Int Ophthalmol (2014) 34:1285–1289 DOI 10.1007/s10792-014-9999-4
CASE REPORT
Apophysomyces elegans: a novel cause of endogenous endophthalmitis in an immunocompetent individual Vivek Pravin Dave • Savitri Sharma Rohit Yogi • Swapna Reddy
•
Received: 15 June 2014 / Accepted: 27 August 2014 / Published online: 3 September 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract A 20-year-old male presented with sudden onset redness, pain, and decreased vision in his left eye. Best-corrected visual acuity in the left eye was noted to be perception of light positive with inaccurate projection. On clinical examination, he was diagnosed to have left eye endogenous endophthalmitis. Smear and culture of vitreous biopsy were positive for Apophysomyces elegans, a fungus known to cause extensive soft tissue infections systemically characteristically in immunocompetent individual. The patient was treated aggressively with topical, systemic, and intravitreal antifungals but had a poor visual and anatomical outcome. This is a first known report of endogenous endophthalmitis due to Apophysomyces elegans. Keywords Endogenous endophthalmitis Apophysomyces elegans Immunocompetent Outcome Slide culture
V. P. Dave (&) R. Yogi Smt. Kanuri Santhamma Center for Vitreo Retinal Diseases, LV Prasad Eye Institute, Hyderabad, India e-mail: [email protected] S. Sharma Jhaveri Microbiology Center, Brian Holden Eye Research Center, LV Prasad Eye Institute, Hyderabad, India S. Reddy Jhaveri Microbiology Center, LV Prasad Eye Institute, Hyderabad, India
Introduction Endogenous (metastatic) endophthalmitis occurs due to blood borne dissemination of microorganisms to the inner coats of the eye and the vitreous cavity [1]. It is an uncommon entity accounting for only 8 % of all cases of endophthalmitis [2, 3]. Most cases are associated with underlying morbid systemic condition like multi organ failure, immunocompromised state, malignancies, in-dwelling catheters, and intravenous drug abuse [4]. The commonest organisms in endogenous endophthalmitis worldwide are fungi, especially Candida albicans [5]. Other common organisms are Aspergillus species. Apophysomyces elegans is an infrequent cause of zygomycosis worldwide. Though periorbital infections are known, there is no known case report of intraocular infection by Apophysomyces elegans. We report a case of Apophysomyces elegans endogenous endophthalmitis in a young healthy male with a poor outcome in spite of aggressive treatment.
Case report A 20-year-old male presented to us with complaints of sudden onset diminution of vision in the left eye (OS) since a week. Decrease in vision was associated with ocular pain, redness, and watering. There were no associated systemic complaints or any complaints in the right eye (OD). There was a history of trauma to the left hand in a road traffic accident 3 years back for
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Fig. 1 Preoperative B scan ultrasound showing moderate intensity echoes in the vitreous cavity with an attached retina at first visit
which a laceration repair was done locally. The patient gave a history of the skin wound being treated with an antiseptic wash, local ointment application, and oral tablets; however, the details were not available. No microbiological examination was done. The presenting best-corrected visual acuity (BCVA) in OD was 20/20 and in OS was perception of light positive with inaccurate projection. On local examination, OD was unremarkable. OS showed circum ciliary congestion, 2 mm hypopyon, and exudates in the pupillary area causing occlusio pupillae. Neovascularization of the iris was noted at 9 o clock. Ultrasound B scan (Fig. 1) of OS showed low amplitude echoes all over the vitreous cavity with apparently attached retina and mildly thickened choroid. Based on these findings, a provisional diagnosis of OS endogenous endophthalmitis was made. An internist opinion was sought to rule out a systemic immunocompromised state or focal infection. Complete blood picture, blood culture, urine culture, and HIV-ELISA done were within normal limits. The patient was advised OS pars plana vitrectomy with lensectomy with intravitreal injection of vancomycin 1 mg/0.1 ml and ceftazidime 2.25 lgm/ 0.1 ml, and a vitreous biopsy was immediately sent to the in house microbiology laboratory for smears and cultures.
