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| ORIGINAL ARTICLE |
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| Year : 2003 | Volume
: 51
| Issue : 3 | Page : 231-236 |
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Rhino-Orbito-Cerebral Mucormycosis. A Retrospective Analysis of Clinical Features and Treatment Outcomes
S Nithyanandam, Moire S Jacob, Ravindra R Battu, Reji K Thomas, Majorie A Correa, O D'Souza
Department of Ophthalmology, St. John's National Academy of Health Sciences, Bangalore, India
Correspondence Address:
S Nithyanandam
Department of Ophthalmology, St. John's National Academy of Health Sciences, Bangalore
India
 Source of Support: None, Conflict of Interest: None  | Check |
PMID: 14601848 
Objective: The conventional management of rhino-orbito-cerebral (ROC) mucormycosis includes control of metabolic abnormality, administration of amphotericin B and surgery that spans simple sinus clearance, radical debridement and orbital exenteration. Recent literature includes anecdotal descriptions of successful treatment with conservative management of involved orbits. We evaluated the clinical features and outcome of treatment for the different stages of ROC mucormycosis. Method: In this retrospective case series, 34 case records of patients with a histopathological diagnosis of ROC mucormycosis treated between 1992 and 2000 were reviewed. Three clinical stages and three treatment groups were identified. Patients with limited sino-nasal disease (Clinical stage I) underwent sino-nasal debridement (Treatment group A). Patients with limited rhino-orbital disease (Clinical stage II) underwent either sino-nasal debridement alone (Treatment group A) or orbital exenteration in addition to sino-nasal debridement (Treatment group B). Patients with rhino-orbito-cerebral disease (Clinical stage III) did not undergo any surgical procedure (Treatment group C). Thirty-three patients received intravenous amphotericin B. Outcome for each group was measured as "Treatment success" (disease free, stable patient with metabolic abnormality under control) and "Treatment failure" (progression of disease with worsening general condition or mortality due to the disease). Results: Uncontrolled diabetes in 30 (88.2%) of 34 patients was the commonest underlying disease and 16 (53.3%) of 30 diabetics had ketoacidosis. Chronic renal failure (n = 4), hepatic disease (n = 3) and idiopathic thrombocytopenia (n = 1) were the other underlying diseases. Eleven patients had stage I disease, 16 patients had stage II disease and seven patients had stage III disease. All 11 patients with stage I disease received treatment A; of 16 patients with stage II disease, 7 received treatment A and the remaining with stage III disease received treatment B; 7 patients with stage II disease received treatment C. Ten of 11 patients (91%) with stage I disease had treatment success. In patients with stage II disease, 7 of 7 (100%) with treatment A and 1 of 9 (11.1%) with treatment B had treatment success. All seven patients with stage III disease had treatment failure.
Conclusion: Debridement of the sinuses is necessary in all cases of rhino-orbito-cerebral mucormycosis. Diagnosis in the early stage needs a high degree of suspicion. There is a definite role for retention of orbits in patients whose metabolic derangement is rapidly controlled and orbital involvement is non-progressive.
Keywords: Rhino-orbito-cerebral mucormycosis, clinical features, treatment outcome, exenteration, conservation of orbits.
