Advertisement

Contact lens-related polymicrobial keratitis: Acanthamoeba spp. genotype T4 and Candida albicans

  • Maria Luiza Carneiro Buchele
  • Débora Borgert Wopereis
  • Fabiana Casara
  • Jefferson Peres de Macedo
  • Marilise Brittes Rott
  • Fabíola Branco Filippin Monteiro
  • Maria Luiza Bazzo
  • Fernando dos Reis Spada
  • Jairo Ivo dos Santos
  • Karin Silva Caumo
Original Paper

Abstract

A 31-year-old female daily user of contact lenses sought medical attention, reporting blurred vision and irritation of the left eye. Slit-lamp examination revealed hyperemia and an irregular corneal epithelium surface, and empirical treatment was started. A corneal scrape was obtained and examined for the presence of fungi, bacteria, and Acanthamoeba spp. The results of the microbial culture revealed growth of Acanthamoeba spp. and Candida albicans. The Acanthamoeba isolate was characterized by cyst morphology as belonging to group II according to Pussard and Pons. Sequencing of the diagnostic fragment 3 (DF3) region located on the 18S ribosomal DNA identified the isolate as genotype T4. The patient was treated with chlorhexidine 0.02% and polyhexamethylene biguanide (PHMB) 0.02% drops for 5 months until the infection resolved. Lately, rare cases of polymicrobial keratitis associated with Acanthamoeba and Candida albicans have been reported. Cases of co-infection are more difficult to treat, since the specific treatment depends on precise identification of the agents involved.

Keywords

Infectious keratitis Acanthamoeba spp. Candida albicans Contact lenses 

Notes

Acknowledgments

The authors thank the Clinical analysis Department of the Federal University of Santa Catarina, Brazil, and Dr. Janet W. Reid who revised the English text.

Funding information

This study received financial support from CAPES and CNPq.