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The microbiological processing of the vitreous sample included direct microscopy and culture. Smears were examined after staining with 0.1 % calcofluor white (CFW), Gram and Gomori methenamine silver stains, and the media included for culture were 5 % sheep blood agar, chocolate agar, thioglycollate broth, brain heart infusion broth, Sabouraud dextrose agar (SDA), and potato dextrose agar (PDA). All media were incubated aerobically at 37 °C except SDA and PDA, which were incubated at 27 °C for 2 weeks. Chocolate agar was incubated in 5 % CO2 at 37 °C. All smears showed broad, sparsely septate, ribbon like, hyaline fungal filaments (Fig. 2a–c). White, cottony fungal colonies grew on blood agar, chocolate agar, and brain heart infusion broth after 48 h and on PDA after 8 days (Figs. 2, 3). No sporulation was seen in lactophenol cotton blue mount of the colony even after 2 weeks. Slide culture on PDA for 2 weeks ultimately showed the characteristic spores of Apophysomyces elegans (Fig. 3). Post primary surgery based on smear results, the patient was started on topical Amphotericin B eye drops one hour along with oral Itraconazole 200 mg two times per day, and intravitreal injection of Amphotericin B 5 lgm/0.1 ml was given the next day. A recurrence of exudates was noted in the anterior
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Fig. 2 a Faintly stained, broad, sparsely septate hyaline fungal filaments in the vitreous sample (Gram stain, 91,000) b Black, broad, ribbon like, aseptate fungal filaments (Gomori Methenamine Silver stain, 9400) c Broad, ribbon like, sparsely septate,
fluorescent fungal filaments (Calcofluor white stain, 9400) d Confluent cottony white fungal growth on potato dextrose agar (after 4 days at 27 °C)
chamber and the vitreous cavity after 2 days for which repeat intravitreal injection of Amphotericin B 5 lgm/ 0.1 ml was given twice at an interval of 3 days. Vision in OS remained perception of light positive with inaccurate projection of rays. Postoperative B scan ultrasound showed persistent moderate intensity echoes all throughout the vitreous cavity. The patient underwent repeat vitrectomy and anterior segment wash a week after primary surgery with repeat injection Amphotericin B 5 lgm/0.1 ml intravitreally. The retina visualized during surgery was highly ischemic with multifocal areas of retinal necrosis and disk pallor. At the final visit at one and a half months, the vision in OS was perception of light present with inaccurate projection of light. The globe was hypotonous with intraocular pressure of 4 mm Hg with B scan ultrasound showing vitreous cavity full of echoes and thickened choroid and a funnel retinal detachment. The iris showed 360° neovascularization. As the patient was comfortable, further treatment was discontinued, and the extremely poor visual prognosis with risk of phthisis bulbi was explained.
Discussion Endogenous endophthalmitis is a diagnostic and a therapeutic challenge. Though fungi are the commonest micro organisms to cause endogenous endophthalmitis, Apophysomyces elegans infection till date is unknown. A. elegans is a rare fungus of family Mucoraceae, class Zygomycetes, and order Mucorales [6]. It was first identified from soil samples in India [7]. The first human infection was noted in 1985 [8] in a diabetic lady due to a fall and a traumatic open wound on the lower extremity. Though most fungi of the class Zygomycetes and order Mucorales cause infection in an immunocompromised setting, A. elegans in contrast is known to cause soft tissue and skin infections following trauma in an otherwise healthy patient. Cutaneous damage with subsequent soil contamination is a classical feature of A. elegans infection. A. elegans also causes vascular invasion leading to thrombosis and local tissue necrosis. The patient reported here had a history of a road traffic accident with an open wound on his forearm, which most
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Fig. 3 a Blood agar and b Chocolate agar showing white cottony fungal growth after 4 days of incubation at 37 °C. c Slide culture showing characteristic unbranched sporangiophores, pyriform sporangia with distinct vase-shaped
apophyses, hemispherical collumellae and cylindrical sporangiospores of A. elegans (lactophenol cotton blue stain, 9400). d Rhizoids are seen away from the point of origin of the sporangiophores (lactophenol cotton blue stain, 9200)
likely would have got contaminated with soil (Fig. 4). However, it is difficult to explain the long gap between the infection and endopthalmitis. A. elegans infection has been described as a rhino orbital mucormycosis with poor outcome due to extensive tissue necrosis [9, 10]. In our case, in spite of a quick microbiological diagnosis and aggressive medical and surgical management, there was a poor visual and anatomical outcome possibly due to extensive vascular necrosis occurring in the retina and the ciliary body by the time the patient presented to our clinic. To the best of our knowledge, this is the first case report of intraocular infection of A. elegans presenting as endogenous endophthalmitis. A. elegans should be considered as a possible etiology in cases of endogenous endophthalmitis in otherwise healthy individuals who
Fig. 4 Old sutured lacerated, healed wound on the forearm and back of the hand
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have a past history of an open wound contaminated by soil. Financial disclosures None of the authors have any financial disclosures to make.