How to cite this article:
Nithyanandam S, Jacob MS, Battu RR, Thomas RK, Correa MA, D'Souza O. Rhino-Orbito-Cerebral Mucormycosis. A Retrospective Analysis of Clinical Features and Treatment Outcomes. Indian J Ophthalmol 2003;51:231-6 |
How to cite this URL:
Nithyanandam S, Jacob MS, Battu RR, Thomas RK, Correa MA, D'Souza O. Rhino-Orbito-Cerebral Mucormycosis. A Retrospective Analysis of Clinical Features and Treatment Outcomes. Indian J Ophthalmol [serial online] 2003 [cited 2021 Jan 16];51:231-6. Available from: https://www.ijo.in/text.asp?2003/51/3/231/14677 |
Mucormycosis is an acute, fulminant and fatal fungal infection in humans.[1],[2] Demonstration of tissue invasion on histopathology is mandatory for diagnosis.[2],[3] Histopathology is characterised by the presence of broad aseptate filamentous fungi branching at right angles with a predilection for intravascular invasion.[3] The rhino-orbito-cerebral form is the commonest form of disease.[1],[2],[4] The term rhino-orbito-cerebral (ROC) mucormycosis refers to the entire spectrum of the disease.[2],[4] With rare exceptions it usually starts in the sino-nasal tissues (limited sino-nasal disease), progresses to the orbits (limited rhino-orbital disease) and finally affects the central nervous system (rhino-orbito-cerebral disease). Patients manifest with signs and symptoms relating to the involved tissues. The progression of the disease to the orbits produces a constellation of pathgnomonic signs and symptoms, which makes early diagnosis and treatment possible.[5],[6]
Aggressive surgical debridement of all involved tissues including exenteration of involved orbits with prolonged administration of Amphotericin B is the most common treatment regime. [6],[7],[8],[9] However, there are increasing reports of success with limited or no surgical intervention in the orbit. [2],[10],[11],[12],[13],[14],[15],[16] In this retrospective study we evaluated the clinical characteristics and treatment outcome for the different stages of ROC mucormycosis.
| Materials and Methods | |  |
Charts of 34 patients with histopathologically confirmed diagnosis of ROC mucormycosis treated at St. John's Medical College Hospital, Bangalore, India from January 1992 to December 2000 were analysed. Evaluation at presentation included a detailed history, and otorhinolaryngologic, ophthalmic and neurologic examinations to assess the extent of the disease. We identified three distinct clinical stages based on the signs and symptoms and degree of disease progression [Table - 1][Table - 2]. Clinical stage I had signs and symptoms referable to only sino-nasal disease. Clinical stage II had rhino-orbital disease. Loss of vision, ocular motility restriction, proptosis, external and internal ophthalmoplegia, conjunctival pallor, chemosis and central retinal artery occlusion (CRAO) indicated orbital involvement. Clinical stage III had the full spectrum of ROC disease, indicated by cavernous sinus thrombosis, hemiplegia and altered sensorium. Facial nerve palsy indicated spread of infection to the infratemporal fossa through the inferior orbital fissure.
Initial investigations included complete blood counts, blood urea, serum creatinine, serum glucose, urine for ketone bodies and blood gas analysis. Diagnosis was made on histopathological examination and KOH preparation of biopsy specimens obtained from the nasal cavity and/or paranasal sinuses and the palate. An orbital fine needle aspiration cytological (FNAC) study was done in some patients when histopathological diagnosis from other sites was equivocal. Computerised tomographic scans of the paranasal sinuses, orbits and brain were obtained to assess the extent of disease.
Treatment with systemic Amphotericin B was started as soon as a diagnosis of mucor was established in all patients, along with treatment to stabilise the underlying metabolic derangement. After a test dose of 1 mg of amphotericin B in 100 ml of normal saline, 0.7 mg/kg/day of amphotericin B was given over 6 hours. The dose was increased by 25 mg/day on alternate days to a maximum of 100 mg/day and continued till a cumulative dose of 2.5 - 3 gms was reached. Three distinct treatment groups were identified based on the nature of surgery that the patients underwent. Patients in treatment group A (TG-A) underwent sino-nasal debridement only. Some patients in this group who had orbital involvement also received intraorbital Amphotericin B (1mg/ml/dose retrobulbar injection once a day or through an irrigating cannula). Treatment group B (TG-B) consisted of sino-nasal debridement with orbital exenteration. Treatment group C (TG-C) received only medical treatment with intravenous amphotericin B as all these patients refused surgery.
The outcome for each treatment group was evaluated in terms of treatment success and treatment failure. Treatment success was defined as a disease-free, stable patient with controlled metabolic status. Treatment failure was defined as progression of disease to a more advanced stage, worsening general condition or mortality due to the infection.
| Results | | |
Disease demographics
The average age of the 18 male and 16 female patients was 48.2 years (14-69 years). Twenty-four (70.6%) patients presented between June and September; eight (23.5%) patients presented in December and January, and two (5.9%) patients presented February and May.
