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Table of Contents
Year : 2009  |  Volume : 11  |  Issue : 1  |  Page : 25-31

Socioeconomic factors and ethnicity in the course of pediatric allergic fungal sinusitis with bone erosion in Saudi Arabia and Egypt

1 Department of ENT Surgery, El MenoufyiaUniversity, Egypt
2 Department of ENT surgery, El Iman Hospital, Riyadh, Saudi Arabia
3 Department of ENT Surgery, Riyadh, Medical Complex, Riyadh, Saudi Arabia
4 Department of ENT Surgery, Prince Salman Hospital, Riyadh, Saudi Arabia
5 Department of Radiobiology, El Menoufyia University, Egypt

Date of Web Publication7-Jan-2020

Correspondence Address:
Omar A El-Banhawy
7th floor, Borge El-Ula, El-Shoula Square, El-Mansoura, Dakahlia
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1319-8491.275322

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Objective: to study the socioeconomic factors and ethnicity in the course of pediatric allergic fungal sinusitis (AFRS) with bone erosion who underwent endo-nasal endoscopic surgery (EES) in Saudi Arabia and Egypt
Design and Setting: Descriptive retrospective review study conducted during 5 years period at the ENT Department of El Menoufyia University Hospital, Egypt, Al Iman General Hospital and Riyadh Medical complex, Saudi Arabia..
Methods:Twenty patients (age range, 5-17 years; mean age, 13.1 years; median age, 13.5 years) met previously published criteria for AFRS. Thirteen patients were males and 7 were females. Thirteen were Saudi and 7 were Egyptian. All underwent endo-nasal endoscopic surgery ( EES) after short period of oral systemic corticosteroids followed by postoperative nasal corticosteroid spray. Age, sex, presentation, preoperative serum IgE levels, radiological extent of disease, intra-operative evaluation and recurrence rates were compared in Saudi and Egyptian patients.
Result: Twelve patients (60%) presented with radiographic and intra-operative evidence of intra-orbital extension and /or ventral skull base erosion. They were 9 Saudi (7 male and 2 female) and 3 males Egyptian. Facial dysmorphism, was seen in 9 patients (45 %). Postoperative recurrence was seen in 9 patients (7 Saudi and 2 Egyptian).
Conclusion: Although Saudi AFRS patients have higher socioeconomic status than Egyptians (both belong to the same ethnic group), Saudi AFRS patients were found to have a more aggressive form of the disease with more intraorbital and/or intra-cranial extra-dural extension. These finding are in contrast with the previously published series of AFRS patients. However, further studies would be necessary before the results of these studies could be generalized worldwide.

Keywords: allergic fungal sinusitis, bone erosion, socioeconomic status .

How to cite this article:
El-Banhawy OA, El-Tuaijury M, Elkahtany B, El Amry A, ElKholy MR. Socioeconomic factors and ethnicity in the course of pediatric allergic fungal sinusitis with bone erosion in Saudi Arabia and Egypt. Saudi J Otorhinolaryngol Head Neck Surg 2009;11:25-31

How to cite this URL:
El-Banhawy OA, El-Tuaijury M, Elkahtany B, El Amry A, ElKholy MR. Socioeconomic factors and ethnicity in the course of pediatric allergic fungal sinusitis with bone erosion in Saudi Arabia and Egypt. Saudi J Otorhinolaryngol Head Neck Surg [serial online] 2009 [cited 2022 Dec 4];11:25-31. Available from: https://www.sjohns.org/text.asp?2009/11/1/25/275322

  Introduction Top

Over the past 2 decades, allergic fungal rhinosinusitis (AFRS) has become increasingly defined. It is estimated that approximately 5-10% of patients affected by chronic rhino sinusitis actually carry a diagnosis of AFRS [1].

AFRS is most common among adolescents and young adults; the mean age at diagnosis is 21.9 years [2]. Rare reports allude to a similar disease in children[3]. Presentation in pediatric patients with allergic fungal sinusitis is different from that in adults, with children having obvious abnormalities of their facial skeleton, unilateral sinus disease, and asymmetrical disease more often[4]. Findings on computed tomography scan show an equal amount of bony erosion with extension of disease [5].

