agnostic and therapeutic approach can lead to preservation of life and vision.

Ramin Monshizadeh, MD Colton, Calif Rebecca E. Sands, MD Wilfredo C. Lara, MD William Driebe, MD Gainesville, Fla

This study was sponsored in part by an unrestricted grant from Research to Pre- vent Blindness, Inc, New York, NY. Corresponding author: Ramin Monshizadeh, MD, Vitreoretinal Ser- vice, Inland Eye Institute, 1990 E Washington St, Colton, CA 92324 (e- mail: [email protected]).

1. McDonnell PJ, McDonnell JM, Brown RH, et al. Ocular involvement in patients with fungal in- Figure 2. Intraocular fungal invasion has been completely eradicated after vitrectomy, lensectomy, fections. Ophthalmology. 1985;92:706-709. capsulectomy, and partial iridectomy with intraocular and systemic antifungal therapy. 2. Clinch TE, Duker JS, Eagle RC, et al. Infantile endogenous Candida endophthalmitis present- ing as cataract. Surv Ophthalmol. 1989;34:107- 2,3 repeated lumbar puncture showed dida endophthalmitis. In our case, 112. resolution of pleocytosis. Following hematogenous spread of fungal ele- 3. Shah GK, Vander J, Eagle RC. Intralenticular Can- dida species abscess in a premature infant. Am 8 weeks of systemic amphotericin B ments into the ciliary body most likely J Ophthalmol. 2000;129:390-391. and 5-flucytosine, her visual acuity was followed by extension into the iris 4. Essman TF, Flynn HW, Smiddy WE, et al. Treat- improved to 20/50 OS (Figure 2). and body of the lens, resulting in in- ment outcome in a 10-year study of endoge- nous fungal endophthalmitis. Ophthalmic Surg Retrospective review of the tralenticular abscess formation. Lasers. 1997;28:185-194. medical records showed that 2 Mild cases of fungal chorioreti- months prior to the initial ophthal- nitis can be successfully treated with mic evaluation, the patient was treated systemic antifungal agents. Severe Bilateral Orbital Myeloid for C albicans urosepsis with 10 days endogenous fungal chorioretinitis of intravenous amphotericin B. At the with the presence of vitritis is most Sarcoma as Initial Sign of time, she remained afebrile, and re- often treated with pars plana vitrec- Acute Myeloid : peated blood, urine, and catheter cul- tomy and intravitreal injection of Case Report and Review tures obtained subsequently were all amphotericin B with systemic anti- of the Literature negative for organisms. The source of fungal medications.4 In cases where the intraocular seeding was thought fungal invasion of an avascular tis- Most pediatric orbital tumors are uni- to be the indwelling catheter that was sue such as the lens is suspected lateral, and little is mentioned in the placed around the time of the heart or proven, a thorough debulking, literature of the frequency and differ- transplantation. Because of the re- including lensectomy and capsulec- ential diagnosis of bilateral pediatric peated negative cultures, the cath- tomy, may play an important role. orbital tumors. Acute myeloid leuke- eter was presumed to be sterile and Intravitreal injection of anti- mia (AML) can involve the orbit as a was not removed until the time of vi- fungal medication provides thera- solid tumor termed myeloid sarcoma trectomy. peutic levels, which may not be or chloroma.1-3 We herein describe a achieved by systemic administra- child who was seen with bilateral or- Comment. Fungal intraocular in- tion alone.4 In our case, because of bital tumors that were the initial mani- fection often results from hematog- the extensive nature of the infec- festation of AML. A literature review enous seeding of highly vascular- tion and the presumedly higher vit- suggests that leukemia might be the ized structures, such as the choroid reous clearance rate in an aphakic most likely diagnosis in a child with or retina, and typically manifests as and vitrectomized eye, we elected to bilateral soft tissue orbital tumors, a creamy-white chorioretinal infil- repeat the intravitreal