Global Journal of

Otolaryngology
ISSN 2474-7556

Review Article Glob J Otolaryngol

Volume 13 Issue 3 - February 2018
Copyright © All rights are reserved by Sumit Sharma
DOI: 10.19080/GJO.2018.13.555865

Understanding Allergic Fungal Rhino-Sinusitis

Sumit Sharma*
Department of E.N.T, Mayo Institute of Medical Sciences, India
Submission: February 01, 2018; Published: February 23, 2018
*Corresponding author: Sumit Sharma, Department of E.N.T, Mayo Institute of Medical Sciences, Barabanki. (U.P.), India,
Email:

Introduction
Allergic fungal rhino sinusitis (AFRS) is an allergic response In the present discussion we will discuss about the Clinical
in Sino nasal tract mucosa to aerosolized fungal allergens, manifestations, Diagnostic criteria’s, histopathological criteria’s,
amplified and perpetuated by eosinophils. It is a noninvasive radiological criteria’s of the disease along with management.
form of fungal rhino sinusitis with an incidence of between 6 and
Clinical Presentation
9% of all rhino sinusitis requiring surgery. Regional variation
in incidence has been reported [1]. It is a benign noninvasive The incidence of AFRS appears to vary by geographical region.
sinus disease, believed to be an allergic reaction to aerosolized Review of the world’s literature reveals that the majority of sites
environmental fungi. It has been almost three decades when in reporting cases of AFRS are located in more temperate regions
1976 Safirstein noted that the combination of polyposis, crust where relative humidity is high [3]. The clinical presentation is
formation and sinus cultures yielding aspergillus was similar nonspecific and may be similar to those of other forms of chronic
to the constellation of findings observed in allergic broncho- sinusitis. They present with progressive nasal obstruction,
pulmonary aspergillosis. Initially it was called as Allergic crusting, rhinorrhoea, and chronic rhino sinusitis with nasal
Aspergillus sinusitis but later on it was found that fungus polyposis and viscid, dark mucoid discharge with greenish
other than Aspergillus are also involved henceit was changed black nasal casts not responding to medical or surgical therapy
to Allergic fungal sinusitis. It is probably the most frequently [5]. Pain is uncommon in patients with AFS and when present
occurring fungal rhino sinusitis disorder [2]. AFRS was first suggests the concomitant presence of bacterial rhino sinusitis
recognized in the late 1970s by pulmonologists and pathologists [6]. A patient with AFRS is usually an immune-competent atopic
who noted the distinct clinical and immunologic similarities that young adult or an adolescent, and less commonly a child, though
it shared with allergic broncho-pulmonary aspergillosis (ABPA) the disease has been found in all ages [5]. Children usually
[3]. present with unilateral disease (70% cases) while only 37%
adults have one-sided presentation Patro et al. [7] observed
Fungal rhino sinusitis (FRS) is defined as the rhino
AFRS in children to be more aggressive with higher fungal
sinusitis where fungi are responsible for causing the immune-
load and less response to treatment as compared to adults. In
pathogenesis. Fungal infections involving para-nasal sinuses
general, 66% of AFRS patients have a history of allergic rhinitis,
can be classified under two broad categories. 1. Non invasive
90% demonstrate increased specific IgE to one or more fungi,
– Saprophytic infections, fungal ball, allergic fungal sinusitis 2.
and around 50% suffer from asthma [8]. No linkage to aspirin
Invasive – Acute fulminant invasive sinusitis, chronic invasive
sensitivity has been established [3]. The presence of Nasal
sinusitis and granulomatous invasive fungal sinusitis [4].
polyposis has been reported to be up to 100% [1] Most of these
Clinically 6 different types of fungal sinusitis have been described
patients also show multiple previous sinus surgeries.
depending on the pathophysiology and clinical features:
Complications of AFRS include [5]
a) Acute fulminant invasive fungal sinusitis
a) Occular: Visual disturbances, proptosis, telecanthus,
b) Chronic invasive fungal sinusitis
b) Facial deformity
c) Granulomatous invasive fungal sinusitis
c) Neuropathies
d) Fungal ball
d) Intracranial abscess.
e) Allergic fungal rhino sinusitis
e) Bony erosion is observed in the majority of cases
f) Eosinophilic fungal rhino sinusitis [4].
belonging to a young age group. It probably occurs due

