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The present study reviews the literature concerning the surgical treatment of Aspergillus mycetoma (AM)
in the last 20 years to identify a gold standard surgical technique. Aspergillus mycetoma of the maxillary sinus, or
mycetoma (fungus ball), is a noninvasive or extramucosal mycotic infection. Surgical removal of the sinus fungal
masses to ensure drainage and aeration is performed using the traditional Caldwell-Luc (CL) procedure or endoscopic
sinus surgery (ESS). Results of this review suggest that the gold standard surgical technique for AM is ESS with middle
meatal antrostomy. General or local antifungal drugs are not indicated. Combined approach with an intraoral surgical
access from the anterolateral wall of the maxillary sinus has to be reserved for selected cases in which ESS doesn’t
permit complete extraction of all fungal concretions or foreign bodies. The CL procedure should be avoided, because it
has detrimental consequences for sinus physiology. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;103:
e23-e29)
The recent rise in mycotic nasal and paranasal infec- Aspergillus mycetoma (AM) of the maxillary sinus –
tions is due to both improved diagnostic research and aspergilloma or mycetoma (fungus ball) – is a nonin-
an increase of the conditions that favor fungal infec- vasive or extramucosal mycotic infection. It mostly
tions.1-3 Improvement of the diagnostic research in- affects immunocompetent patients, almost exclusively
volves the use of computerized tomography (CT) in- adults, and is characterized by a female predominance.
stead of conventional radiograph to investigate The etiopathogenesis of AM has been debated, and
paranasal sinuses. Conditions that favor fungal infec- there have been 3 theories: odontogenic, aerogenic, and
tions are diabetes, long-term treatments (antibiotics and mixed origins.6
cortisones), radio- and chemotherapy, immunosuppres- The odontogenic school of thought maintains that the
sive treatments, and immunodeficient disease.4 Many pathogenesis is based on an initial colonization of the
authors suggest that mycotic infections of the paranasal maxillary sinus by means of iatrogenic oral-antral com-
cavity are found more commonly in apparently healthy munication. This theory holds that the zinc oxide which
patients. The most frequent microorganism involved in can be found in endodontic sealers paralyzes the epi-
Europe is Aspergillus fumigatus.5 thelial cilia or causes edema and hyperemia of the soft
tissues, affecting the Schneiderian (sinus membrane)
epithelium function. This favors the accumulation of
a
Assistant Professor of Maxillofacial Surgery, Department of Maxil- fungal waste and impairs elimination of the spores. The
lofacial Surgery, Azienda Ospedaliero Universitaria, Faculty of Med- aerogenic theory suggests that Aspergillus growth is
icine, University of Udine. due to inhalation of high quantities of spores over
b
Associate Professor of Oral Pathology, Faculty of Medicine, Uni-
extended periods. This form of fungal sinusitis has been
versity of Ferrara.
c
Associate Professor of Maxillofacial Surgery, Department of Max- reported primarily in Sudan, is granulomatous in na-
illofacial Surgery, Azienda Ospedaliero Universitaria, Faculty of ture, and is almost always associated to Aspergillus
Medicine, University of Udine. flavus infection. It is also called semi-invasive form of
d
Resident in Maxillofacial Surgery, Department of Maxillofacial fungal sinusitis, according to varying degrees of dis-
Surgery, Azienda Ospedaliero Universitaria, Faculty of Medicine,
University of Udine.
ruption of normal sinus bony architecture observed on
e
Dean of Medicine and Professor of Maxillofacial Surgery, Head of CT scans.7 The third theory is based on the ubiquitous
Department of Maxillofacial Surgery, Azienda Ospedaliero Univer- nature of the Aspergillus spores. They can be inhaled at
sitaria, Faculty of Medicine, University of Udine. any moment and are normally present as saprophytes in
Received for publication Oct 13, 2006; returned for revision Nov 17, the maxillary sinus. Aspergillus growth can be due to
2006; accepted for publication Dec 15, 2006.