Signs and symptoms
The signs and symptoms with their frequency of occurrence are listed in [Table - 1]. Eleven patients had sino-nasal disease (clinical stage I), 16 had rhino-orbital disease (clinical stage II) and seven had rhino-orbito-cerebral disease (clinical stage III) [Table - 2]. Differences in the severity of orbital signs between TG-A and TG-B of clinical stage II are shown in [Table - 3]. The severity of proptosis was the main orbital differentiating determinant between the two treatment groups in this stage. There was no difference in the occurrence of CRAO or ophthalmoplegia between the two groups.
Predisposing condition
Uncontrolled diabetes in 30 (88.2%) patients was the commonest underlying disease and 16 of 30 patients (53.3%) had diabetic ketoacidosis. The other underlying diseases included chronic renal failure (n = 4), hepatic disease (n = 3) and idiopathic thrombocytopenia (n = 1). [Table - 4] lists the underlying disease for each treatment group. Patients in TG-B and TG-C had more severe metabolic derangement with some patients having more than one underlying disease. There was also a marked difference in the severity of the underlying disease in clinical stage II patients undergoing TG-A and TG-B [Table - 3][Table - 4]. Patients in TG-B had more severe forms of metabolic derangement, such as refractory hyperglycemia in 3 of 9 (33.3%) patients; and ketoacidosis in 6 of 9 (66.7%) patients; two or more concurrent underlying diseases were present in 3 of 9 (33.3%) patients. All patients in TG-A had hyperglycemia, which responded to intensive medical treatment, including the three patients with ketoacidosis.
Diagnosis
Evidence of maxillary and ethmoidal sinusitis was present in 31 patients while 3 had maxillary disease only [Figure - 1]. In 18 patients orbital changes on CT were evident which included pre-septal oedema, proptosis, medial rectus thickening and minimal obliteration of fat shadow at the orbital apex [Figure - 2][Figure - 3]. Intracranial disease on CT included cerebral infracts (n = 2), cerebellar infarct (n = 1), cavernous sinus thrombosis
(n = 2) and a mass in the cavernous sinus (n = 1) [Figure - 4]. Remarkably, CT findings were absent in 5 patients with clinical evidence of orbital disease [Figure - 5] and 2 patients with CNS disease.
Medical treatment
Thirty-three patients received intravenous amphotericin B as soon as a diagnosis of mucor was established. The cumulative dose ranged from 25mg to 2500mg. Two patients with rising serum creatinine and two patients due to drug hypersensitivity were switched to oral ketoconazole. Local amphotericin B into the orbit was administered in four patients in clinical stage II, who received Treatment A.
Surgical treatment
Surgical treatment varied depending on the clinical stage as shown in [Table - 4]. Overall 18 patients received Treatment A (TG-A), 9 received Treatment B (TG-B) and 7 patients received Treatment C (TG-C). All 11 patients with sino-nasal disease underwent debridement of all necrotic tissue in the sinuses and the nasal cavity (TG-A). Either endoscopic sinus clearance or the external approach was used. Seven of 16 patients with rhino-orbital disease underwent sinus debridement alone (TG-A). Four of these received local amphotericin B into the orbit. The remaining nine patients with clinical stage II disease underwent orbital exenteration with extensive sinus debridement (TG-B). This included partial maxillectomy and excision of necrosed facial skin in four patients. None of the seven patients in clinical stage III underwent any surgical procedure (TG-C).
Outcome
Patients undergoing Treatment A had the best outcome with 17 of 18 (94.4%) treatment success [Table - 4]. All 17 patients had no evidence of disease at follow-up ranging from 2 months to 8 years. This included 10 patients with sino-nasal disease and all 7 patients with rhino-orbital disease. One patient from clinical stage I died due to amphotericin B-induced acute renal failure and not as a consequence of the infection per se . Treatment failure occurred in 8 of 9 (88.9%) patients with rhino-orbital disease undergoing Treatment B with treatment success in 1 of 9 (11.1%) patient. Seven of these patients died due to uncontrolled disease and one patient was discharged on request with spread of infection to the contralateral side. All 7 patients with rhino-orbito-cerebral disease who received Treatment C were treatment failures. Three patients died due to uncontrolled disease. Four were discharged on request with worsening condition and did not return for follow-up. Thus treatment success was seen in 18 (52.9%) patients, treatment failure was seen in 16 (47.1%) patients and the overall mortality was 32.4% (11 patients).