References 1. Wong JS, Chan TK, Lee HM, Chee SP (2000) Endogenous bacterial endophthalmitis: an East Asian experience and a reappraisal of a severe ocular affliction. Ophthalmology 107:1483–1491 2. Shrader SK, Band JD, Lauter CB, Murphy P (1990) The clinical spectrum of endophthalmitis: incidence, predisposing factors, and features influencing outcome. J Infect Dis 162:115–120 3. Chee SP, Jap A (2001) Endogenous endophthalmitis. Curr Opin Ophthalmol 12:464–470
1289 4. Okada AA, Johnson RP, Liles WC, D’Amico DJ, Baker AS (1994) Endogenous bacterial endophthalmitis. Report of a ten-year retrospective study. Ophthalmology 101:832–838 5. Binder MI, Chua J, Kaiser PK (2003) Endogenous endophthalmitis: an 18-year review of culture positive cases at a tertiary care centre. Medicine 82:97–105 6. Kwon-Chung KJ, Bennett JE (1992) Mucormycosis. In: Cann C (ed) Medical Mycology. Lea & Febiger, Philadelphia, pp 524–559 7. Misra PC, Srivastava KJ, Lata K (1979) Apophysomyces, a new genus of the Mucorales. Mycotaxon 8:377–382 8. Wieden MA, Steinbronn KK, Padhye AA, Ajello L, Chandler FW (1985) Zygomycosis caused by Apophysomyces elegans. J Clin Microbiol 22:522–526 9. Liang KP, Tleyjeh MI, Wilson WR, Roberts GD, Temesgen Z (2006) Rhino-orbitocerebral mucormycosis caused by apophysomyces elegans. J Clin Microbiol 44:892–898 10. Schutz P, Behbehani J, Khan Z, Ahmad S, Kazem M, Dhar R et al (2006) Fatal rhino-orbito-cerebral zygomycosis caused by apophysomyces elegans in a healthy patient. J Oral Maxillofac Surg 64:1795–1802
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CASE REPORT
Apophysomyces elegans: a novel cause of endogenous endophthalmitis in an immunocompetent individual Vivek Pravin Dave • Savitri Sharma Rohit Yogi • Swapna Reddy
•
Received: 15 June 2014 / Accepted: 27 August 2014 / Published online: 3 September 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract A 20-year-old male presented with sudden onset redness, pain, and decreased vision in his left eye. Best-corrected visual acuity in the left eye was noted to be perception of light positive with inaccurate projection. On clinical examination, he was diagnosed to have left eye endogenous endophthalmitis. Smear and culture of vitreous biopsy were positive for Apophysomyces elegans, a fungus known to cause extensive soft tissue infections systemically characteristically in immunocompetent individual. The patient was treated aggressively with topical, systemic, and intravitreal antifungals but had a poor visual and anatomical outcome. This is a first known report of endogenous endophthalmitis due to Apophysomyces elegans. Keywords Endogenous endophthalmitis Apophysomyces elegans Immunocompetent Outcome Slide culture
V. P. Dave (&) R. Yogi Smt. Kanuri Santhamma Center for Vitreo Retinal Diseases, LV Prasad Eye Institute, Hyderabad, India e-mail: [email protected] S. Sharma Jhaveri Microbiology Center, Brian Holden Eye Research Center, LV Prasad Eye Institute, Hyderabad, India S. Reddy Jhaveri Microbiology Center, LV Prasad Eye Institute, Hyderabad, India
Introduction Endogenous (metastatic) endophthalmitis occurs due to blood borne dissemination of microorganisms to the inner coats of the eye and the vitreous cavity [1]. It is an uncommon entity accounting for only 8 % of all cases of endophthalmitis [2, 3]. Most cases are associated with underlying morbid systemic condition like multi organ failure, immunocompromised state, malignancies, in-dwelling catheters, and intravenous drug abuse [4]. The commonest organisms in endogenous endophthalmitis worldwide are fungi, especially Candida albicans [5]. Other common organisms are Aspergillus species. Apophysomyces elegans is an infrequent cause of zygomycosis worldwide. Though periorbital infections are known, there is no known case report of intraocular infection by Apophysomyces elegans. We report a case of Apophysomyces elegans endogenous endophthalmitis in a young healthy male with a poor outcome in spite of aggressive treatment.