Management of allergic fungal sinusitis in children has remained controversial; surgery has emerged as a universally accepted component of treatment [6]. Surgery in allergic fungal sinusitis involves removal of allergic fungal mucin from involved sinuses to reduce fungal load and provide long-term ventilation and drainage of sinuses [7].

It is believed that the incidence of AFRS appears to be influenced by demographic and socioeconomic factors [8].Literature review reveals that the majority of regions reporting cases of AFRS are sited in high temperate regions of relatively high humidity [8],[9]. However, the incidence varied remarkably on the basis of the location of reporting sites.

The aim of the present work was to study socioeconomic factors and ethnicity in the course of pediatric allergic fungal sinusitis with bone erosion who underwent endo-nasal endoscopic surgery in Saudi Arabia and Egypt.

  Patients and Methods Top

This was a retrospective study conducted during a 5 years period at the ENT Department of El Menoufyia University Hospital, Egypt, Al Iman General Hospital and Riyadh Medical Complex, Saudi Arabia. Twenty patients (age range, 5-17 years; mean age, 13.1 years; median age, 13.5 years) who met previously published criteria for AFS were included in this study. These criteria were proposed by Bent and Kuhn [10] for the diagnosis of AFS: 1- nasal polyposis; 2- allergic mucin; 3- computed tomographic (CT) scan findings consistent with chronic rhinosinusitis (CRS); 4- positive fungal histology or culture; and 5- type I hypersensitivity (atopy) diagnosed by history, positive skin test, or serology. None of the patients had received prior antifungal therapy for their sinusitis.

Data were collected for age, sex, and preoperative serum IgE level. CT scans were reviewed for presence of areas of hyper attenuation [Figure 1] and extent of disease. Based on CT scan findings, patients were classified as having bilateral or unilateral disease and ventral skull base erosion and/or intra-orbital extension.
Figure 1: A case of Saudi pediatric allergic fungal sinusitis with bone erosion: A- Plain CT, bone window, coronal view, showing heterogeneous opacification of left nasal cavity, ethmoid and maxillary sinus. Bony erosion is noted at left cribriform plate (yellow line). B: MRI (T1), for the same patient showing accumulation at the same site.

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Oral corticosteroid (prednisolone) were prescribed in a dose of 1 mg per kg / body weight (maximum 60 mg) daily dose for 5 days pre-operatively and was tapered to 10 mg daily within 1 month postoperatively.

All patients underwent endo-nasal endoscopic sinus surgery under hypotensive general anesthesia. Endoscopic ethmoidectomy, sphenoidotomy and middle meatal antrostomy with clearance of the disease was done depending upon the extent of the disease. Intraorbital and/or intra-cranial extra-dural extensions of the disease were managed endoscopically in the same sittting of surgery. The mucin removed was sent for histopathological examination in all cases and culture for fungi were done in 5 cases. Polyps and mucosa removed from involved sinuses were subjected to histopathological examination for evidence of fungal invasion.

Postoperative care included regular nasal douches with copious amount of hypertonic saline at least twice a day for 1 month. At the end of the first postoperative month, nasal corticosteroid spray (beclomethasone dipropionate), 2 puffs in each nostril twice per day, was prescribed for a period of 3 months. Endoscopic examination was done after 4, 8, and 12 weeks postoperatively; thereafter every 3 months for the follow-up period.

Patients were considered to have recurrence when symptoms persisted and postoperative endoscopic and/or when CT demonstrated one or more sinus cavity showed polypoid or edematous mucosa with or without fungal mucin leading to complete closure of 1 or more sinuses. These patients were treated with oral prednisolone 1 mg per kg for 1 week subsequently tapering to 10 mg daily dose. Endoscopic examination was done again after 1 month. Outcome of postrecurrence management was analyzed.

The data collected for age, sex, preoperative serum IgE level, extent of disease and recurrence was analyzed between those who were diagnosed and operated on in Saudi Arabia and those in Egypt.

  Results Top

Twenty pediatric patients were diagnosed with AFRS using the Bent/Kuhn criteria [10]. The youngest patient was 5 years old and the oldest was 17. The mean age of this population was 13.1 years and the median was 13.5 years. Thirteen patients were males and 7 were females. Thirteen were Saudi and 7 were Egyptian [Table 1].
Table 1: Sex, nationality, preoperative serum IgE levels, extension of the disease, facial dysmorphism and recurrences of studied pediatric allergic fungal rhionsinusitis with bone erosion in the current work.