injection of point that has not been widely rec- trates with an associated vitritis.1,2 amphotericin B. ognized. The unusual manifestation of our Endogenous fungal endoph- case included an isolated progres- thalmitis may present a diagnostic Report of a Case. Painless, progres- sive iridocyclitis with a hypopyon challenge. Ocular signs and symp- sive proptosis of the left eye devel- that later advanced to iridolenticu- toms can be atypical, vague, and oped in a previously healthy boy lar abscess formation. slowly progressive. A high degree of aged 25 months during the course Lenticular abscess is a rare find- suspicion in susceptible patients of 2 weeks. Orbital magnetic reso- ing associated with endogenous Can- along with an aggressive surgical di- nance imaging (MRI) showed bilat-

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©2003 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 eral orbital tumors, and he was re- ferred to the Service at Wills Eye Hospital, Philadelphia, Pa, for diagnosis and management. Examination disclosed that the child could follow and fix on small objects with each eye and had nor- mal intraocular pressures. A 4-mm left proptosis was seen (Figure 1), and ductions and versions were nor- mal. An ill-defined orbital mass was palpable inferior to the left eye- brow. The remainder of his ocular examination, including ophthalmos- copy, showed normal findings. Or- bital computed tomography (CT) was performed. A review of the CT (Figure 2) Figure 1. Facial photograph shows proptosis of the left eye. and MRI (Figure 3) scans dis- closed a superior, irregular, homo- geneous tumor in each orbit. The left orbital mass measured 38ϫ24ϫ15 mm, and the right orbital mass mea- sured 27ϫ18ϫ11 mm. Both le- sions showed enhancement with contrast agents. There was no bone erosion or sinus or brain involve- ment. Based on the clinical findings and imaging study results, the dif- ferential diagnosis included leuke- mia, , metastatic neuro- blastoma, and idiopathic orbital inflammation (inflammatory pseudotumor). The initial periph- eral blood cell count revealed an el- evated count of 26.9ϫ103/µL, with a differential count of 3% segmented neutro- phils, 56% lymphocytes, 17% mono- Figure 2. Coronal computed tomographic scan of the orbits shows bilateral superior orbital masses. The cytes, 6% promyelocytes, and 18% mass on the left eye is larger and more clearly seen. blast cells, which was strongly sug- gestive of leukemia. No or thrombocytopenia was found. Se- rum chemistry studies disclosed a markedly elevated lactate dehydro- genase level of 1143 U/L. A confirmatory left orbital bi- opsy was performed through an eye- lid-crease incision. Diagnostic fro- zen sections obtained at the time of the orbital showed poorly dif- ferentiated malignant round cells. The differential diagnosis included leukemia, lymphoma, and, less likely, rhabdomyosarcoma or neu- roblastoma. Given this differential diagnosis, tissue was saved for and possible electron mi- croscopy in addition to routine his- topathologic study. Review of the Figure 3. Coronal magnetic resonance scan of the orbits in a T1-weighted image with enhancement permanent sections showed a dif- shows diffuse masses along the roof of each orbit.

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©2003 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 definition, however, final subtyping of AML must be performed by study- ing the . The patient subsequently un- derwent a diagnostic bone marrow as- piration and biopsy that showed re- placement of the normal bone marrow with blasts and cells with ma- turing monocytic features. Auer rods were not seen. Flow cytometry find- ings were positive for the monocytic markers CD14, CD33, CD4, and CD15. A diagnostic lumbar punc- ture showed no evidence of central nervous system involvement. On the basis of these findings, a final diag- nosis of M5b AML was made. The