1079-2104/$ - see front matter
poorly ventilated sinus, a pre-existing sinusitis, or for-
© 2007 Mosby, Inc. All rights reserved. eign bodies in the sinus. For the ostium to be ventilated
doi:10.1016/j.tripleo.2006.12.015 and drained, it must be unobstructed. If the ostium is
e23
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e24 Costa et al. June 2007
blocked, the mucociliar clearance system is negatively techniques in modern rhinology until the advent of
influenced and Aspergillus growth is favored. ESS.
Several clinical presentations have been reported, Patients treated with CL for chronic and recurrent
from acute infection to an asymptomatic form.8-9 Nev- maxillary sinusitis have a higher complication rate than
ertheless, the most frequent clinical presentation is not patients treated with ESS.16 In a comparative study of
specific, with various symptoms such as nasal obstruc- Penttila et al.,17 patients’ global evaluation was dem-
tion, purulent nasal discharge, facial pain, and chronic onstrated to be superior after ESS compared with CL.
cough. Endoscopic examination is most often normal, Overall patients’ compliance, asked postoperatively,
but edema and purulent secretions may be observed. was 80.2% in CL patients and 93.0% in ESS patients.
Often for asymptomatic forms the diagnosis is made The CT and endoscopic appearance of the sinus after
after an occasional orthopantomography performed ESS is superior compared with CL.18 Fibrosis and
during routine dental treatment (Fig. 1). abnormal bony changes of the maxillary sinus were
The characteristic CT scan presentation includes typ- encountered in more than half of CL cases.
ically heterogeneous opacities associated with a metal Inferior meatal antrostomy, as performed during CL,
dense spot in the involved maxillary sinus (Fig. 2).10-11 seems to be useless, because analysis of ciliary flow
Diagnosis is made after histologic examination, be- patterns in rabbits revealed that the nasal antral window
cause cultural exams are often negative.5,8
did not cause redirection of the mucociliary clearance
With respect to the treatment of AM, it is necessary
pattern19 and that the cilia in the sinus continue to clear
to remove surgically the sinus fungal masses and ensure
mucus toward the natural ostium despite surgical
the establishment of adequate sinus drainage and aera-
alteration.20
tion via the Caldwell-Luc (CL) procedure12-13 or endo-
For these reasons, the CL procedure is no longer the
scopic sinus surgery (ESS).9,14
surgical treatment of choice and is only indicated by
We reviewed the literature concerning the surgical
treatment of maxillary aspergilloma in the last 10 years some authors9,21 as a complementary step when the
to verify which is the actual best surgical treatment. complete removal of the fungal ball is impossible
through a middle meatal antrostomy approach alone.
In the present review we found 262 cases of maxil-
REVIEW OF THE LITERATURE lary AM in the last 10 years (Table I). The studies
Aspergillus mycetoma of the maxillary sinus may be reviewed confirm that ESS is the treatment of choice,
found in immunocompetent patients with 2 different clin- with a higher prevalence of this surgical treatment (236
ical features: symptomatic and asymptomatic. Symptom- cases, 90%) against the traditional CL approach (26
atic patients have classic symptoms of chronic sinusitis cases, 10%).
with nasal secretions, pain, and sometimes zygomatic
Only 6 studies with a consistent sample of patients
swellings. Asymptomatic patients have diagnosis after
have been published. Even if ESS can be considered to
routine radiographic examinations.
