Acta Oto-Laryngologica

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Aspergillosis of the Maxillary Sinus: Clinical and

Histopathological Features of 4 Cases and a
Review of the Literature

H. Axelsson, B. Carlsöö, J. Weibring & B. Winblad

To cite this article: H. Axelsson, B. Carlsöö, J. Weibring & B. Winblad (1978) Aspergillosis of
the Maxillary Sinus: Clinical and Histopathological Features of 4 Cases and a Review of the
Literature, Acta Oto-Laryngologica, 86:1-6, 303-308, DOI: 10.3109/00016487809124751

To link to this article: http://dx.doi.org/10.3109/00016487809124751

Published online: 08 Jul 2009.

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 Acta Otolaryngol86: 303-308, 1978

ASPERGILLOSIS OF THE MAXILLARY SINUS

Clinical and Histopathological Features of 4 Cases and
a Review of the Literature

H. Axelsson, B. Carlsoo, J. Weibring and B. Winblad

From the Departments of Oto-rhino-laryngology and Pathology, University of Urne;, Urned, Sweden

(Received January 5 , 1978)

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Absrract. Four patients with aspergillus maxillary sinuitis
are reported and a review of the literature on aspergillus
paranasal sinuitis during the last 10 years is presented.
The patients had symptoms and X-ray findings similar to
a chronic bacterial sinuitis. One patient had been operated
upon 6 years previously due to a chronic sinuitis and 3
of the patients had been treated with broad-spectrum anti-
biotic drugs. Caldwell-Luc operations were performed,
also to exclude malignant tumours. The aspergillus etio-
logy of the sinuitis was discovered in routine stained sec-
tions by histo-pathological examination of the sinus mu-
cosae. No recurrence of the fungus infection occurred
after the Caldwell-Luc operation, which was valuable for
the correct diagnosis as well as being the best suited
therapy.
Fungus infection caused by aspergillus is a
rare disorder in man in industrialized coun-
tries. The most important site of infection is
the lung, with or without hematogenous spread
to other organs (Emrnons et al., 1963; Young
et al., 1970). A localized aspergillus infection
can also occur in the upper respiratory tract,
and is probably more common than was previ-
ously suspected (Iwamoto et al., 1972; Gri-
goriu et al., 1977). To our knowledge only 3
patients with sinuitis caused by aspergillus
have been reported from Scandinavia (Rohrt,
1954; Andersen & Stenderup, 1956; Mikael-
sen, 1975). Consequently, and because of the
concurrent diagnostic difficulties, we want to
report 4 additional cases.
Review of the literature
In cattle, sheep and birds, aspergillus infec-
tions are common. For example, in horses as-
pergillus is the etiologic agent in a sinuitis-like
condition, guttural pouch mycosis, where the
clinical picture is dominated by purulent dis-
charge from the nose and invasion of blood
vessels, often leading to fatal epistaxis (Cook,
1968; Bjorklund & Phlsson, 1970; Lingard et
al., 1974).
In man, aspergillus infection of the maxillary
sinus can behave either as an invasive or non-
invasive infection (Hora, 1965). In the non-
invasive infection the symptoms, clinical signs
and X-ray findings are similar to a chronic bac-
terial sinuitis. In the invasive form, bone de-
struction and involvement of the orbit often
render the clinical differentiation from a malig-
nant tumour difficult (Chapnic & Bach, 1976).
Infections due to aspergillus in the nose and
paranasal sinus, since the review of Sandison
et al. (1967), are summarized in Table I.
The cases reported by Sandison et al. (1967)
were included and reinvestigated in the ar-
ticles by MiloSev et al. (1969) and Veress et al.
(1973).
Most authors report solitary cases of asper-
gillus infection of the paranasal sinuses, but in
a recent systemic histopathological and rnyco-
logical investigation, aspergillus sinuitis was
seen more frequently (Grigoriu et al., 1977).
In the Sudan the disease appears mostly as a
granuloma with giant cell reaction, fibrosis and
often involvement of the orbit (Sandison et al.,
1967; MiloSev et al., 1969; Veress et al., 1973).
The hot climate with a low humidity, toxic
Actu Otolaryngol86
 304 H . Axelsson et al.

