Original article

Rhinocerebral mucormycosis: the disease spectrum in 27 patients

Sandeep Mohindra,1 Satyawati Mohindra,2 Rahul Gupta,1 Jaimanti Bakshi2 and Sunil Kumar Gupta1
1
Department of Neurosurgery and 2Department of Otolaryngology and Head Neck Surgery, Postgraduate Institute of Medical Education and Research,
Chandigarh, India

Summary The variable forms of clinical complaints, findings and time interval of presentation in
27 cases of mucormycosis have been described, which were encountered over a span of
8 years. The previous concept about this fungal infection attacking chronic,
debilitated, immunocompromised patients does not appear to hold true. Seven of the
27 patients (22.2%) did not reveal any predisposing factors and their outcome of
42.9% survival seems to be poorer than the total outcome (66.7%). ÔChronic formÕ of
disease presentation, the definition of which is still not delineated, was encountered in
four patients (14.8%). Again, the outcome was not significantly different from the total
survival. Burr-hole tap of an intracranial abscess revealing mucor in a 2-month-old
infant has been described. Even in the present era, extranasal exenteration of sinuses
along with disfiguring orbital exenteration is required to ensure satisfactory surgical
debridement. Control of the underlying predisposing illness, along with the aggressive
surgical debridement and the parenteral administration of amphotericin B, remains the
treatment essentials even today.

Key words: Predisposing factors, rhinocerebral, cranio-facial, mucormycosis.

seven cases of rhino-orbito-cerebral mucormycosis

Introduction
Mucormycosis is an acute, often fatal infection caused
by fungi of the family Mucoraceae. The principal
pathogens in this family are Rhizopus, Mucor and
Absidia species. These organisms belong to the class
Phycomycetes, which also encompasses the order
Entomophthorales.1–3 Often, mucormycosis attacks
immunocompromised patients, notably diabetes melli-
tus,4–10 severe burns, blood dyscrasias, renal diseases,11
sepsis, severe dehydration4,12 and cirrhosis.11
Rhino-orbito-cerebral mucormycosis is notable for
its high morbidity and mortality.4,6 Early recognition
of this disorder, particularly in medically compromised
patients, prompts early medical and surgical manage-
ment, leading to an improved prognosis.6,13 Historic-
ally, only a few patients have survived without orbital
exenteration to eradicate the infection.14 Twenty-
Correspondence: Dr Sandeep Mohindra, Department of Neurosurgery,
Postgraduate Institute of Medical Education and Research, Chandigarh
160012, India.
Tel.: +91 172 275 6712/269 3124. Fax: +91 172 274 4401.
E-mail: satya_sandee@yahoo.com
Accepted for publication 10 January 2007
managed at our institute, over a period of 8 years
are discussed, regarding presenting complaints and
management.
Patients and methods
We conducted a retrospective review of 27 patients
treated at our hospital for rhino-cerebral mucormycosis
from January 1997 to December 2005. Hospital in-
patient records, radiological investigations, operative
and out-patient follow-up records were analysed for
predisposing factors, demographic profile (age/sex),
clinical presentation, complications and causes of mor-
tality. Radiological studies were also reviewed for
disease sites, location and extension. All patients
underwent contrast-enhanced computerised tomogra-
phy (CT) scan of the nose, paranasal sinuses, orbit and
cranial cavity, obtained in both axial and coronal
planes. Gadolinium-enhanced magnetic resonance ima-
ging (MRI) was obtained in eight patients. The diagnosis
was confirmed by microbiological and pathological
examination of transnasal or cerebral biopsy/aspiration
material. The clinical details of all the patients are
summarized in Table 1.

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doi:10.1111/j.1439-0507.2007.01364.x Journal Compilation  2007 Blackwell Publishing Ltd • Mycoses (2007), 50, 290–296
 Rhinocerebral mucormycosis

Table 1 Summary of rhino-orbito-cerebral mucormycosis

Age/ Clinical Cranial Radiological Surgical Orbital

Predisposition sex presentation nerve Intracranial involvement intervention surgery Outcome