Glob J Otolaryngol 13(3): GJO.MS.ID.555865 (2018) 001

 Global Journal of Otolaryngology

to blockage of ostia of the sinuses by polyposis leading to findings on examination is typically broad, ranging from nasal
expansion of sinuses. Commonly, the ethmoid sinus is affected airway obstruction resulting from intranasal inflammation and
with lesion extending to orbit (especially lamina papyracea) and polyposis to gross facial disfigurement and orbital or ocular
the anterior cranial fossa. Expansion, remodeling, or thinning of abnormalities (3) and complications mentioned above.
involved sinus walls was common and was thought to be due to
Diagnostic Criterias
the expansile nature of the accumulating mucin.
The most widely accepted criteria for the diagnosis is the
In contrast to the often subtle symptoms of AFRS, physical
Bent & Kuhn diagnostic criteria for RFRS Table 1.
findings are often more remarkable. The range of physical
Table 1: Diagnostic criteria for afrs by bradley f. Marple [3].

Major Criteria’s Minor criteria’s

Type I hypersensitivity confirmed by history, skin tests, or
1 Asthma
serology
2 Nasal polyposis Unilateral predominance
3 Characteristic CT scan (double density sign) Radiographic bone erosion
4 Eosinophilic mucus without fungal invasion into sinus tissue. Fungal culture
Positive fungal stain of sinus contents removed intraoperative or
5 Charcot Leyden crystals
during office endoscopy
6 Immuno-competence (replaces no 1 at St Paul’s Sinus Centre) Serum Eusinophilia.

Swain’s modification of Bent’s criteria [4] alone since only 2/3 of patients with allergic fungal sinusitis
manifested with hypersensitivity to fungal protein in various
de Shazo and Swain slightly modified the diagnostic criteria
studies Table 2.
laid out by Bent. They left out the type I hypersenitivity criteria
Table 2: Bradley F Marple [3] suggested the following CT findings associated with AFRS.

A. Symptoms Requires one of the following: B. Objective findings Requires all of the following:
1. Anterior and/or posterior nasal drainage 1. Presence of allergic mucin (pathology showing fungal hyphae
2. Nasal obstruction with degranulating eosinophils)

3. Decreased sense of smell 2. Evidence of fungal specific IgE (skin test of in vitro test)

4. Facial pain-pressure-fullness 3. No histologic evidence of invasive fungal disease

C. Radiographic Findings Highly recommended: B. Objective findings Requires all of the following:
1. Sinus CT demonstrating 1. Presence of allergic mucin (pathology showing fungal hyphae
2. Bone erosion with degranulating eosinophils)

3. Sinus expansion 2. Evidence of fungal specific IgE (skin test of in vitro test)

4. Extension of disease into adjacent anatomic areas 3. No histologic evidence of invasive fungal disease

Pitfalls to be avoided in the diagnosis of AFRs are The Allergic Mucin

a) The failure to recognize that the presence of classic It is the production of allergic mucin that is unique to AFRS,
allergic mucin, but without fungal involvement, can also be and serves as a hallmark of the disease. Grossly, allergic fungal
seen patients with the non-AFS disorder ‘eosinophilic mucin mucin is thick, tenacious, and highly viscous in consistency;
rhino sinusitis’ (EMRS). its color may vary from light tan to brown or dark green. This
characteristic gross appearance has led to the use of such
b) Diagnostic confusion can be minimized by avoiding the
descriptive terms as ‘peanut-butter’ and ‘axlegrease’. Given
temptation to culture trans nasal secretions in the office, the
both the location of this mucin within the para nasal sinuses as
results of which include the presence of normal nasal flora.
well as its thick consistency, it is common that allergic fungal
Histopathological Criterias mucin is initially encountered at the time of surgery. As a result
of this, the diagnosis of AFRS is frequently delayed until such
The diagnosis of AFRS is histopathological. We will discuss
time [3]. Microscopically hematoxylin and eosin (H&E) staining
this in two heads – The allergic mucin and the fungus.
shows eosinophilic mucin in the form of onion laminations