Table I . Review of reported aspergillus paranasal sinuitis during the last 10 years
-
No. of Ageand
Authors pats. sex Symptoms Site Treatment

MiloSev et al. (1969), 17 11 males Proptosis. Painless swell- Paranasal Medial orbito-
Sudan 6 females ing of the ethmoid and/or sinus and tomy.
maxillary region orbit Caldwell-Luc
Taillens et al. (1970), 1 F 35 Tuba1 obstruction with Maxillary Op. ad modum
Switzerland otosalpingitis. “Chronic sinus Taillens
maxillary sinuitis”
Zinnernan (1972), 1 M 46 Unilateral pain, rapidly Maxillary Amphoteri-
USA declining vision. Mucosan- sinus and cin B. i.v.
gineous nasal discharge. orbit Caldwell-Luc
Proptosis
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Iwamoto et al. (1972), 1 M 60 Nasal obstruction. Fever. Maxillary Explorative

Japan Purulent rhinorrhea. Cheek sinus antrotomy
pain
Grigoriu & Dutoit 1 M 53 “Maxillary sinuitis” Maxillary Op. ad mod.
(19731, Switzerland and ethmoid Taillens
sinuses
Veress et al. (1973), 46 25 males Swelling of the maxillary Paranasal Not stated
Sudan 21 females and/or ethmoid sinuses. sinus and
Proptosis orbit

Mikaelsen (1975), 1 M41 Cheek pain. Unilat. rhinor- Maxillary Caldwell-Luc

Norway rhea. Sneezing and ethmoid
sinuses
Ruch et al. (1975), 2 F74 Unilateral nasal obstruction. Paranasal Ethmoidectomy
France Purulent and hemorrhagic sinus and antrotomy
rhinorrhea. Headache
F 22 Unilateral purulent Maxillary Caldwell-Luc
rhinorrhea. Cacosomia sinus

Warder et al. (1975), 3 F67 Facial pain Maxillary Caldwell-Luc

USA F 63 Nasal obstruction. Hemor- sinus
rhagic rhinorrhea
M 18 Proptosis Fronto- Ethmoidectomy
ethmoid
complex
Gonty & Page (1977), I M26 Cheek pain Maxillary Caldwell-Luc
USA sinus bilat.

Grigoriu et al. (1977), 43 18 females Nasal obstruction. Maxillary Lavage and

Switzerland 25 males Rhinorrhea. Orbital pain. sinus antimycotic
Headache drugs.
Caldwell-Luc-
Lima
 Aspergillosis of the maxillary sinus 305
metabolites of the fungus and the local im-
munological conditions are discussed as a pos-
Surg. specimen
and pathology Mycology Remarks sible explanation for this concentration of the
disease in the Sudan (Sandison et al., 1967;
Fibroua granuloma A . jlavus Veress et al., 1973). For us, another possible
with septate hyphae cultured
and giant cells explanation could be the living habits and the
Thick, black-green A . niger environmental conditions in parts of the
mass. Branching cultured Sudan, where among the Nuer, for instance,
mycelia
the carcasses and bodily products of the cattle
Gangrenous tissue. A . jlavus Cutaneous
Chronic inflam. muco- and Nocar- fistulae are widely used for household purposes. Cattle
sae and hyphae inter- dia asteroi- in the ca- dung is used for plastering walls and floors of
preted as Mucor des cultured nine fossa
straw huts in cattle compounds, as plaster to
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Dark brown mass. -