1. Nephrotic syndrome 13/M Bloody discharge – – Sinusoidal – – Death

2. DM 23/F Painful proptosis, 3,4,5(S),6,7 – Sino-orbital Pansinusectomy – Alive
diplopia
3. DM 48/M Proptosis, blind 2,3,4,5,6,7 Cav. sinus Cav. sinus, orbital Med. maxillectomy Exent Alive
4. Nil 45/F Proptosis 3,4,5,6,7 – Sino-orbital – Exent Death
5. Nil 45/M Proptosis, blind 2,3,5 – Sino-orbital Pansinusectomy Exent Alive
6. Nil 40/M Teeth loosening 5(S) – Sinusoidal Pansinusectomy – Death
7. Nil 2/12F Palatal perforation – Brain abscess Frontal lobe abscess Burr-hole tap – Alive
8. Bronchial asthma 26/F Proptosis, blind 2,3,4,6 – Sinusoidal intraconal Ethmoidectomy Exent Alive
9. DM 60/M Proptosis, blind 2,5 – Sino-orbital Ethmoidectomy Exent Death
10. DM, pancr., chr. alc. 48/M Proptosis, blind 3,4,6,7 Cav. sinus Cav. sinus, orbital – – Death
11. DM, renal transplant 40/M Proptosis, blind 2 – Orbital – – Death
12. DM, corneal 58/M Orbital pain, 3,4, 6 – Sino-orbital Ethmoidectomy – Alive
transplant proptosis
13. Nil 36/F Diplopia, trismus 6 Infratemporal Sinusoidal, Pansinusectomy – Alive
infratemporal
14. Necrotizing gingivitis 38/FProptosis, orbital 5(S) – Sino-orbital disease Ethmoidectomy Exent Alive
cellulitis
15. DM, oesophagitis 60/F Blind, proptosis 2,3,4,5,6,7 – Sino-orbital disease Pansinusectomy Exent Alive
16. Cirrhosis 48/M Pain, proptosis, – – Sino-orbital disease Pansinusectomy Decomp Alive
eschar
17. DM, herpes 48/M Blind, pain, 2,3,4,6 Occlusive Mca infarct, Ethmoidectomy Exent Alive
proptosis stroke sino-orbital
18. Nil 18/M Blind 2,3,4,6 Frontal mass Sino-cranial disease Craniofacial – Death
debridement
19. DM 71/F Blind 2 – Sinusoidal disease Endoscopic – Alive
clearance
20. DM 35/F Blind, proptosis, 2,3,4,6 – Sino-orbital disease Pansinusectomy Exent Alive
diplopia
21. DM 48/M Blind, proptosis, 2,3,4,5(SM), – Sino-orbital disease Maxillectomy Decomp Alive
diplopia 6,7
22. DM 45/M Facial pain, eschar – – Sinusoidal disease Caldwel luc – Alive
23. DM 45/M Facial pain, blind 2 – Sino-orbital disease Ethmoidectomy Decomp Alive
24. DM 63/M Blind, palatal – Occlusive Aca, mca infarct – Exent Alive
perforation stroke
25. DM 24/F Painful proptosis, 3,4,5(S),6 Cav. sinus, Fr. cerebritis, Pansinusectomy – Alive
diplopia sino-orbital
26. Nil 24/F Raised ICP, seizures – Thalamic Thalamic abscess Temp polectomy, – Death
lesion tap
27. DM 60/M Altered sensorium – Bifrontal Both frontal lobes – – Death
mass

DM ¼ Diabetes mellitus, ICP ¼ Intracranial pressure.

was found to be a chronic alcoholic, with a history of

Results
Predisposing factors
Predisposing factors included diabetes mellitus
(n ¼ 16), immunosuppressive drugs (n ¼ 3), hepatic
cirrhosis (n ¼ 1) and necrotizing gingivo-stomatitis
(n ¼ 1). One of the diabetic patients was a renal
transplant recipient and was receiving azathioprine,
cyclosporin and prednisolone. Another diabetic patient
acute pancreatitis in the recent past.
Clinical presentation
The age range was 2.5–71 years (mean ¼ 41.7 -
years). The male to female ratio was 16:11. Fifteen
patients presented relatively early, with history of less
than 2 weeks (Fig. 1a,b), while others had a pro-
longed symptomatology. In most patients (n ¼ 21),

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Journal Compilation  2007 Blackwell Publishing Ltd • Mycoses (2007), 50, 290–296 291
S. Mohindra et al.