patient was treated under Figure 4. Photomicrograph of the orbital biopsy specimen shows proliferation of poorly differentiated the current protocol of the Chil- cells with irregular nuclear contours, typical of monoblasts (hematoxylin-eosin, original magnification ϫ250). dren’s Oncology Group for newly di- agnosed AML, which consists of 2 cycles of highly intensive chemo- therapy, followed by an allogeneic bone marrow transplantation if a suit- able donor can be found. The first round of was started and consisted of idarubicin hydro- chloride, vidarabine, etoposide phos- phate, thioguanine, dexamethasone, daunorubicin hydrochloride, and in- trathecal vidarabine for central ner- vous system prophylaxis. The patient was found to be in remission by results of bone mar- row aspiration performed 6 weeks after initiation of chemotherapy. He then underwent a second round of chemotherapy, which consisted of fludarabine phosphate, idarubicin, Figure 5. Photomicrograph shows Leder stain positive for chloroacetate (specific) esterase, a marker of and vidarabine. Results of a second granulocytic differentiation. Less than 20% of cells show positive findings; most cells show positive bone marrow aspiration after the findings for monocytic markers, consistent with an M5 subtype of acute (Leder stain, original magnification ϫ250). second round of chemotherapy showed that the patient remained in remission. An orbital MRI ob- fuse proliferation of poorly differ- Sudan black B, which are indicators tained 10 weeks after diagnosis dem- entiated blast cells with somewhat ofgranulocyticdifferentiation.Results onstrated resolution of the bilateral irregular nuclear contours and of immunohistochemical stains were orbital masses seen at diagnosis. The prominent nucleoli. Occasional cells strongly positive for lysozyme and patient’s sister was found to be a 6/6 demonstrated finely granular eo- CD68, further indicating monocytic antigen match, which made her a sinophilic cytoplasm (Figure 4). differentiation.Theywerenegativefor suitable donor, and the patient un- Numerous mitoses were evident. terminaldeoxynucleotidyltransferase, derwent an allogeneic bone mar- Flow cytometry showed a blast which is present in lymphoblastic leu- row transplant 13 weeks after diag- populationwithamyeloidphenotype, kemia and lymphoblastic lymphoma. nosis. At present, he is undergoing includinggreaterthan90%ofcellsthat Approximately 20% of the cells were close follow-up as an outpatient. expressed CD11c and CD56 and 66% positive for Leder (chloroacetate or of cells that expressed CD13. Enzyme specific esterase) stain in paraffin sec- Comment. It is well known that cytochemistry on cytospin prepara- tions (Figure 5), indicating granu- AML can be seen initially with or- tions showed the blasts to be diffusely locytic differentiation. The immuno- bital involvement, before the diag- and strongly positive for ␣-naphthyl phenotypeandtheotherdescribedfea- nosis of the underlying leuke- acetate esterase, an indicator of mono- turesofthebiopsyspecimenweremost mia.3-31 Soft tissue accumulations of cytic differentiation. The preparations consistent with AML of the poorly dif- leukemic cells were previously re- werenegativeformyeloperoxidaseand ferentiated monocytic type (M5a). By ferred to as granulocytic sarcoma or

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©2003 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 chloroma.7-31 As several variants of AML by definition have few or no Laterality Among Some Reported Cases of Orbital Myeloid Sarcoma in Children cells of granulocytic lineage, the and Young Adults With Myeloid Leukemia* broader term myeloid sarcoma is cur- No. of Proptosis the rently preferred. The term chlo- Source Patients Unilateral Bilateral First Sign roma “green tumor” is derived from Wright† (1938) 1 0 1 1/1 the greenish gross coloration of this Chatterjee and Sen7 (1960) 1 1 0 1/1 lesion, attributable