Eumycetes assumed to protect wounds and as tooth powder (Evans-
be Aspergillus Pritchard, 1940). From the report by MiloSev
Necrotic mass. A . fumiga tus et al. (1969) it is also evident that many of the
Mycelium suggested cultured
to be Aspergillus patients were working as farmers and asper-
Hard, fibrotic grey- A . jlavus Prolifera- gillus species were isolated from the environ-
ish-white mass. cultured tive form. ment of the patients (Sandison et al., 1967).
Pseudotubercles with Exudative-
fibrosis, necrosis, necrotiz-
septate hyphae and in- ing form.
flammatory cells with Mixed form
giant cells CASE REPORTS
Dark brown mass.
The clinical features of the 4 cases, all with left-sided in-
Sepate mycelium
similar to Aspergillus volvement of the maxillary sinus, studied in the present
investigation are summarized in Table 11.
Necrotic, fungoid
- - Immuno-
There was a considerable age variation in the material
mass. Aspergillus mycelia el.-uhoresis.
A . kdulans consisting of 1 female and 3 male patients. The female had
Friable caseous brown A . flavus Tooth ex- a previous history of Caldwell-Luc operation 6 years
mass. Foreign body cultured traction earlier due to a chronic maxillary sinuitis after a tooth
granuloma. Aspergil- 6 months extraction with sinus perforation. The 3 male patients had
lus mycelia previously been in good health. None of the patients suffered from a
Mucosal thickening malignant or systemic disease. The duration of symptoms
and purulent necrotic before the present operation varied markedly between the
mass. Aspergilloma patients. One patient (M 80) had symptoms of bad smell
from the nose for 3 years. The first symptom of the dis-
ease in one patient (M61) was an acute attack of ep-
istaxis. Sinus X-ray revealed mucosal swelling or opacifi-
Grey, greasy, foul- A . fumigatus Op. max. frac- cation. All 3 male patients had been treated with tetra-
smelling material. cultured ture 6 years cycline for their sinuitis. Due to persistent symptoms, and
“Fungus ball” of previously. in spite of a regime of nasal decongestant, antibiotics and
septate hyphae Caldwell-Luc lavage, all 4 patients were operated ad modum Caldwell-
2 years pre-
viously due Luc. The mucosal lining of the sinuses were found to be
to chron. max edematous and markedly thickened. In 2 of the patients,
greyish necrotic masses were observed and in one of
Chronic inflamed mu- A . fumigatus Mucopuro- these (M 80) the medial sinus wall was replaced by necro-
cosa with mycelia (40) lent form.
Budding tic tissue.
and spores A . niger
(2) and/or ca-
A . flavus seous form. Histo-pathology
(1) cultured Pseudotu- Microscopic examination of the material removed at Cald-
mor form
well-Luc operation revealedz an inflamed respiratory
mucosa, diffusely invaded by numerous polymorphonu-
clear granulocytes and mononuclear inflammatory cells.
Eosinophilic granulocytes were not very conspicuous.
Separated from or situated on the surface of the pseudo-
stratified, ciliated columnar epithelium, separate and

Acta Otolaryngol86
 306 H. Axelsson et al.
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Fig. I a . Micrograph of inflamed maxillary sinus mucosa
with adjacent, partly necrotic fungal mycelia. Hematox-
ylin-eosin, X40.
Fig. I b. Maxillary mucosa with suspicion of fungal in-
vasion. Hematoxylin-eosin, X 100.
dichotomous branching hyphae with conidiophores were
observed (Fig. l a ) . Occasionally the mycelia were sus-
pected of infiltrating the mucosa, as depicted in Fig. 1 b.
No granuloma or giant cell reaction with fribrosis could
be detected. The pigmented conidiophores ended in a
gradually widening vesicle (Fig. 1c). The upper part of the
vesicle (capitulum) was covered with a single layer of
parallel arranged primary sterigmata. Spherical conidia,
sometimes forming unbranched chains, were observed in
the vicinity of the fruiting bodies (Fig. I d ) (Thom &
Raper, 1945). No cultures were performed but the mor-
phology of the conidiophores, as seen in the tissue sec-
tions from all 4 cases, indicated that the fungus infection
most probably was due to Aspergillus fumigatus (Emmons
et al., 1963). The diagnosis of the mycotic infection could
be made in sections stained with hematoxylin-eosin or
Acrri O ~ o l r i r ? t i ~ 86
o/
Fig. I c. Fungal mycelia showing dichotomous branching,
septation and conidiophores. P A S , x 500.
Fig. I d . A conidiophore with single sterigmata and partly
detached conidia. Grocott, x 1200.
according to van Gieson. Staining with Grocott/Griedly
and PAS are not necessary for the histo-pathological
diagnosis.
DISCUSSION
Aspergillus infection of the maxillary sinus can
be found in patients in general good health, in
nutritionally deprived persons and in patients
with an underlying debilitating disease (Em-
mons et al., 1963). Systemic diseases, such as
collagenosis and malignant tumours, and also
treatment with immunosuppressive drugs and
cytostatic agents, have been associated with