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Clinically, all patients had nasal congestion and some degree of nasal airway obstruction, postnasal drainage, and headaches with durations ranging from several months to years. Physical examinations in both groups of patients outside the head and neck were normal. Facial dysmorphism, consisting of proptosis, telecan- thus, and malar flattening, was seen in 9 patients, 45 % (Table 1).

Total IgE values generally were elevated in all patients, often to more than 1000 U/mL (range from 650 to 2500 U/mL (mean 1441.5, and median 1355 U/mL).

All had typical heterogeneous opacification and almost uniform expansion of the affected sinuses [Figure 1]. Bilaterality was seen in 11 patients and in 9 patients the lesion was unilateral (Table 1). Twelve patients (12/20-60%) were presented with radiographic and intraoperative evidence of ventral skull base erosion and/or intra-orbital extension [Figure 2] and [Figure 3]. Nine patients had proptosis (with or without ventral skull base erosion) and 3 with ventral skull base erosion. They were 9 Saudi (7 male and 2 female) and 3 males Egyptian. The mean age of the AFRS patients with bony erosion was 13.33 years and the median was 12.5 year.
Figure 2: A case of Saudi pediatric allergic fungal sinusitis with bone erosion: A- Plain CT, bone window, axial view, showing heterogeneous opacification of bilateral nasal cavities, ethmoids, and sphenoid sinuses. Bony erosion is noted at both lamia papyrecea, lateral wall of the sphenoid sinus (yellow lines), with proptosis of the left eye. B- Sagittal reformation view of the same patient.

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Figure 3: A case of Saudi pediatric allergic fungal sinusitis with bone erosion: A- Plain CT, soft tissue window, showing heterogeneous opacification of right nasal cavity, ethmoid and maxillary sinuses. Bony erosion is noted at right cribriform plate, fovea ethmoidalis and lamina papyracea (yellow lines). B: the same patient in bone window.

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Fungal hyphae were seen in allergic fungal mucin on histopathological examination in all patients. Fungus culture from mucin removed was done in 5 cases. It showed Aspergillus flavus in 4 cases and Aspergillus fumigatus in one.

All cases were followed up for a minimum of 6 months and 14 cases were followed for more than 2 years. The maximum duration of follow-up was 48 months and the average follow-up was 18 months.

Signs of postoperative recurrence were seen in 9 patients (45%). They were 7 Saudi (6 males and one female) and 2 Egyptian (boy and girl). The distribution of sex, age, extent of disease, preoperative Ig E levels, and disease recurrence of these patients are shown in Table 1. Six patients with recurrences were among those who showed radiological and intra-operative evidence of ventral skull base erosion and/or intra-orbital extension of the disease. Recurrence was noted within 4 months of surgery in 4 patients and from 4 to 24 months in the other 4 patients. It occurred in the same sinuses reported before surgery. Patients with recurrences had received another course of oral corticosteroid followed by corticosteroid nasal spray.

  Discussion Top

AFRS has remained a diagnostic and therapeutic challenge since its first description about two decades ago. The exact pathophysiology of AFRS remains a matter of conjecture for which several theories have been offered. One popular theory proposed by Manning and colleagues [11] , is based on the assumption that AFRS exists as the nasal correlate of allergic bronchopulmonary aspergillosis, and suggests that several interrelated factors and events lead to the development and perpetuation of the disease. First, an atopic host is exposed to fungi through normal nasal respiration, thus providing an initial antigenic stimulus. Gel and Coombs type I (IgE) and III (immune complex) -mediated reactions then trigger an intense eosinophilic inflammatory response. The resulting inflammation leads to obstruction of the sinus ostia, which may be accentuated by anatomic factors such as septal deviation or turbinate hypertrophy, resulting in stasis within the sinuses. This, in turn, creates an ideal environment for further proliferation of the fungus, thus increasing the antigenic exposure. At some point this cycle becomes self-perpetuating and results in the eventual product of this process: allergic mucin, the material that fills the involved sinuses of patients with AFRS. Accumulation of allergic mucin obstructs the involved sinuses and propagates the process.