to the myeloper- Mortada8 (1963) 2 0 2 2/2 oxidase in the cells of granulocytic Consul et al9 (1967) 1 0 1 1/1 lineage, which are present in vary- Jha and Lamba31 (1971) 2 1 1 1/2 ing proportions according to sub- Seal and Gupta10 (1973) 2 2 0 2/2 Zimmerman and Font1 (1975) 33 ‡ ‡ 29/33 type. Myeloid sarcomas are most 11 common in certain subtypes of AML, Michelson et al (1975) 1 0 1 1/1 Brownstein et al12 (1975) 1 1 0 1/1 in particular M5a (monoblastic), Cavdar et al13 (1978) 20 11 9 17/20 M5b (monocytic), M4 (myelomono- Baijal et al14 (1979) 1 0 1 1/1 cytic), and M2 (myeloblastic with Rajantie et al15 (1984) 1 0 1 1/1 maturation).32 Davis et al16 (1985) 1 1 0 1/1 The French-American-British Singh et al17 (1985) 4 0 4 4/4 18 Cooperative Group defines this sub- Cohen et al (1988) 1 0 1 1/1 Jordan et al19 (1991) 1 1 0 1/1 type of AML, which is also referred Kalmanti et al20 (1991) 2 1 1 1/2 to as , as Shome et al21 (1992) 7 2 5 0/7 having a bone marrow biopsy speci- Sundareshan et al22 (1992) 1 0 1 ‡ men showing 80% or more of the Bulas et al23 (1995) 1 0 1 1/1 nonerythroid cells demonstrating Tanigawa et al24 (1998) 1 1 0 1/1 25 monocytic lineage (therefore, less Puri and Grover (1999) 1 1 0 1/1 Gujral et al26 (1999) 32 13 19 31/32 than 20% are of granulocytic lineage). Uyesugi et al27 (2000) 1 0 1 1/1 In addition, fewer than 80% of the Lakhkar et al28 (2000) 1 0 1 1/1 monocytic lineage cells must be Olson et al29 (2000) 1 0 1 1/1 monoblasts (ie, maturing promono- Present report (2002) 1 0 1 1/1 cytes are clearly evident). When 80% Total No. (%) of Cases 89 36 (40) 53 (60) 104/121(86) or more of the cells are monoblasts, the lesion is classified as acute mono- *The large series of 33 cases reported by Zimmerman and Font1 is not included in the tabulation of 33,34 laterality here, because it was a histopathologic series of slides and tissue submitted to the Armed Forces blastic leukemia (M5a). Institute of Pathology and, in most cases, insufficient data were submitted to determine laterality. In that Inmostinstances,orbitalmyeloid series, only 4 of the 33 cases were listed as having bilateral proptosis. However, the number of bilateral sarcoma occurs in young children. It cases in that series would probably have been much higher had complete histories and imaging study results been available (Lorenz E. Zimmerman, MD, oral communication, December 23, 2001). is rare among the orbital tumors of †Quoted by Consul et al.9 childhood,accountingforonly1of250 ‡Information was unclear from article review. cases in a previous report from our de- partment.5 Thediseaseisrelativelyun- tic nerve glioma, usually affect only a relatively uncommon pediatric or- common in the western hemisphere, a single orbit. Rhabdomyosarcoma, bital tumor, it becomes a major diag- but is more prevalent in the Middle the most common malignant orbital nostic consideration in the setting of East, Asia, and Africa.1 Most of the tumor of childhood, is invariably uni- bilateral orbital involvement. Pub- larger reported series have come from lateral.2-6 lished reports on orbital myeloid sar- Turkey13 and India.21,26 The main conditions that can coma have not always provided com- When evaluating an orbital mass cause bilateral orbital masses in chil- plete details with regard to initial in a child, the ophthalmologist must dren are idiopathic nongranuloma- features and laterality. However, on consider a variety of benign and ma- tous orbital inflammation,35 meta- the basis of a review of the available lignantconditions,particularlyinflam- static neuroblastoma,36 and myeloid literature, we calculated that about matory, cystic, and vascular lesions sarcoma. Pediatric idiopathic non- 88% of cases with proptosis that are such as idiopathic orbital inflamma- granulomatous orbital inflamma- seen by the ophthalmologist have no tion, dermoid cyst, capillary heman- tion is initially unilateral in 10% of history of leukemia