Figure 2 Sagittal section of contrast MRI, showing periorbital

thickening.

nasal sinuses, involving mostly ethmoidal sinuses. In 16

patients, masses extended into the orbits causing
proptosis (Fig. 2). Intracranial extension was seen in
10 patients, in form of cavernous sinus thrombosis
(n ¼ 3) (Fig. 3), intracranial masses (n ¼ 3) (Figs 4, 5
and 6a), brain abscesses (n ¼ 2) (Fig. 6b), and ischae-
mic infarcts (n ¼ 2). In one of these patients, there was
a massive intracranial extension involving entire floor of
anterior cranial fossa (Fig. 4). MRI was helpful for better
delineation of the extent of the disease.

Figure 1 Axial section CT scans showing rapid spread of the Surgical management
disease (4 days).
Paranasal sinuses were involved in 21 patients, orbits in
the symptomatology started with ophthalmological 20 patients, while 10 had intracranial spread of disease.
complaints. The major presenting symptoms were A total of 23 patients underwent surgical intervention.
proptosis (n ¼ 16), blindness (n ¼ 14), retro-orbital
pain (n ¼ 7), diplopia (n ¼ 5), bloody nasal discharge
(n ¼ 1). Six patients had lower motor neuron facial
paralysis. As many as 14 patients had multiple cranial
nerve palsies with variable involvements of third,
fourth, fifth, sixth cranial nerves. Deterioration in
sensorium was observed in 10 patients, while one had
seizures. Eschar (black necrotic tissue surrounded by
pale mucosa) was seen carpeting the turbinates and
palate in four patients. One patient presented with
loosening of teeth due to infra-orbital nerve disease
secondary to paranasal sinusoidal disease.

Radiological studies

All patients underwent contrast-enhanced CT scans, Figure 3 Axial section of contrast MRI, showing invasion of
while MRI was performed in eight patients. Twenty-two cavernous sinus bilaterally. Both internal carotid arteries are
patients had contrast-enhancing masses within para- encased.