Children with AFRS appear to differ from adults in some aspects of their clinical presentation [4] . Nine patients of this work (45%) had facial dysmorphism. This finding is in agreement with a study done by Marple et al., [12] that found facial alterations in 35% of 26 pediatric patients and 11% of 56 adult patients. Proptosis (with or without telecanthus, and malar flattening) was the facial alteration noted in all 9 patients of the current study. The growing facial skeleton of the children may account for the higher degree of dysmorphism seen. Although studies note that the facial skeleton continues to grow and change into the third and even fourth decade of life, the bulk of facial growth is completed by adolescence [13]. During this time of growth, the facial skeleton is more susceptible to being altered by external forces. This principle is widely used in the treatment of pediatric and adolescent orthodontic problems [13]. Thus, the expansile forces of AFRS debris might act to create more dysmorphism in the growing facial skeletons of children by actively expand ing the more pliable bony structure.

Bony erosion with subsequent intracranial extra-dural extension associated with AFRS has previously been documented[14],[15]. They are seen much more commonly in AFRS than in all other types of inflammatory sinusitis combined. Typically, AFRS is slowly progressive and not aggressive, but has been shown to destroy bone of the orbit and skull base [14],[15],[16]. In this study there were 6 patients (5 Saudi and one Egyptian) who showed ventral skull base bony erosion (either alone or with proptosis) with intracranial extra- dural extension. These finding emphasized that AFRS must be considered in the differential diagnosis of ventral skull base masses in children. This will avoid unnecessary treatment for intracranial extra-dural disease such as craniotomy, dural resection, and systemic antifungal agents. As in this study illustrates even the most severe cases of skull base AFRS may be managed successfully with endoscopic sinus surgery [Figure 2] with systemic and topical nasal steroids. Traditional sinus surgery may be indicated for refractory maxillary or frontal sinus disease, just as in chronic non-fungal sinusitis. Biopsy to rule out neoplasia and more aggressive forms of fungal sinusitis must be performed.

Erosion by AFRS of the osseous boundaries separating the intracranial fossa from the sinonasal cavities may increase the risk of subsequent encephalocele formation. It is commonly accepted within the otologic community that dural exposure in the absence of dural injury along the tegmen mastoideum rarely results in the development of an encephaloceles [17]. None of the patients showed skull base bony erosion in the current work demonstrated encephalocele formation during the follow-up period. Unfortunately, no analogous information within the rhinologic literature exists. It is logical to assume, however, that eventual encephalocele formation may occur as a result of a combination of factors, including dural injury, location of bony dehiscence, and/or size of the bony dehiscence. Long term monitoring for development of encephaloceles may be necessary because their occurrence may require subsequent repair of the bony dehiscence.

Riyadh district, the place of this study in Saudi Arabia, has a desert climate characterized by extreme heat during the day with relative high humidity, and abrupt drop in temperature at night, and slight, erratic rainfall. The Nile Delta, the place of this study in Egypt, has a Mediterranean climate, characterized by little rainfall in the winter months. The delta experiences its hottest temperatures in July and August, averaging 30°C, with a maximum of around 45°C. Winter temperatures are normally in the range of 5° to 10°C.

In the current wok it was found that Saudi patients have a higher incidence of AFRS with intracranial extradural and intraorbital extension (9/13), and they appear to present with a more aggressive form of the disease. The incidence of AFRS appears to be impacted by geographic factors. Review of the world’s literature reveals the majority of sites reporting cases of AFRS to be located in high temperate regions with relatively high humidity [18],[9],[8]. Ferguson et al.[8] performed a questionnaire-based study within the United States to assess variations in the regional incidence of AFRS. Results of their study indicated that the incidence of AFRS varied remarkably based on the location of reporting sites and was most commonly encountered within the Mississippi basin, the Southeast, and the southwest. The reason for this geographic difference remains unexplained.

Both Saudi and Egyptian belong to the Arab group and have the same Islamic culture and Arabic language. Saudi AFRS patients were found to have a more aggressive form of the disease with more intra-orbital and/or intracranial extra-dural extension. Wise et al. [19] reported that ethnicity was a significant predictor of paranasal sinus bone erosion, with 71.4 percent of African Americans presenting with bone erosion compared with 23.1 percent of Caucasians. Although Wise et al.[9], failed to detect a significant difference in bone erosion for gender in their group of AFRS patients. Ghegan et al. [15]], found that African Americans males with AFRS were 15 times more likely to have bone erosion than Caucasians and African American females combined.