Table 11. Cases of aspergillosis of the maxillary sinus
Predisposing
Patient factors Symptoms
Female Chronic max. sinuitis Cheek pain, na-
F 36 after tooth extraction sal discharge.
and Caldwell-Luc op. Rhinorrhea
6 years previously
Male Tetracycline Cheek pain.
M61 treatment Epistaxis
Male Tetracycline Unilateral
M62 treatment nasal dis-
charge.
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Cacosomia
Male Tetracycline Cacosomia
M80 treatment
an increased incidence of fungal infections
(Young et al., 1970). In patients in general
good health there are probably some factors,
systemic or local, predisposing to the fungal
infection of the paranasal sinus (Chapnic &
Bach, 1976). Most patients reported have been
treated with broad-spectrum antibiotics, which
suppress the bacterial flora and support a fun-
gal overgrowth. Recurrent bacterial infec-
tions, tooth-extraction, trauma or surgery may
affect the drainage of the sinus.
Our 4 patients were all in good health, ex-
cept for their E.N.T. symptoms. Three of the
patients had been treated with lavage and sys-
temic tetracycline drugs without improvement
of the disease prior to operation. One patient
(F 36) had 6 years previously been operated ad
modum Caldwell-Luc for a sinus infection
after a tooth extraction. In all patients the
aspergillus infections were of the non-invasive
type, except for the oldest patient (M80)
where the medial wall of the maxillary sinus
was destroyed and at operation found to be
replaced by a “necrotic granular mass”. Histo-
pathological examination of the tissue re-
moved from this patient revealed a suspicious
fungus infiltration in the mucosa. However,
this elderly patient did not suffer from any de-
bilitating disease or nutritional deficit, but the
thymic involution and cellular immune dys-
function known to occur in elderly persons
Aspergillosis of the maxillary sinus 307
~ ~~
X-ray Treatment Follow-up
Opacifi- Caldwell-Luc Control after 3 months and
cation telephone contact after
3 years: no symptoms
Opacifi- Caldwell-Luc Control after 9 months and
cation telephone contact after
5.5 years; no symptoms
Mucosal Caldwell-Luc Control after 1 month;
thicken- no symptoms
ning.
Fluid
Opacifi- Caldwell-Luc Control after 3 months;
cation no symptoms
could have caused decreased host defence and
enhanced a destructive infection.
In none of the patients was the mycotic in-
fection suspected preoperatively , and no cul-
tures with respect to fungus were performed.
The etiology of the sinuitis was obvious first
upon histo-pathological examination of the
surgically removed material. Due to the my-
celial structure and the presence of fruiting
bodies the diagnosis of aspergillus infection
could be made on routine stained sections.
The Caldwell-Luc operations have been of
diagnostic importance as well as the therapy of
choice, as not all infections of the paranasal
sinuses can be satisfactorily treated by lavage
and antibiotics. No other treatments were
given after the operations and all patients were
free from symptoms at follow-up, indicating
that with Caldwell-Luc operation no addi-
tional local or systemic drug therapy is neces-
sary.
The clinical conclusions from the review
and our reported cases are: (1) A maxillary
sinuitis which is not improved by lavage and
oral antibiotic therapy should be subjected to
diagnostic Caldwell-Luc operation. (2) The
diagnosis of aspergillus infection can be es-
tablished by histo-pathological examination of
routinely stained sections. (3) The Caldwell-
Luc operation is also the therapy of choice in
cases of aspergillus maxillary sinus infection.
Acta Otolaryngol86
 308 H . Axelsson et a / .
ACKNOWLEDGEMENT
We thank Robert N. Elston, Department of Pathology,
Ume%University, for drawing our attention to the condi-
tions among the Nuer in the Sudan. This study was sup-
ported by grants from Carin Tryggers Foundation.
ZUSAMMENFASSUNG
Vier Patienten mit Aspergillusinfektion der maxillaren
Nebenhohle und eine Literaturubersicht von Aspergillus-
infektionen der Nasennebenhohlen der letzten 10 Jahre
werden prasentiert. Symptome und Rontgenbefunde der
Patienten sind ahnlich einer chronisch bakteriellen
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Sinuitis. Ein Patient wurde vor 6 Jahren wegen einer
chronischen Sinuitis operiert und drei Patienten hatten
Behandlung mit Breitspektrumantibiotika bekommen.
Operation ad modum Caldwell-Luc, auch um einen
malignen Tumor auszuschlieflen, wurde bei allen Pa-
tienten durchgefuhrt. Die Aspergillusatiologie der Sinuitis
war bei der mikroskopischen Routineuntersuchung der
Sinusmucosae erfaRt. Kein Rezidiv der Pilzinfektion
konnte nach der Operation festgestellt werden. Die Cald-
well-Luc-Operation brachte die korrekte Diagnose und
war gleichzeitig die adaquate Therapie.
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Dr Bengt Winblad
Patologiska inst
UmeB lasarett
S-90185 Umed
Sweden