002 How to cite this article: Sumit S.Understanding Allergic Fungal Rhino-Sinusitis. Glob J Oto 2018; 13(3): 555865. DOI: 10.19080/GJO.2018.13.555865
 Global Journal of Otolaryngology

of eosinophils and their degradation products in the center Approximately 40% of patients may have each of the
surrounded by light-stained mucin and Charcot Leyden crystals. following features 4:
Polypoid mucosa is edematous with inflammatory mixture
a) Expansion of an involved sinus
of lymphocytes, eosinophils, and plasma cells. Routine H&E
staining shows hyphae as a negative image as fungus fails to b) Remodeling and thinning of the bone sinus walls
stain with H&E and are detected in 67.5% of AFRS cases. The
c) Erosion of the sinus wall
morphology of hyphae may be distorted, swollen, and have
central pallor [5]. Given that fungal hyphae are frequently rare, Am Fam [9] suggested that the degree of bony erosion
scattered, and fragmented within allergic mucin, identification is and extension beyond a sinus may mimic aggressive sinonasal
extremely difficult unless specific histologic stains are used [3]. neoplasms. The presence of increased internal attenuation on
The specimen for the testing of allergic mucin must be collected unenhanced CT scans may help to distinguish allergic fungal
preoperatively and not as a nasal lavage to avoid a false positive sinusitis from an invasive tumor. The presence of expansion
test as well as to rule out isolating normal non pathological and thinning of the sinus walls may help separate allergic
fungal flora of the nose. fungal sinusitis from chronic sinusitis of other origins. He
also suggested that mucosal thickening was visualized in any
The Fungus
of the sinuses, but the ethmoid sinus complex was the most
Since initially aspergillous was isolated from many samples commonly involved sinus. At least one ethmoid sinus complex
of allergic mucin hence it was initially labeled as “Allergic demonstrated infection in 96% of the patients. And the next
Aspergillus Sinusitis.” However, the term AAS was changed most commonly involved region was the maxillary sinus, which
to “allergic fungal sinusitis” when etiologic agents other than harbored infection in 93% of patients Table 3.
Aspergillus spp. (dematiaceous group including Bipolaris spp., Table 3.
Alternaria spp., Curvularia spp.) were identified [5]. Fungal
Complete opacification of at least one paranasal
elements are recognized for a unique ability to absorb silver. 1
sinus
This property is the basis for various silver stains, such as
2 Expansion of involved sinuses
Fontana Masson stains and Grocott’s or Gomori’s methamine
silver (GMS) stain, which turn fungi black or dark brown. The use Attenuation/erosion of the bone bordering involved
3
sinus
of a fungal stain complements the findings of initial H&E stain,
and is extremely important in the identification of fungi. Fungal 4 Heterogeneity of signal within involved sinus
cultures of allergic fungal mucin may provide some supportive 5 Unilateral or asymmetric distribution of disease
evidence helpful in the diagnosis and subsequent treatment
of AFRS, but must be interpreted with caution. It is important 6 Displacement of adjacent anatomic compartments
to realize that the diagnosis of AFRS is not established, nor
Note: Bradley F Marple [3] suggested the following CT
eliminated based upon the results of these cultures. The variable
findings associated with AFRS.
yield of fungal cultures (64-100%) renders AFRS in the presence
of a negative fungal culture quite possible. Conversely, a positive Cade Martin [10] suggested that in non-contrast CT –
fungal culture fails to confirm the diagnosis of AFRS, as it may high attenuation allergic mucin within lumen of sinuses can
merely represent the presence of saprophytic fungal growth. It mimic a mucocele with expansion of the sinus. Arunaloke
is for this reason that the histologic appearance of allergic mucin Chakrabarti [5] described CT findings as consisting of multiple
remains the most reliable indicator of AFRS [3]. sinus opacifications with central hyper-attenuation (central
serpiginous or starry sky appearance), sinus mucocele, skull
Note: Bacterial cultures or staining of this allergic mucin
base erosions (56% of AFRS patients versus 5% of non AFRS
may detect the presence of Staphylococcal aureus [5].
patients) and remodeling with a “pushing border” at skull base.
Radiological Criterias He also suggested that Bone erosion and extension of
The radiological features of Allergic Fungal sinusitis are disease into adjacent anatomic areas was encountered in 20%
quite characteristic and radiology must always be done in all of the patients and was more likely to occur in the presence
suspected cases. Bothe CT scan and MRI have distinctive features of bilateral, advanced disease. Expansion, Remodeling, or
like: thinning of involved sinus walls was thought to be due to the
expansile nature of the accumulating mucin. Desiccation of sinus
CT Scan contents may also contribute to the hyperdense areas seen on
Dr. Bruno Di Muzio (1) suggested that the majority of sinuses CT scans. Although these findings are not specific for AFRS, they
show near complete opacification. On unenhanced CT, the sinuses are relatively characteristic of the disease, and may provide
are typically opacified by centrally (often serpiginous) hyper preoperative information suggestive of a diagnosis of AFRS.
dense material with a peripheral rim of hypo dense mucosa.