The potential contribution of socioeconomic factors to the diagnosis and progression of AFRS has not been examined extensively. Gross Domestic Product (GDP) per capita, is the value of all final goods and services produced within a nation in a given year, divided by the average population for the same year. The GDP per capita data for the year 2006 from the World Bank is US $1,449 for Egyptians and US$14,745 for Saudis (World Bank report). It is difficult to assume that the income of the 20 patients included in this study is equivalent to the average income in the country. Both countries studied have large variations in annual income amongst workers and the sample is too small to make such an extrapolation. The high level of GDP per capita for Saudis in comparison of Egyptians and knowing the type of heath care system in both countries that make a potential for decreased access to health care among Egyptian patients with more uninsured or Medicaid patients than Saudi. According to the result of this study and our accumulated experience in dealing with pediatric AFRS Saudi patients have a more aggressive than Egyptian pediatric AFRS. This in contrast to socioeconomic status including heath care system of both countries. A recent study of 20 AFRS patients from Pakistan note that 80 percent of their AFRS patients were of low socioeconomic status [8].

Although the results of this study are intriguing, potential pitfalls should be noted. First, owing to the retrospective nature of this study, limited socioeconomic information was available. We feel that the preliminary information gathered in this study and other studies[18],[9], may provide a basis for future prospective studies in which patient specific socioeconomic information may be obtained.

It is not clear from the data of this study if the increased presentation of erosion in Saudi patients is due to the disease process itself, or simply due to a referralbias.

A higher rate of recurrences were reported in most of the reports describing pediatric AFRS. In the current study postoperative recurrences were seen in 9 patients (45%). Recurrence was noted within 4 months of surgery in 4 patients and from 4 to 24 months in the other 5 patients. The reported incidence of recurrence in the literatures ranges from 10% [19] to 79% [20]. Surgery plays an important role in the treatment of allergic fungal sinusitis. Marple and Mabry[21], feel that inadequate initial surgery was an important contributory factor to recurrence in their cases. All of the endo-nasal endoscopic surgery of this work were done or supervised by the senior author, who is a rhinologist specialized in endoscopic endo-nasal surgery. We were able to achieve complete surgical removal of mucin and satisfactory marsupialization of involved sinuses in all cases. Schubert and Goetz [18], found 35% recurrence rate at one year after initial surgery in patients treated with oral corticosteroids. Kuhn and Javer [20], have reported recurrence in 8 of 11 patients within 27 months in spite of systemic corticosteroid therapy.

In the current study 6 patients with postoperative recurrence were among those who had intracranial extra-dural and intra-orbital extension. The soft tissue that was involved with the extension of the disease to intracranial extra-dural and intra-orbital region could be harbored and contaminated with some fungi that were difficult to be seen and removed during surgery causing the same inflammatory reaction and recurrence. Or, are these contaminants? In addition, allergy to fungi (IgE production) may not cause AFRS, but may be a result of the inflammatory cascade induced by the fungus. Clearly, more information is needed. We agree that the number of patients used in this study is small and the number of patients who had recurrence is even smaller.

  Conclusion: Top

The result of this study and our accumulated experience in dealing with pediatric AFRS were found to have a more aggressive form of the disease with more intraorbital and/or intracranial extra-dural extension. Patients with extension of the disease that made bone erosion showed high recurrence rate after EES. This information may allow us to alert our colleagues about the potential of AFRS aggressiveness in certain demographic groups. Larger number of patients preferably in a prospective multicenter meta study are required to address this issue.