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Figure 4 Coronal section of contrast MRI, showing massive
carpeting of floor of anterior cranial fossa by the disease.
Figure 5 An example of deep seated invasive mucormycosis.
Four patients could not be operated, as three were
haemodynamically unstable, while one did not give
consent for surgery. Surgical intervention for the orbital
pathology was required in 13 patients; 10 underwent
orbital exenteration and in three patients, orbital
decompression was achieved by removal of the lamina
papyraceae. Three of the 10 patients with intracranial
disease required surgical intervention. Both patients
with brain abscesses required burr-hole and aspiration,
while the third one required single stage cranio-facial
resection to debulk the frontal lobe mass. Nineteen of
the 21 patients with sinusoidal disease underwent
surgical debridement. Six patients required multiple
debridements, while two underwent endoscopic exen-
teration of the sinuses. Operative findings revealed
polyps in paranasal sinuses along with necrotic tissue
and serosanguinous discharge, while black eschar
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Rhinocerebral mucormycosis
Figure 6 (a) Fungal abscess formation (b) after performing biopsy
of non-enhancing intracranial lesion.
carpeted over turbinates and hard palate in four
(14.8%) patients. Post-surgical debridement, all 23
patients were administered amphotericin B, in a dose
of 1 mg kg)1 body weight to the total dose of 2.5–4.0 g.
A test dose of 1 mg of amphotericin B was given
intravenously over 1 h and in the absence of adverse
reactions, increased doses (10–15 mg increments) were
given every 12 h, until a daily dose of 1 mg kg)1 day)1
was achieved.15,16 The onset of nephrotoxicity, was the
usual cause for limiting the dose of amphotericin B.
Liposomal amphotericin B was not used in any of our
patients due to cost constraints. Once a day irrigation of
paranasal sinuses with povidone–iodine (10%) solution
was performed for all patients, during postoperative
management.
Treatment results
Eighteen (78.3%) of the operated 23 patients recov-
ered, while all non-operated (n ¼ 4) patients expired.
293
S. Mohindra et al.
Over-all, nine (33.3%) of 27 patients in our series had
unfavourable outcome; eight patients expired, while one
left the hospital against medical advice. The cause of
death was pyogenic septicaemia in three patients,
fungal meningoencephalitis in three patients, while
drug induced renal failure and multiorgan dysfunction
syndrome led to mortality in one patient each. Eighteen
(66.7%) patients had favourable outcome and all have
been followed to date. Of the 14 patients, who presented
early, 11 (78.6%) made a good recovery, while three
(21.4%) expired. Among 13 patients with delayed
diagnosis, six (46.2%) expired.
Pathological diagnosis was established in all operated
23 patients, by obtaining a biopsy from involved area.
Microscopic findings were coagulative and haemorrhagic
necrosis with non-septate hyphae, suppurative inflam-
mation and vascular thrombosis.
Discussion
Phycomycetes are ubiquitous fungi occurring in soil,
air, skin, body orifices, manure, spoilt food, bread and
dust.4,17 Inoculation occurs by inhalation, when spores
reach the nasopharynx and oropharynx.14 At this
stage, most patients generate phagocytic containment
of the organisms. Individuals with compromised cellular
and humoral defence mechanisms may generate inad-
equate response.14 The fungus may, then spread to the
paranasal sinuses and subsequently to the orbit, men-
inges and brain by direct extension.14 Mucormycosis,
preferentially invades the walls of the blood vessels
resulting in vascular occlusion, thrombosis and infarc-
tion and even haematogenous dissemination to cen-
tral nervous system from the primary pulmonary
focus.4,7,18 Vascular occlusion may occur in ophthal-
mic artery,10 internal carotid artery and cavernous
sinus.7,14 Mixed fungal infection with mucormycosis
has been reported, but it does not require alteration in
the management protocol.19
Symptoms that may suggest mucormycosis in sus-
ceptible individuals include multiple cranial nerve
palsies,20 unilateral periorbital facial pain, orbital
inflammation, eyelid oedema, blepharoptosis, proptosis,
acute ocular motility changes, internal or external
ophthalmoplegia, headache or acute vision loss.3,20
Protuberant, fixed eyeball without vision is a common
ophthalmological presentation.5 Mucormycosis is fre-
quently seen in predisposed patients of diabetic ketoac-
idosis,5,17,21–23 neutropenia, immunosuppressive
medications,21,23 renal failure,6,22 severe burns, mal-
nutrition, protracted, severe diarrhoea or desferoxamine
therapy.4,6,23 Few cases of rhino-orbital mucormycosis
294 Journal Compilation  2007 Blackwell Publishing Ltd • Mycoses (2007), 50, 290–296
with acquired immunodeficiency syndrome and neu-
tropenia have been reported.10,24 Acidosis, probably
accompanies most of the cases of diabetes, renal and
diarrhoeal illness. It is the acidosis, the chief biochemical
and biophysical derangement, which is responsible for
the initiation of the fungal infection. Rhizopus species
have an active ketone reductase system and thrive in
high glucose and acidotic conditions. These patients also
have decreased phagocytic activity because of an
impaired glutathione pathway. The normal serum
inhibits Rhizopus whereas serum from patients of
diabetic ketoacidosis stimulates growth.12 Mucormyco-
sis in an immunocompetent host is rare and is often
related to trauma.23
Preoperative contrast-enhanced CT scan is useful in
defining the extent of the disease.18 The scans show the
edematous mucosa, fluid filling the ethmoid sinuses and
destruction of periorbital tissues and bony margins.
Heterogeneously enhancing anterior cranial fossa floor
masses, contiguous with sinusoidal masses with intra-
orbital invasion as periorbital thickening or focal
nodules is a strong indicator towards fungal infection.