| Discussion | | |
Most reports state that rhino-orbito-cerebral mucormycosis is a rather uncommon disease. [1],[10],[17]. The unusually high incidence of ROC mucormycosis at our centre could be a reflection of poor diabetic control, poor socio-economic factors and the low level of patient education and awareness. Currently we do not have a proper explanation for the apparent seasonal predilection (June to September) of ROC mucormycosis. Diabetic patients with ROC mucormycosis have the best chance of survival, as the underlying metabolic derangement is most amenable to treatment.[1],[2],[5],[18] Patients with other immunocompromised states had a poor outcome. Patients with liver disease rarely develop mucormycosis. [3],[19] None of our patients had AIDS; the literature has only 12 reported cases of mucormycosis for all organs in AIDS patients. [20],[21],[22]
Intravenous amphotericin B, is the drug of choice for mucormycosis. In our series it could not be administered to four patients (all in Treatment group A), due to well-known adverse reactions.[23] These four patients received oral ketoconazole. Successful use of oral ketoconazole only is also reported [24]. Liposomal amphotericin B increases the efficacy of the drug facilitating prolonged administration for ROC mucormycosis, without side effects [25],[26]. Direct infiltration of the drug into the orbit helps in higher levels of drug reaching the affected areas.[10],[13],[14],[15] Treatment outcome is good when the disease is anatomically confined to the sinuses.[2] In this series the treatment success rate was 91% in stage I disease.
The argument for radical debridement of all affected tissue in a patient with mucormycosis, is based on the capacity of the fungus to spread along the walls and the lumen of blood vessels, leading to necrotising arteritis and ischaemic necrosis of the involved tissues. [7],[8],[9] This results in poor penetration of systemically administered drugs. However, there is evidence including ours that there exists a clinical group of patients who do well with conservative management.[2],[10],[11],[12],[13],[14],[15],[16] It would appear that addition of exenteration (TG-B) to the surgical plan was actually detrimental to patients in our series. But this was actually due to severity of disease. Stage II patients who received Treatment A had only moderate systemic disease that was rapidly stabilised and the orbital disease was not progressive.
On the other hand stage II patients who received Treatment B had rapidly progressive, severe orbital disease with proptosis, periorbital cellulitis and necrosis of the eyelid skin and the skin over the maxilla. The underlying metabolic derangement was severe, such as ketoacidosis, liver disease and idiopathic thrombocytopenic purpura.
All the patients with ROC mucormycosis stage III did not do well. All patients in this group at presentation had intracranial disease, which is associated with poor prognosis. A surgical clearance of all infected tissues including an exenteration was mandatory.
A rapidly corrected underlying metabolic derangement is the most important criterion for considering conservation of orbits. This is applicable even in the presence of total ophthalmoplegia and CRAO.[2] Conservative management can also be considered in patients with isolated extraocular muscle involvement, preserved vision and absence of progression. Infiltration of amphotericin B into the orbit and surrounding sinuses is benificial in these patients. In all cases, sinus and palatal disease debridement should be done wherever possible. This would help in reducing the load of infection in the sinuses and also obtain tissue for histopathological diagnosis. Exenteration should be prescribed in advanced involvement of orbit.
To conclude, the treatment of rhino-orbito-cerebral mucormycosis mandates a high index of suspicion in predisposed individuals. The management following a diagnostic biopsy includes rapid correction of the underlying metabolic and immunological derangements, intravenous amphotericin B and surgical clearance of all infected nasal and sinus tissue. The severity of predisposing factors, extent and aggressiveness of orbital disease at presentation, rate of progression and response to initial treatment should guide surgical management of the orbit. There is a definite role for the conservative management of the orbit in a select group of patients.