at the time of pre- gioma, lymphangioma, and others.4-6 cases, but it can eventually show bi- sentation (Table). In addition, we es- About 90% to 95% of orbital masses lateral involvement in 46%.35 How- timate that about 60% of orbital my- ofchildhoodthatcometobiopsyprove ever, involvement of the second eye eloid sarcomas are bilateral. tobebenignonhistopathologicexami- is usually sequential and not simul- Orbital involvement by acute nation.5 Of the 5% to 10% that are ma- taneous. Orbital metastasis is the ini- myeloid sarcoma is relatively rare lignant, rhabdomyosarcoma is the tial sign of abdominal neuroblas- among orbital tumors and pseudo- most common disease.5,6 toma in 3% to 4% of patients and is tumors. However, in the setting of Most childhood orbital tumors bilateral in 50%.36,37 simultaneous bilateral orbital tu- are unilateral.1-5 Most benign condi- Our patient had bilateral or- mors in children, myeloid sarcoma tions, like dermoid cyst, capillary he- bital involvement by myeloid sar- appears to be a highly likely, if not mangioma, lymphangioma, and op- coma. Although myeloid sarcoma is the most likely, diagnostic possibil-

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©2003 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 ity. Any child with an orbital mass 4. Bullock JD, Goldberg SH, Rakes SM. Orbital tu- acute nonlymphocytic leukemia. Cancer. 1992; mors in children. Ophthal Plast Reconstr Surg. 70:2298-2301. of uncertain origin, particularly if it 1989;5:13-16. 22. Sundareshan TS, Augustus M, Yasha TC, is bilateral, should undergo prompt 5. Shields JA, Bakewell B, Augsburger JJ, Donoso Shailaja SN, Lalitha N. Variant complex trans- evaluation for underlying AML. LA, Bernardino V. Space-occupying orbital location 5 (8;15;21) in acute myeloblastic leu- masses in children: a review of 250 consecu- kemia (M2) associated with bilateral chlo- tive . Ophthalmology. 1986;93:379- roma. Cancer Genet Cytogenet. 1992;64:35-37. Jerry A. Shields, MD 384. 23. Bulas RB, Laine FJ, Das Narla L. Bilateral or- 6. Shields CL, Shields JA, Honavar SG, Demirci bital granulocytic sarcoma (chloroma) preced- Gary A. Stopyra, MD H. The clinical spectrum of primary ophthal- ing the blast phase of acute myelogenous leu- Brian P. Marr, MD mic rhabdomyosarcoma. Ophthalmology. 2001; kemia: CT findings. Pediatr Radiol. 1995;25: Carol L. Shields, MD 108:2284-2292. 488-489. 7. Chatterjee BM, Sen NN. Acute myeloid leukae- 24. Tanigawa M, Tsuda Y, Amemiya T, et al. Orbital Philadephia, Pa mia with leukaemic deposit in the orbit. Br tumor in associated Wilbur Pan, MD, PhD J Ophthalmol. 1960;44:440-442. with karyotype 46,XX,t (8;21)(q22;q22): a 8. Mortada A. Orbital lymphoblastomas and acute case report. Ophthalmologica. 1998;212:202- New Brunswick, NJ in children. Am J Ophthalmol. 1963; 205. 55:327-331. 25. Puri P, Grover AK. Granulocytic sarcoma of or- Ralph C. Eagle, Jr, MD 9. Consul BN, Kulshrestha OP, Mehrotra AS. Bi- bit preceding acute myeloid leukaemia: a case Philadelphia lateral proptosis in acute myeloid leukemia. Br report. Eur J Cancer Care. 1999;8:113-115. J Ophthalmol. 1967;51:65-67. 26. Gujral S, Bhattarai S, Mohan A, et al. Ocular Jay Bernstein, MD 10. Seal GN, Gupta AK. Orbital deposit in acute my- extramedullary myeloid cell tumour in chil- Westfield, NJ eloid leukaemia. Indian J Ophthalmol. 1973;21: dren: an Indian study. J Trop Pediatr. 1999;45: 73-77. 112-115. 11. Michelson JB, Shields JA, Leonard BC, Caputo 27. Uyesugi WY, Wagtabe J, Petermann G. Or- Submitted for publication April 11, AR, Bergman GE. Periorbital chloroma and prop- bital and facial granulocytic sarcoma (chlo- tosis in a two-year-old with acute myelog- roma): a case report. Pediatr Radiol. 2000;30: 2002; final revision received August enous leukemia. J Pediatr Ophthalmol Strabis- 276-278. 5, 2002; accepted August 16, 2002. mus. 1975;12:255-258. 