Case report A 20-year-old male presented to us with complaints of sudden onset diminution of vision in the left eye (OS) since a week. Decrease in vision was associated with ocular pain, redness, and watering. There were no associated systemic complaints or any complaints in the right eye (OD). There was a history of trauma to the left hand in a road traffic accident 3 years back for
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Int Ophthalmol (2014) 34:1285–1289
Fig. 1 Preoperative B scan ultrasound showing moderate intensity echoes in the vitreous cavity with an attached retina at first visit
which a laceration repair was done locally. The patient gave a history of the skin wound being treated with an antiseptic wash, local ointment application, and oral tablets; however, the details were not available. No microbiological examination was done. The presenting best-corrected visual acuity (BCVA) in OD was 20/20 and in OS was perception of light positive with inaccurate projection. On local examination, OD was unremarkable. OS showed circum ciliary congestion, 2 mm hypopyon, and exudates in the pupillary area causing occlusio pupillae. Neovascularization of the iris was noted at 9 o clock. Ultrasound B scan (Fig. 1) of OS showed low amplitude echoes all over the vitreous cavity with apparently attached retina and mildly thickened choroid. Based on these findings, a provisional diagnosis of OS endogenous endophthalmitis was made. An internist opinion was sought to rule out a systemic immunocompromised state or focal infection. Complete blood picture, blood culture, urine culture, and HIV-ELISA done were within normal limits. The patient was advised OS pars plana vitrectomy with lensectomy with intravitreal injection of vancomycin 1 mg/0.1 ml and ceftazidime 2.25 lgm/ 0.1 ml, and a vitreous biopsy was immediately sent to the in house microbiology laboratory for smears and cultures.
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The microbiological processing of the vitreous sample included direct microscopy and culture. Smears were examined after staining with 0.1 % calcofluor white (CFW), Gram and Gomori methenamine silver stains, and the media included for culture were 5 % sheep blood agar, chocolate agar, thioglycollate broth, brain heart infusion broth, Sabouraud dextrose agar (SDA), and potato dextrose agar (PDA). All media were incubated aerobically at 37 °C except SDA and PDA, which were incubated at 27 °C for 2 weeks. Chocolate agar was incubated in 5 % CO2 at 37 °C. All smears showed broad, sparsely septate, ribbon like, hyaline fungal filaments (Fig. 2a–c). White, cottony fungal colonies grew on blood agar, chocolate agar, and brain heart infusion broth after 48 h and on PDA after 8 days (Figs. 2, 3). No sporulation was seen in lactophenol cotton blue mount of the colony even after 2 weeks. Slide culture on PDA for 2 weeks ultimately showed the characteristic spores of Apophysomyces elegans (Fig. 3). Post primary surgery based on smear results, the patient was started on topical Amphotericin B eye drops one hour along with oral Itraconazole 200 mg two times per day, and intravitreal injection of Amphotericin B 5 lgm/0.1 ml was given the next day. A recurrence of exudates was noted in the anterior
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Fig. 2 a Faintly stained, broad, sparsely septate hyaline fungal filaments in the vitreous sample (Gram stain, 91,000) b Black, broad, ribbon like, aseptate fungal filaments (Gomori Methenamine Silver stain, 9400) c Broad, ribbon like, sparsely septate,
fluorescent fungal filaments (Calcofluor white stain, 9400) d Confluent cottony white fungal growth on potato dextrose agar (after 4 days at 27 °C)
chamber and the vitreous cavity after 2 days for which repeat intravitreal injection of Amphotericin B 5 lgm/ 0.1 ml was given twice at an interval of 3 days. Vision in OS remained perception of light positive with inaccurate projection of rays. Postoperative B scan ultrasound showed persistent moderate intensity echoes all throughout the vitreous cavity. The patient underwent repeat vitrectomy and anterior segment wash a week after primary surgery with repeat injection Amphotericin B 5 lgm/0.1 ml intravitreally. The retina visualized during surgery was highly ischemic with multifocal areas of retinal necrosis and disk pallor. At the final visit at one and a half months, the vision in OS was perception of light present with inaccurate projection of light. The globe was hypotonous with intraocular pressure of 4 mm Hg with B scan ultrasound showing vitreous cavity full of echoes and thickened choroid and a funnel retinal detachment. The iris showed 360° neovascularization. As the patient was comfortable, further treatment was discontinued, and the extremely poor visual prognosis with risk of phthisis bulbi was explained.