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[Figure - 1], [Figure - 2], [Figure - 3], [Figure - 4], [Figure - 5]
[Table - 1], [Table - 2], [Table - 3], [Table - 4]
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Zygomycetes and zygomycosis in the new era of antifungal therapies | [Zigomicetos y zigomicosis en la era de las nuevas terapias antifúngicas] |
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| Torres-Narbona, M., Guinea Ortega, J., Muńoz, P., Bouza, E. | | Revista Espanola de Quimioterapia. 2007; 20(4): 375-386 | | [Pubmed] | | | 30 |
Mucormycosis in patients with complicated cirrhosis |
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| Abbas, Z., Jafri, W., Rasool, S., Abid, S., Hameed, I. | | Singapore Medical Journal. 2007; 48(1): 69-73 | | [Pubmed] | | | 31 |
Rhinocerebral mucormycosis: The disease spectrum in 27 patients |
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| Mohindra, S., Mohindra, S., Gupta, R., Bakshi, J., Gupta, S.K. | | Mycoses. 2007; 50(4): 290-296 | | [Pubmed] | | | 32 |
Zygomycosis: an uncommon cause for peripheral facial palsy in diabetes |
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| Meas, T., Mouly, S., Kania, R., Hervé, D., Herman, P., Kévorkian, J.P., Virally, M., (...), Guillausseau, P.J. | | Diabetes and Metabolism. 2007; 33(3): 227-229 | | [Pubmed] | | | 33 |
Nosocomial fungal infections: Epidemiology, diagnosis, and treatment |
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| Perlroth, J., Choi, B., Spellberg, B. | | Medical Mycology. 2007; 45(4): 321-346 | | [Pubmed] | | | 34 |
Mucormycosis: An emerging disease? |
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| Bouza, E., Muñoz, P., Guinea, J. | | Clinical Microbiology and Infection. 2006; 12(Supp 7): 7-23 | | [Pubmed] | | | 35 |
Zygomycosis: The re-emerging fungal infection |
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| Chayakulkeeree, M., Ghannoum, M.A., Perfect, J.R. | | European Journal of Clinical Microbiology and Infectious Diseases. 2006; 25(4): 215-229 | | [Pubmed] | | | 36 |
Rhinocerebral mucormycosis in four diabetics | [La mucormycose rhinocérébrale chez le diabétique: À propos de quatre observations] |
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| Ferchichi, L., Chadli-Debbiche, A., Koubâa, W., Khayat, O., Labbène, N., Ben Gamra, O., Khedim, A., Ben Ayed, M. | | Journal des Maladies Vasculaires. 2006; 31(2): 85-87 | | [Pubmed] | | | 37 |
Prosthetic rehabilitation of face following naso-orbital mycosis |
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| Deshpande, S., Bhat, S., Sharma, R., Singh, S., Fernandes, J. | | Indian Journal of Plastic Surgery. 2006; 39(1): 73-75 | | [Pubmed] | | | 38 |
Fatal Rhino-Orbito-Cerebral Zygomycosis Caused by Apophysomyces elegans in a Healthy Patient |
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| Schütz, P., Behbehani, J.H., Khan, Z.U., Ahmad, S., Kazem, M.A., Dhar, R., Eskaf, W., (...), Cunningham Jr., L.L. | | Journal of Oral and Maxillofacial Surgery. 2006; 64(12): 1795-1802 | | [Pubmed] | | | 39 |
Novel perspectives on mucormycosis: Pathophysiology, presentation, and management |
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| Spellberg, B., Edwards Jr., J., Ibrahim, A. | | Clinical Microbiology Reviews. 2005; 18(3): 556-569 | | [Pubmed] | | | 40 |
Mucormycosis presenting with painful ophthalmoplegia |
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| Karakurum, B., Karatas, M., Cagici, A.C., Uncu, H., Yildirim, T., Hurcan, C., Karaca, S., (...), Tan, M. | | Acta Neurologica Belgica. 2005; 105(4): 201-205 | | [Pubmed] | | | 41 |
Mycoses of the head and neck | [Les mycoses ORL] |
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| Rousseau, A., Cornet, M., Carnot, F., Brasnu, D., Bruneval, P., Badoual, C. | | Annales de Pathologie. 2005; 25(2): 104-116 | | [Pubmed] | |
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