28. Lakhkar BN, Banavali S, Philip P. Orbital granu- This study was supported by the 12. Brownstein S, Thelmo W, Olivier A. Granulo- locytic sarcoma in acute myelogenous leuke- cytic sarcoma of the orbit. Can J Ophthalmol. mia. Indian J Pediatr. 2000;67:234-235. Eye Tumor Research Foundation, 1975;10:174-183. 29. Olson JL, May MJ, Stork L, Kadan N, Bateman Philadelphia, Pa (Drs J. A. and C. L. 13. Cavdar AO, Arcasoy A, Babacan E, Gozdaso- JB. Acute megakaryoblastic leukemia in Down glu S, Topuz U, Fraumeni JF. Ocular granulo- syndrome: orbital infiltration. Am J Ophthal- Shields); the Award of Merit in Retina cytic sarcoma (chloroma) with acute myelo- mol. 2000;130:128-130. Research, Houston, Tex (Dr J. A. monocytic leukemia in Turkish children. 30. Stockl FA, Dolmetsch AM, Saornil MA, Font Shields); the Macula Foundation, New Cancer. 1978;41:1606-1609. RL, Burnier MN Jr. Orbital granulocytic sar- 14. Baijal GC, Agarwal ML, Gawande C, Gupta DC. coma. Br J Ophthalmol. 1997;81:1084-1088. York, NY (Dr C. L. Shields); and the Leukaemic deposits in the orbit. Indian J Oph- 31. Jha BK, Lamba PA. Proptosis as a manifesta- Noel T. and Sara L. Simmonds En- thalmol. 1979;26:53-55. tion of acute myeloid leukaemia. Br J Ophthal- dowment for Ophthalmic Pathology, 15. Rajantie J, Tarkkanen A, Rapola J, Merenmies mol. 1971;55:844-847. L, Perkkio M, Siimes MA. Orbital granulo- 32. Byrd JC, Edenfield J, Shields DJ, et al. Extra- Wills Eye Hospital (Dr Eagle). cytic sarcoma as a presenting sign in acute my- medullary myeloid cell tumors in acute non- Corresponding author and re- elogenous leukemia. Ophthalmologica. 1984; lymphocytic leukemia: a clinical review. J Clin 189:158-161. Oncol. 1995;13:1800-1816. prints: Jerry A. Shields, MD, Oncol- 16. Davis JL, Parke DW II, Font RL. Granulocytic 33. Bennett JM, Catavsky D, Daniel MT, et al. Pro- ogy Service, Wills Eye Hospital, 840 sarcoma of the orbit: a clinicopathologic study. posed criteria for the classification of acute my- Walnut St, Philadelphia, PA 19107. Ophthalmology. 1985;92:1758-1762. eloid leukemia: a report of the French- 17. Singh T, Jayaram G, Gupta AK. Cytologic di- American-British Cooperative Group. Ann Intern agnosis of myeloid sarcoma. Am J Ophthalmol. Med. 1985;103:460-462. 1. Zimmerman LE, Font RL. Ophthalmologic 1985;99:496-497. 34. Siernick PH, Serpick AA. Granulocytic sar- manifestations of granulocytic sarcoma (my- 18. Cohen R, Segall HD, Nelson MD Jr, Zee CS, Ah- coma (chloroma). Blood. 1970;35:361-369. eloid sarcoma or chloroma): the third Pan madi J. Bilateral retroorbital chloromas in a 16- 35. Mottow LS, Jakobiec FA. Idiopathic inflamma- American Association of Ophthalmology and month-old child: CT features. J Comput Assist tory orbital pseudotumors in childhood, I: clini- American Journal of Ophthalmology Lecture. Tomogr. 1988;12:895-896. cal characteristics. Arch Ophthalmol. 1978;96: Am J Ophthalmol. 1975;80:975-990. 19. Jordan DR, Noel LP, Carpenter BF. Chlo- 1410-1417. 2. White VA, Rootman J. Orbital pathology: leu- roma. Arch Ophthalmol. 1991;109:734-735. 36. Albert DM, Rubenstein RA, Scheie HG. Tu- kemia. In: Albert DM, Jakobiec FA, eds. Prin- 20. Kalmanti M, Anagnostou D, Liarikos S, et al. mor metastases to the eye, II: clinical studies ciples and Practice of Ophthalmology. Philadel- Ocular granulocytic sarcoma in childhood acute in infants and children. Am J Ophthalmol. 1967; phia, Pa: WB Saunders Co; 1994:2323. myelogenous leukemia. Acta Paediatr Jpn. 1991; 63:727-732. 3. Shields JA, Shields CL. Lymphoid tumors and 33:172-176. 37. Musarella M, Chan HSL, DeBoer G, Gallie BL. leukemias. In: Atlas of Orbital Tumors. Phila- 21. Shome DK, Gupta NK, Prajapati NC, Krishnam Ocular involvement in neuroblastoma: prog- delphia, Pa: Lippincott Williams & Wilkins; Raju GM, Choudhury P, Dubey AP. Orbital nostic implications. Ophthalmology. 1984;91: 1999:316-340. granulocytic sarcomas (myeloid sarcomas) in 936-940.

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