003 How to cite this article: Sumit S.Understanding Allergic Fungal Rhino-Sinusitis. Glob J Oto 2018; 13(3): 555865. DOI: 10.19080/GJO.2018.13.555865
 Global Journal of Otolaryngology

MRI outcome among all types of CRS. The FESS improves quality of
life although revision surgery is required in 15%–20% patients
Dr. Bruno Di Muzio [11] suggested that Hypo intensity on
[5]. The factors contributing to need of revision surgery are poor
T1WI and T2WI is the most common finding. T1: hypo intense
drainage of the frontal recess or the frontal sinus neo-ostium due
inflamed mucosal thickness. It can have multiple T1 appearances.
to the presence of remains of the uncinate process and anterior
T2: usually a hyper intense peripheral inflamed mucosal
ethmoid cells, a missed maxillary sinus ostium, a lateralized
thickness, He suggested that low T2 signal or signal void is due
middle turbinate, scarring, osteoneogenesis, or recurrent
to high concentration of various metals such as iron, magnesium
polyposis. The disease-specific measures and quality of life are
and manganese concentrated by fungal or Nganisms as well as
predicted to be poor when the amount of mucosal eosinophilia
high protein and low free water content in allergic mucin. T1 C+
is >10 eosinophils /high-power field during FESS procedure [5].
(Gd): an inflamed mucosal lining has contrast enhancement -- no
The accumulation of mucin appears to play a role in the cyclic
enhancement in the center or majority of the sinus contents (c.f.
recurrence of the disease by way of perpetuating antigenic
neoplasms) Table 4.
exposure. In theory, complete surgical removal of mucin breaks
Table 4. this cycle [3]. Endoscopic surgery for allergic fungal sinusitis
Stage 0 No evidence of disease. may be associated with more complications when compared
Odematous mucosa / allergic to endoscopic sinus surgery for other pathologies. Extensive
Stage 1
mucin disease may cause spatial disorientation. There may be areas
Polypoidal mucosa / allergic of bony dehiscence, which may confuse or distort anatomic
Stage 2
mucin boundaries, causing increased risk of orbital and intracranial
Stage 3 Polyps and Fungal debris complications. It includes penetration of dura or periorbita
resulting in diplopia, blindness, intracranial hemorrhage or
Manohar Aribandi et al. [12] suggested that they have
cerebrospinal fluid rhinorrhoea. Occasional cases of fungal
frequently observed high signal intensity or mixed low,
invasion into adjacent tissues have also been described [2]. In
intermediate, and high signal intensity on T1-weighted images
addition to surgery, postoperative endoscopic cleanings should
in these patients. He also stated that although the condition is
be periodically scheduled after surgery, and patients should
not considered invasive, if left untreated, the involved sinuses
be followed for a very long period which helps in preventing
expand and there is smooth bone erosion with subsequent
recurrence [6].
intracranial or intra orbital extension and resulting cranial or
orbital symptoms. Intracranial extension is usually limited by The rate of relapse in pediatric cases (ranges from 25 to
the dura to the extradural space. 55%) is higher than in adults. It has been hypothesized that this
high rate of recurrence in the pediatric population is related
Cade Martin [10] suggest that moderately high T1 signal,
to the risks associated with long-term or repetitive systemic
low T2 signal with expanded sinus can be seen in allergic fungal
steroid therapy. However, patients with recurrence should
sinusitis, mucocele, or sino-nasal polyposis.
undergo surgical revision [6]. Patients should be followed up
Treatment for a long time and post treatment mucoal status described by
The treatment of AFRS continues to evolve, most Kupferberg etal (endoscopic staging system of Allergic Fungal
otolaryngologists now understand what constitutes AFS, but sinusitis) must be used to evaluate patients as given below.
this improved recognition has not translated into treatment Oral Corticosteroids
advances. Main treatment modalities are Surgery, oral steroids,
Similar to surgical therapy, oral steroids is the mainstay of
Immunotherapy, Oral antifungals and leukotriene modulators.
management of AFRS and have a significant role postoperatively
Most of the times a combination therapy is recommended.
in reducing recurrence and inflammatory markers, and
Surgery ultimately improving the outcome in these patients. They may
The first step in treatment for any AFS patient is paranasal even obviate the need of revision surgery [5]. Most experts now
sinus surgery to both remove all obstructing inspissated agree that adding OCS to sinus surgery gives the best outcomes.
allergic mucin and resect all diseased hypertrophic sinus But there is no uniformity in optimal dosing regimen and length
mucosa and polyps [1]. Earlier radical surgery was performed of therapy. Kuhn and Javer recommend oral prednisolone
to remove the whole mucosa. Currently, endoscopic tissue- starting with 0.4mg/kg body weight postoperatively and slowly
sparing (conservative) technique called functional endoscopic tapering it to 0.2mg/kg body weight. After maintaining normal
sinus surgery (FESS) has surpassed it as the surgery of choice. mucosa for four months period, the dose is reduced to 0.1mg/
The surgery also helps remove the antigenic stimulus from kg body weight for another two months and stopped. Landsberg
the sinuses. It is recommended to enlarge the maxillary sinus et al. [2]. Demonstrated the radiologic and endoscopic benefits
to the maximum possible width through the middle meatus of preoperative administration of oral steroids in AFRS patients.
in AFRS patients. AFRS is considered to have poor surgical Their use in preoperative period helps in removing mechanical