MRI is useful in identifying the intradural and intra-
cranial extent of the disease, cavernous sinus thrombo-
sis or thrombosis of cavernous portion of the internal
carotid artery8 (Fig. 3). Perineural spread of the disease
can also be demonstrated with contrast-enhanced MRI
scans.25 In the present series, also, contrast-enhanced
CT scans demonstrated an irregular sinusoidal mass,
with occasional extension into the orbit, with heterog-
enous contrast enhancement. MRI was found to be
superior in delineating the intracranial spread and in
identifying invasion of cavernous sinus by the disease as
well as in the detection of vascular complication like
ischaemia.
In our series, there were six (23.1%) patients,
where no definite predisposing factor could be found.
Similar cases have been reported earlier, but are
uncommon.3,26,27 Four (66.7%) of these patients
survived after debridement and amphotericin B ther-
apy. Patients, who have no underlying immunocom-
promised state, are considered to have better
prognosis.2 Nevertheless, two of our immunocompe-
tent patients died, one of fungal meningitis, and the
other of multiorgan failure. This was probably, because
of the diagnostic delay due to immunocompetent state
of the patient. The infant reported in the present series
is probably the youngest reported in the literature.28
Inspite of facial necrosis, a poor prognostic indica-
tor,6,22 his infant improved.
There were six patients, where the disease evolved
over a period of months. This Ôchronic formÕ of disease
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was also treated with repeated surgical debridements
and amphotericin B. The outcome of these patients
(83.3%) was slightly better, when compared with total
outcome (66.7%). The only patient, who was lost had
an 8-month history of molar pain, loosening of teeth
and multiple sinuses over the face, with the involvement
of the right orbit. This patient died of fungal meningitis.
Four of these patients had diabetes as predisposing
factor. All except one patient with chronic form of
disease had orbital involvement. Similar Ôchronic formÕ
of the disease has been reported earlier5 in two patients.
Contrary to the literature,5 none of our patients had
cavernous sinus or internal carotid artery involvement.
The maximum time from symptom onset to diagnosis
was 4 years, while median time interval was 9 months
for these six patients.
Even when the role of orbital exenteration remains
controversial, it was mandatory in patients having
intraorbital focal masses and widespread necrosis.
Radiological findings may help in deciding about orbital
exenteration when supplemented with clinical findings.
Such a mutilating surgery may be avoidable, if no
localized intraorbital mass is present. Exenteration of the
sinus disease, with or without decompression of the
orbit and amphotericin B therapy may be useful in
preserving the orbit, without compromising the disease
clearance. Although, the vision in these patients would
never return to normal, it is cosmetically more accept-
able. The extent of surgical excision should balance the
degree of morbidity and mutilation against the life-
threatening risk, this fungal infection may represent.14
Endoscopic sinus surgery may be of help in selected
patients,29 but proved to be of no help to us (n ¼ 2), as
the disease process and repeated surgical interventions
distorted the bony architecture to a great extent.
Irrigation and packing of involved orbital areas with
amphotericin B (1 g cm)3) has been recommended in
view of vaso-occlusive nature of pathology.9,14 Amph-
otericin B local packing of the paranasal sinuses has also
been advocated.14
Liposomal amphotericin, administered at the dosage
of 5 mg kg)1 day)1,20,30 can build up the drug levels in
one-fourth of time duration when compared with
conventional amphotericin therapy, with minimal renal
toxicity and greater tissue penetration.30 Cost remains
the major limiting factor. The sinusoidal debridement
remains essential, even when orbital preservation has
been attempted, with varying success.14,24,29,31 The
adjuvant therapies range from local amphotericin
irrigation,4,9,14 packing,4,14 hyperbaric oxygen,20
5-fluoro-cytosine18 and even decompressive craniotomy
for malignant occlusive stroke.7
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Journal Compilation  2007 Blackwell Publishing Ltd • Mycoses (2007), 50, 290–296
Rhinocerebral mucormycosis
The favourable outcome in our series is 66.7%. The
presence or absence of predisposing factors, also did not
determine the outcome. Three of four patients with
wildly spreading black eschar over the turbinates, the
poor prognosticator6,22 died. The outcome becomes
highly unfavourable, once there is intracranial spread of
disease.4,7 Nevertheless, four (40%) of our 10 such
patients survived.
Conclusion
Rhino-cerebral or cranio-facial mucormycosis, once
thought to occur exclusively in diabetics, can occur in
other immunosuppressive patients and also apparently
healthy individuals. Patients may not present a typical,
unilateral acute illness, comprising of black eschar,
rather this entity should also be entertained among
long-standing, smouldering sinus symptomatology. The
clinical suspicion, supplemented with radiological inves-
tigations, aid in making correct diagnosis. Prompt
control of immunosuppression, other predisposing fac-
tors, initiation of amphotericin B therapy and meticu-
lous, extensive surgical debridement of the involved
tissues and drainage of the focal collections in the orbit
and the cranial cavity are required to achieve a good
outcome. Orbital exenteration in selected patients, may
help to have better disease control.
The prolonged survival of debilitated patients, along
with increased therapeutic use of antibiotics and
immunosuppressive agents, has increased the incidence
of mucormycosis. Our heightened awareness of this
devastating condition is the first step towards a more
favourable outcome in this disease.
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