  References Top

Tosun F, Hidir Y, Saracli MA, Caliskaner Z, Sengul A. Intranasal fungi and chronic rhinosinusitis: what is the relationship? Ann Otol Rhinol Laryngol. 2007 Jun; 116(6):425-9.  Back to cited text no. 1
Schubert MS. Allergic fungal sinusitis. Clin Allergy Immunol. 2007;20:263-71.  Back to cited text no. 2
Campbell JM, Graham M, Gray HC, Bower C, Blaiss MS, Jones SM. Allergic fungal sinusitis in children. Ann Allergy Asthma Immunol. 2006;96(2):286-90.  Back to cited text no. 3
McClay JE, Marple B, Kapadia L, Biavati MJ, Nussenbaum B, Newcomer M, Manning S, Booth T, Schwade N. Clinical presentation of allergic fungal sinusitis in children. Laryngoscope. 2002;112(3):565-9.  Back to cited text no. 4
Mukherji SK, Figueroa RE, Ginsberg LE, Zeifer BA, Marple BF, Alley JG, Cooper LL, Nemzek WR, Yousem DM, Jones KR, Kupferberg SB, Castillo M Allergic fungal sinusitis: CT findings. Radiology. 1998;207(2):417-22.  Back to cited text no. 5
Kuhn FA, Javer AR.Allergic fungal sinusitis: a four-year follow-up. Am J Rhinol. 2000;14(3):149-56.  Back to cited text no. 6
Quraishi HA, Ramadan HH.Endoscopic treatment of allergic fungal sinusitis. Otolaryngol Head Neck Surg.1997;117(1):29-34.  Back to cited text no. 7
Wise SK, Ghegan MD, Gorham E, Schlosser RJ. Socioeconomic factors in the diagnosis of allergic fungal rhinos- inusitis. Otolaryngol Head Neck Surg. 2008 ; 138(1):38-42.  Back to cited text no. 8
Wise SK, Venkatraman G, Wise JC, et al. Ethnic and gender differences in bone erosion in allergic fungal sinusitis. Am J Rhinol 2004; 18:397- 404.  Back to cited text no. 9
Bent JP 3rd, Kuhn FA.Diagnosis of allergic fungal sinusitis. Otolaryngol Head Neck Surg. 1994; 111(5):580-8.  Back to cited text no. 10
Manning S, Vuitch F, Weinberg A, et al. Allergic aspergillosis: a newly recognized form of sinusitis in the pediatric population. Laryngoscope.1989; 99:681-685.  Back to cited text no. 11
Marple BF, Gibbs SR, Newcomer MT, Mabry RL. Allergic fungal sinusitis induces visual loss. Am J Rhinol. 1999;13:191–195.  Back to cited text no. 12
Vig KW, Fields HW. Facial growth and management of orthodontic problems. Pediatr Clin North Am. 2000;47:1085–1123.  Back to cited text no. 13
Lydiatt WM, Sobba-Higley A, Huerter JV, Liebroch LG: Allergic fungal sinusitis with intracranial extra-dural extension and frontal lobe symptoms: a case report. ENT Journal. 73:402-404, 1994.  Back to cited text no. 14
Ghegan, Mark D. MD; Lee, Fu-Shing PhD; Schlosser, Rodney J. MD Incidence of skull base and orbital erosion in allergic fungal rhinosinusitis AFRS and non-AFRS. Otolaryngol Head Neck Surg.2006;134(4):592-595.  Back to cited text no. 15
Chang WJ, Tse DT, Bressler KL, Casiano RR, Rosa RH, Johnson TE. Diagnosis and management of allergic fungal sinusitis with orbital involvement. Ophthal Plast Reconstr Surg. 2000; 16:72-74.  Back to cited text no. 16
Jackson CG, Pappas DG, Manolidis S, et al. Brain herniation into the middle ear and mastoid: concepts in diagnosis and surgical management. Am J Otol. 1997;18:198–206.  Back to cited text no. 17
Schubert MS, Goetz DW: Evaluation and treatment of allergic fungal sinusitis. I. Demographics and diagnosis. J Allergy Clin Immunol.1998;102(3): 387-94.  Back to cited text no. 18
Sohail MA, Al Khabori MJ, Hyder J, Verma A.Allergic fungal inusitis: can we predict the recurrence? Otolaryngol Head Neck Surg. 2004 Nov;131(5):704-10.  Back to cited text no. 19
Kuhn FA, Javer AR. Allergic fungal rhinosinusitis: perioperative management, prevention of recurrence, and role of steroids and antifungal agents. Otolaryngol Clin North Am. 2000; 33:419-33.  Back to cited text no. 20
Marple BF, Mabry RL. Allergic fungal sinusitis: learning from our failures. Am J Rhinol. 2000; 14:223-6. World Bank report: Facts and figures: web.worldbank.org/WBSITE/EXTERNAL/COUNTRIES/MENAE  Back to cited text no. 21


  [Figure 1], [Figure 2], [Figure 3]

  [Table 1]


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