be the treatment of choice, there are 1 of the 6 studies
Certain conditions may change the normal ecosys-
with a consistent sample8 and many case reports, even
tem to allow fungal proliferation. The most common of
recently published,13,24-25 in which treatment of max-
these favorable conditions are prolonged antibiotic and
illary aspergilloma was performed with the traditional
corticosteroid treatments, nasal obstructions that aid
blockage of the ostium and anaerobic conditions, and CL. Ferreiro et al.,8 who reported the most consistent
endosinal penetrations at the time of a dental procedure, sample of patients treated with the CL, justified this
such as root canal perforation, a canal overfilling, or a surgical approach with the fact that recurrence has not
dental extraction. been documented after this procedure, whereas the re-
Even if the therapeutic strategies for treating AM are currence rate after endoscopic techniques is 6.8%. Re-
mainly surgical and ESS is nowadays the favorite ap- sults of the present review revealed a recurrence rate
proach, it is surprising that CL has continued to be after ESS lower than that reported by Ferreiro et al. (3%
performed even recently.8,12-13 This procedure, de- vs. 6.8%).
scribed in 1893 by George Walter Caldwell, provides A recent experimental study by Dufour et al.30 seems
an enlarged canina fossa opening to obtain access to the to emphasize the importance of ESS for the treatment
maxillary antrum and a complete removal of the sinus of AM. They divided 34 rabbits into 3 groups. In the
mucosa. The procedure was combined with an inferior first group (10 rabbits), A. fumigatus was inoculated
or middle meatus antrostomy that facilitated gravita- into the maxillary sinus. In the second group (10 rab-
tional drainage of secretions. The same technique was bits), A. fumigatus was inoculated into the maxillary
described independently by Henri-Paul Luc in 1897.15 sinus in the presence of a wound in the mucosa. In the
The CL procedure remained one of the most used third group (14 rabbits), A. fumigatus was inoculated
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Volume 103, Number 6 Costa et al. e25
into the maxillary sinus in the presence of a blocked trauma to the patient is less than that derived from
ostium. They found that noninvasive fungal sinusitis external procedures, and ventilation and drainage are
had been induced in 2 rabbits of the second group and re-established through the natural ostia31 (Fig. 4). En-
8 rabbits of the third group. They concluded that intro- doscopic sinus surgery with a middle meatus antros-
duction of fungi into a sinus with a blocked ostium tomy presents only 1 technical problem for the treat-
induces fungal sinusitis. The traditional CL procedure ment of maxillary AM. It does not allow visualization
does not affect the maxillary natural ostium, which of the angle formed by the bony lacrimal duct and the
seems to be important in the development of AM. anterior maxillary sinus wall (lacrimal recess of the
The aim of ESS, which has replaced traditional CL, maxillary sinus). Permanence of mycotic concretions at
is to open the natural ostium of the sinus involved to this level has been suggested as a possible cause for
restore drainage and ventilation. Debridement of the recurrence.22 However, in cases of difficult removal of
polypoid mucosa, if present, in the middle meatus can mycotic concretions it is possible to complete the re-
be performed, and a wide antrostomy may be created moval by a trocar in the canine fossa,9 the so-called
by removing most of the posterior fontanelle and con- double approach.27
necting a possible secondary maxillary ostium to the Endoscopic sinus surgery with middle meatus antr-
area of the maxillary natural ostium anteriorly. From ostomy, with or without a canine fossa approach, is the
the middle meatus antrostomy, sinus lavages may be treatment of choice in 4 of the 6 studies reviewed with
performed using an angled aspirator to facilitate endo- a more consistent sample of patients,9,14,26,27 but the
nasal discharge of the mycotic concretions of the sinus most recent study by Dufour et al.14 is an integration of
(Fig. 3). The advantages of this method are that the a previous sample.9 Double approach was performed in
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e26 Costa et al. June 2007
Table I. Continued
Recurrence
Authors and institute Year No. patients ESS after ESS Caldwell Luc Comment
Kobayashi29 1995 1 — — 1 Case report
Department of Oral Surgery,
Saitama, Japan
Total 262 236 (90%) 7 (3%) 26 (10%)
ESS, endoscopic sinus surgery; FESS, functional endoscopic sinus surgery.