004 How to cite this article: Sumit S.Understanding Allergic Fungal Rhino-Sinusitis. Glob J Oto 2018; 13(3): 555865. DOI: 10.19080/GJO.2018.13.555865
 Global Journal of Otolaryngology

obstruction and that helps in viewing sin nasal anatomy during Although Marple et al. [2] in 2002 failed to show any significant
FESS [13] although the steroids have shown significant benefit benefit of immunotherapy, thereby questioning its role in
in AFRS patients, their prolonged use is associated with adverse management. Since subcutaneous form of Immunotherapy is not
effects. On the contrary, topical corticosteroids possess a better associated with any side effect Therefore, immunotherapy may
safety profile and have shown benefit in the form of decreased serve as adjunct therapy in patient’s refractory to surgery and
polyp size and recurrence when added to local saline irrigation. antifungal therapy.
(5) However we must understand that essentially, steroids act
Leukotriene Modulators
by blunting the pathologic hypersensitivity to fungal antigens,
but they do not permanently reverse the disease process, leaving There is no controlled study available regarding use of these
a great need for other forms of therapy. agents in AFRS. There is only one case report of successful
postoperative management of AFRS with montelukast 10 mg
Oral Anti Fungals
daily along with topical corticosteroids. However, these agents
There is a lack of evidence for any recommendation of have shown mixed results and no benefit in comparison to
oral or topical antifungal agents for AFRS. Since the disease is steroids [5].
noninvasive and the fungus lies in the allergic mucin, systemic
Conclusion
antifungals should be ineffective against the fungi, which are
located extramucosally, outside the range of the drug circulation. Allergic fungal rhino sinusitis (AFRS) is an allergic response
Thus in order to produce an effect, a systemic antifungal must of the Sino nasal tract mucosa to aerosolized fungal allergens,
be secreted in sinus mucus, a phenomenon that has not been and is a noninvasive form of fungal rhino sinusitis. It is now
supported and probably does not occur. (14) A study by Kuhn recognized to be a distinct subgroup of the common hypertrophic
and colleagues showed amphotericin B and ketoconazole to be rhino sinusitis disorders. It is a unique entity with a great
most effective agents in-vitro [2]. However it may be considered deal of controversy in classification, pathogenesis, diagnostic
as an option in post-surgical refractory patients and they may criteria, and management protocols. The diagnosis of AFRS
provide benefit in terms of reduction of symptoms, steroid although straightforward which combines clinical, radiological,
dependence, and tendency of recurrences such as ABPA. microbiological, and pathological criterias, presentation
Kupferberg et al. noted improved endoscopic scoring when oral sometimes can be confusing. Multimodality treatment with
antifungals were administered to AFRS patients while decreased surgery and Oral steroids is the mainstay of the treatment with
recurrence (around 50%) and revision surgery (around 20%) antifungals and Immune-modulators being used in special
were reported by Rains and Mineck using oral itraconazole [3] circumstances. Since the diagnosis and treatment modalities are
Systemic antifungals such as amphotericin B play no role in AFS being understood, more studies are needed to enable improved
Jen et al. [14] also supported the benefits of a topical antifungal postoperative results.
medication. However, the benefits of antifungal use still need to
be assessed over the adverse effects associated with systemic
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006 How to cite this article: Sumit S.Understanding Allergic Fungal Rhino-Sinusitis. Glob J Oto 2018; 13(3): 555865. DOI: 10.19080/GJO.2018.13.555865