Med J Malaysia
 , 
2008
, vol. 
63
 (pg. 
415
-
416
)
178.
Das
A
Chakrabarti
A
Clinicopathological discussion. Disseminated aspergillosis in chronic liver disease
SIHAM Mycoses Newsletter
 , 
2009
, vol. 
9
 (pg. 
2
-
3
)
179.
Shen
X
Xu
G
Vitrectomy for endogenous fungal endophthalmitis
Ocul Immunol Inflamm
 , 
2009
, vol. 
17
 (pg. 
148
-
152
)
180.
Sihota
R
Agarwal
HC
Grover
AK
Sood
NN
Aspergillus endophthalmitis
Br J Ophthalmol
 , 
1987
, vol. 
71
 (pg. 
611
-
613
)
181.
Gupta
A
Srinivasan
R
Kaliaperumal
S
Saha
I
Post-traumatic fungal endophthalmitis — a prospective study
Eye
 , 
2008
, vol. 
22
 (pg. 
13
-
17
)
182.
Narang
S
Gupta
A
Gupta
V
, et al.  . 
Fungal endophthalmitis following cataract surgery: clinical presentation, microbiological spectrum, and outcome
Am J Ophthalmol
 , 
2001
, vol. 
132
 (pg. 
609
-
617
)
183.
Cameron
JA
Antonios
SR
Cotter
JB
Habash
NR
Endophthalmitis from contaminated donor corneas following penetrating keratoplasty
Arch Ophthalmol
 , 
1991
, vol. 
109
 (pg. 
54
-
59
)
184.
Klotz
SA
Penn
CC
Negvesky
GJ
Butrus
SI
Fungal and parasitic infections of the eye
Clin Microbiol Rev
 , 
2000
, vol. 
13
 (pg. 
662
-
685
)
185.
Chakrabarti
A
Chatterjee
SS
Radotra
BD
Pasqualotto
AC
Cutaneous and wound aspergillosis
Aspergillosis: From Diagnosis to Prevention
 , 
2010
New York
Springer
(pg. 
939
-
959
)
186.
Singh
SA
Dutta
S
Narang
A
Vaiphei
K
Cutaneous Aspergillus flavus infection in a neonate
Indian J Pediatr
 , 
2004
, vol. 
71
 (pg. 
351
-
352
)
187.
Chakrabarti
A
Gupta
V
Biswas
G
Kumar
B
Sakhuja
VK
Primary cutaneous aspergillosis: our experience in 10 years
J Infect
 , 
1998
, vol. 
37
 (pg. 
24
-
27
)
188.
Agarwal
R
Nath
A
Aggarwal
AN
Gupta
D
Chakrabarti
A
Aspergillus hypersensitivity and allergic bronchopulmonary aspergillosis in patients with acute severe asthma in a respiratory intensive care unit in North India
Mycoses
 , 
2010
, vol. 
53
 (pg. 
138
-
143
)
189.
Guan
HJ
Lu
H
Rapid pathogens diagnosis of infected keratitis and endophthalmitis using two steps polymerase chain reaction
Zhonghua Yan Ke Za Zhi
 , 
2004
, vol. 
40
 (pg. 
819
-
823
)
190.
Bagyalakshmi
R
Therese
KL
Madhavan
HN
Application of semi-nested polymerase chain reaction targeting internal transcribed spacer region for rapid detection of panfungal genome directly from ocular specimens
Indian J Ophthalmol
 , 
2007
, vol. 
55
 (pg. 
261
-
265
)
191.
Tarai
B
Gupta
A
Ray
P
Shivaprakash
MR
Chakrabarti
A
Polymerase chain reaction for early diagnosis of post-operative fungal endophthalmitis
Indian J Med Res
 , 
2006
, vol. 
123
 (pg. 
671
-
678
)
192.
Walsh
TJ
Anaissie
EJ
Denning
DW
, et al.  . 
Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America
Clin Infect Dis
 , 
2008
, vol. 
46
 (pg. 
327
-
360
)
193.
Panda
NK
Balaji
P
Chakrabarti
A
Sharma
SC
Reddy
CE
Paranasal sinus aspergillosis: its categorization to develop a treatment protocol
Mycoses
 , 
2004
, vol. 
47
 (pg. 
277
-
283
)
194.
Srinivasan
US
Intracranial aspergilloma in immunocompetent patients successfully treated with radical surgical intervention and antifungal therapy: case series
Ann Acad Med Singapore
 , 
2008
, vol. 
37
 (pg. 
783
-
787
)

This paper was first published online on Early online on 20 August 2010.