Discussion Endogenous endophthalmitis is a diagnostic and a therapeutic challenge. Though fungi are the commonest micro organisms to cause endogenous endophthalmitis, Apophysomyces elegans infection till date is unknown. A. elegans is a rare fungus of family Mucoraceae, class Zygomycetes, and order Mucorales [6]. It was first identified from soil samples in India [7]. The first human infection was noted in 1985 [8] in a diabetic lady due to a fall and a traumatic open wound on the lower extremity. Though most fungi of the class Zygomycetes and order Mucorales cause infection in an immunocompromised setting, A. elegans in contrast is known to cause soft tissue and skin infections following trauma in an otherwise healthy patient. Cutaneous damage with subsequent soil contamination is a classical feature of A. elegans infection. A. elegans also causes vascular invasion leading to thrombosis and local tissue necrosis. The patient reported here had a history of a road traffic accident with an open wound on his forearm, which most
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Fig. 3 a Blood agar and b Chocolate agar showing white cottony fungal growth after 4 days of incubation at 37 °C. c Slide culture showing characteristic unbranched sporangiophores, pyriform sporangia with distinct vase-shaped
apophyses, hemispherical collumellae and cylindrical sporangiospores of A. elegans (lactophenol cotton blue stain, 9400). d Rhizoids are seen away from the point of origin of the sporangiophores (lactophenol cotton blue stain, 9200)
likely would have got contaminated with soil (Fig. 4). However, it is difficult to explain the long gap between the infection and endopthalmitis. A. elegans infection has been described as a rhino orbital mucormycosis with poor outcome due to extensive tissue necrosis [9, 10]. In our case, in spite of a quick microbiological diagnosis and aggressive medical and surgical management, there was a poor visual and anatomical outcome possibly due to extensive vascular necrosis occurring in the retina and the ciliary body by the time the patient presented to our clinic. To the best of our knowledge, this is the first case report of intraocular infection of A. elegans presenting as endogenous endophthalmitis. A. elegans should be considered as a possible etiology in cases of endogenous endophthalmitis in otherwise healthy individuals who
Fig. 4 Old sutured lacerated, healed wound on the forearm and back of the hand
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Int Ophthalmol (2014) 34:1285–1289
have a past history of an open wound contaminated by soil. Financial disclosures None of the authors have any financial disclosures to make.
References 1. Wong JS, Chan TK, Lee HM, Chee SP (2000) Endogenous bacterial endophthalmitis: an East Asian experience and a reappraisal of a severe ocular affliction. Ophthalmology 107:1483–1491 2. Shrader SK, Band JD, Lauter CB, Murphy P (1990) The clinical spectrum of endophthalmitis: incidence, predisposing factors, and features influencing outcome. J Infect Dis 162:115–120 3. Chee SP, Jap A (2001) Endogenous endophthalmitis. Curr Opin Ophthalmol 12:464–470
1289 4. Okada AA, Johnson RP, Liles WC, D’Amico DJ, Baker AS (1994) Endogenous bacterial endophthalmitis. Report of a ten-year retrospective study. Ophthalmology 101:832–838 5. Binder MI, Chua J, Kaiser PK (2003) Endogenous endophthalmitis: an 18-year review of culture positive cases at a tertiary care centre. Medicine 82:97–105 6. Kwon-Chung KJ, Bennett JE (1992) Mucormycosis. In: Cann C (ed) Medical Mycology. Lea & Febiger, Philadelphia, pp 524–559 7. Misra PC, Srivastava KJ, Lata K (1979) Apophysomyces, a new genus of the Mucorales. Mycotaxon 8:377–382 8. Wieden MA, Steinbronn KK, Padhye AA, Ajello L, Chandler FW (1985) Zygomycosis caused by Apophysomyces elegans. J Clin Microbiol 22:522–526 9. Liang KP, Tleyjeh MI, Wilson WR, Roberts GD, Temesgen Z (2006) Rhino-orbitocerebral mucormycosis caused by apophysomyces elegans. J Clin Microbiol 44:892–898 10. Schutz P, Behbehani J, Khan Z, Ahmad S, Kazem M, Dhar R et al (2006) Fatal rhino-orbito-cerebral zygomycosis caused by apophysomyces elegans in a healthy patient. J Oral Maxillofac Surg 64:1795–1802
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