Fig. 3. Removal of the mycotic concretions from the middle Fig. 4. Postoperative endoscopic view one year after middle
meatus after sinus lavages from the antrostomy. meatus antrostomy showing maintenance of opening and the
absence of discharge from the sinus.
97 of 150 procedures (65%) by Dufour et al.14 Feng canine fossa approach), and group C included 12 pa-
et al.27 observed that the period of convalescence of tients who were operated on using an endoscopic ca-
double pathway surgery (via ostium of maxillary sinus nine fossa approach alone. No recurrences were noted
and canine fossa) was 4.7 weeks, whereas single path- in any group, but in group B 3 patients presented mild
way (via ostium of maxillary sinus only) was 9.3 complications, such as persistent purulent discharge
weeks. They asserted that the double pathway operation through the meatotomy and nasal crusting. The authors
is superior to the single pathway. There is a general concluded that the endoscopic canine fossa approach of-
agreement that ESS is effective in treating aspergilloma fers several advantages over other techniques: an optimal
of the maxillary sinus and that general or local antifun- visualization of all maxillary sinus walls; the possibility of
gal drugs are not indicated.14,27 performing the procedure under local anesthesia; the pres-
The last of the 6 studies with a consistent sample of ervation of the anatomy and physiology of the natural
patients retrospectively analyzed the results of the sur- maxillary ostium, and an easy removal of any foreign
gical treatment of 31 patients presenting maxillary bodies of dental origin in the sinusal cavity which could
AM.22 Patients were divided into 3 groups. Group A favor the development of AM.
included 10 patients operated on with an endonasal The first observation regarding this study is the short
middle meatotomy only, group B included 9 patients follow-up of the sample, which is of at most 6 months.
who were operated on using a combined approach Concerning the preservation of the natural maxillary
(endonasal middle meatus antrostomy and endoscopic ostium, we may observe that it cannot be considered an
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e28 Costa et al. June 2007
23. Chao TK. Triple discrete fungus balls of the paranasal sinuses. 29. Kobayashi A. Asymptomatic aspergillosis of the maxillary sinus
Otolaryngol Head Neck Surg 2004;131:1014-5. associated with foreign body of endodontic origin. Report of a
24. Shams MG, Motamedi MH. Aspergilloma of the maxillary sinus case. Int J Oral Maxillofac Surg 1995;24:243-4.
complicating an oroantral fistula. Oral Surg Oral Med Oral 30. Dufour X, Kauffmann-Lacroix C, Goujon JM, Grollier G, Rodier
Pathol Oral Radiol Endod 2003;96:3-5. MH, Klossek JM. Experimental model of fungal sinusitis: a pilot
25. Khongkhunthian P, Reichart PA. Aspergillosis of the maxillary study in rabbits. Ann Otol Rhinol Laryngol 2005;114:167-72.
sinus as a complication of overfilling root canal material into the 31. Stammberger H. Endoscopic surgery for mycotic and chronic re-
sinus: report of two cases. J Endod 2001;27:476-8. curring sinusitis. Ann Otol Rhinol Laryngol Suppl 1985;119:1-11.
26. Castelnuovo P, Gera R, Di Giulio G, Canevari FR, Benazzo M,
Emanuelli E, et al. Paranasal sinus mycoses. Acta Otorhinolar- Reprint requests:
yngol Ital 2000;20:6-15. Dr. F. Costa
27. Feng LR, Tan CQ, Guo QM. Treatment of noninvasive aspergil- Clinica di Chirurgia Maxillo-Facciale
losis of maxillary sinus by functional endoscopic sinus surgery. Azienda Ospedaliero Universitaria
Lin Chuang Er Bi Yan Hou Ke Za Zhi 2000;14:554-5. P.le S. Maria della Misericordia
28. Ogata Y, Okinaka Y, Takahashi M. Antrolith associated with 33100 Udine
aspergillosis of the maxillary sinus: report of a case. J Oral Italy
Maxillofac Surg 1997;55:1339-41. maxil2@med.uniud.it