Compliance with ethical standards

We obtained approval for this study from the Committee for Human Research at the University of Santa Catarina, Florianópolis (CAAE No. 32938014.5.0000.0121).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aitken D, Hay J, Kinnear FB, Kirkness CM, Lee WR, Seal DV (1996) Amebic keratitis in a wearer of disposable contact lenses due to a mixed Vahlkampfia and Hartmannella infection. Ophthalmology 103:485–494CrossRefPubMedGoogle Scholar
  2. Alipour F, Khaheshi S, Soleimanzadeh M, Heidarzadeh S, Heydarzadeh S (2017) Contact lens-related complications: a review. J Ophthalmic Vis Res 12:193–204.  https://doi.org/10.4103/jovr.jovr_159_16 PubMedPubMedCentralGoogle Scholar
  3. Balczun C, Scheid PL (2017) Free-living amoebae as hosts for and vectors of intracellular microorganisms with public health significance. Viruses 9.  https://doi.org/10.3390/v9040065
  4. Booton GC, Visvesvara GS, Byers TJ, Kelly DJ, Fuerst PA (2005) Identification and distribution of Acanthamoeba species genotypes associated with nonkeratitis infections. J Clin Microbiol 43:1689–1693.  https://doi.org/10.1128/JCM.43.4.1689-1693.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cariello AJ, Passos RM, Yu MCZ, Hofling-Lima AL (2011) Microbial keratitis at a referral center in Brazil. Int Ophthalmol 31:197–204.  https://doi.org/10.1007/s10792-011-9441-0 CrossRefPubMedGoogle Scholar
  6. Carnt N, Stapleton F (2016) Strategies for the prevention of contact lens-related Acanthamoeba keratitis: a review. Ophthalmic Physiol Opt 36:77–92.  https://doi.org/10.1111/opo.12271 CrossRefPubMedGoogle Scholar
  7. Carrijo-Carvalho LC, Sant'ana VP, Foronda AS, de Freitas D, de Souza Carvalho FR (2017) Therapeutic agents and biocides for ocular infections by free-living amoebae of Acanthamoeba genus. Surv Ophthalmol 62:203–218.  https://doi.org/10.1016/j.survophthal.2016.10.009 CrossRefPubMedGoogle Scholar
  8. Cope JR, Collier SA, Rao MM, Chalmers R, Mitchell GL, Richdale K, Wagner H, Kinoshita BT, Lam DY, Sorbara L, Zimmerman A, Yoder JS, Beach MJ (2015) Contact lens wearer demographics and risk behaviors for contact lens-related eye infections--United States, 2014. MMWR Morb Mortal Wkly Rep 64:865–870CrossRefPubMedPubMedCentralGoogle Scholar
  9. Corsaro D, Walochnik J, Köhsler M, Rott MB (2015) Acanthamoeba misidentification and multiple labels: redefining genotypes T16, T19, and T20 and proposal for Acanthamoeba Micheli sp. nov. (genotype T19). Parasitol Res 14:2481–2490.  https://doi.org/10.1007/s00436-015-4445-8 CrossRefGoogle Scholar
  10. Corsaro D, Köhsler M, Montalbano di Filippo M, Venditti D, Monno R, di Cave D, Berrilli F, Walochnik J (2017) Update on Acanthamoeba Jacobsi genotype T15, including full-length 18s RDNA molecular phylogeny. Parasitol Res 116:1273–1284.  https://doi.org/10.1007/s00436-017-5406-1 CrossRefPubMedGoogle Scholar
  11. Dudley R, Matin A, Alsam S, Sissons J, Maghsood AH, Khan NA (2005) Acanthamoeba isolates belonging to T1, T2, T3, T4 but not T7 encyst in response to increased osmolarity and cysts do not bind to human corneal epithelial cells. Acta Trop 95:100–108.  https://doi.org/10.1016/j.actatropica.2005.05.004 CrossRefPubMedGoogle Scholar
  12. Fernandes M et al (2015) Comparison betweenpolymicrobial and fungal keratitis: clinical features, risk factors, and outcome. Am J Ophthalmol 160: 873-881.e2. doi: https://doi.org/10.1016/j.ajo.2015.07.028
  13. Gomes Tdos S et al (2016) Acanthamoeba spp. in contact lenses from healthy individuals from Madrid, Spain. PLoS One 11:e0154246.  https://doi.org/10.1371/journal.pone.0154246 CrossRefPubMedGoogle Scholar
  14. Karsten E, Watson SL, Foster LJ (2012) Diversity of microbial species implicated in keratitis: a review. In Open Ophthalmol J 6: 110-24. NetherlandsGoogle Scholar
  15. Lakhundi S, Siddiqui R, Khan NA (2017) Pathogenesis of microbial keratitis. Microb Pathog 104:97–109.  https://doi.org/10.1016/j.micpath.2016.12.013 CrossRefPubMedGoogle Scholar
  16. Lim NC, Lim DK, Ray M (2013) Polymicrobial versus monomicrobial keratitis: a retrospective comparative study. Eye Contact Lens 39:348–354.  https://doi.org/10.1097/ICL.0b013e3182a3024e CrossRefPubMedGoogle Scholar
  17. Lin HC, Hsiao CH, Ma DHK, Yeh LK, Tan HY, Lin MY, Huang SCM (2009) Medical treatment for combined fusarium and Acanthamoeba keratitis. Acta Ophthalmol 87:199–203.  https://doi.org/10.1111/j.1755-3768.2008.01192.x CrossRefPubMedGoogle Scholar
  18. Loh AR, Hong K, Lee S, Mannis M, Acharya NR (2009) Practice patterns in the management of fungal corneal ulcers. Cornea 28:856–859.  https://doi.org/10.1097/ICO.0b013e318199fa77 CrossRefPubMedGoogle Scholar
  19. Lorenzo-Morales J, Martínez-Carretero E, Batista N, Álvarez-Marín J, Bahaya Y, Walochnik J, Valladares B (2007) Early diagnosis of amoebic keratitis due to a mixed infection with Acanthamoeba and Hartmannella. Parasitol Res 102:167–169.  https://doi.org/10.1007/s00436-007-0754-x CrossRefPubMedGoogle Scholar
  20. Lorenzo-Morales J, Khan NA, Walochnik J (2015) An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. In Parasite 22:10CrossRefGoogle Scholar
  21. Maciver SK, Asif M, Simmen MW, Lorenzo-Morales J (2013) A systematic analysis of Acanthamoeba genotype frequency correlated with source and pathogenicity: T4 is confirmed as a pathogen-rich genotype. Eur J Protistol 49:217–221.  https://doi.org/10.1016/j.ejop.2012.11.004 CrossRefPubMedGoogle Scholar
  22. Maghsood AH et al (2005) Acanthamoeba genotype T4 from the UK and Iran and isolation of the T2 genotype from clinical isolates. J Med Microbiol 54:755–759.  https://doi.org/10.1099/jmm.0.45970-0 CrossRefPubMedGoogle Scholar
  23. Marciano-Cabral F, Cabral G (2003) Acanthamoeba spp. As agents of disease in humans. Clin Microbiol Rev 16:273–307.  https://doi.org/10.1128/CMR.16.2.273-307.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  24. McLaughlin-Borlace L, Stapleton F, Matheson M, Dart JK (1998) Bacterial biofilm on contact lenses and lens storage cases in wearers with microbial keratitis. J Appl Microbiol 84:827–838CrossRefPubMedGoogle Scholar
  25. Michel R, Walochnik J, Scheid P (2014) Article for the “free-living amoebae special issue”: isolation and characterisation of various amoebophagous fungi and evaluation of their prey spectrum. Exp Parasitol 145:S131–S136.  https://doi.org/10.1016/j.exppara.2014.10.005 CrossRefPubMedGoogle Scholar
  26. Nielsen SE, Nielsen E, Julian HO, Lindegaard J, Højgaard K, Ivarsen A, Hjortdal J, Heegaard S (2015) Incidence and clinical characteristics of fungal keratitis in a Danish population from 2000 to 2013. Acta Ophthalmol 93:54–58.  https://doi.org/10.1111/aos.12440 CrossRefPubMedGoogle Scholar
  27. Nunes TE et al (2016) Acanthamoeba and fusarium interactions: a possible problem in keratitis. Acta Trop 157:102–107.  https://doi.org/10.1016/j.actatropica.2016.02.001 CrossRefPubMedGoogle Scholar
  28. Page FC (1988) A new key to freshwater and soil gymnamoebae: with instructions for culture. Freshwater Biological Association, AmblesideGoogle Scholar
  29. Pussard M, Pons R (1977) Morphologie de la paroi kystiqueet taxonomie du genre Acanthamoeba (Protozoa, Amoebida). Protistologica 8:557–598Google Scholar
  30. Raqqad NA, Fgara NA (2015) Management of Acanthamoeba and Candida Keratitis in a young female: our experience at Princess Haya Military Hospital. Int J Keratoconus Ectatic Corneal Dis 4:120–122Google Scholar
  31. Said DG et al (2011) The challenge of fungal keratitis. In Br J Ophthalmol 95: 1623-4. EnglandGoogle Scholar
  32. Scheid P (2016) A strange endocytobiont revealed as largest virus. Curr Opin Microbiol 31:58–62.  https://doi.org/10.1016/j.mib.2016.02.005 CrossRefPubMedGoogle Scholar
  33. Scheid PL, Schwarzenberger R (2011) Free-living amoebae as vectors of cryptosporidia. Parasitol Res 109:499–504.  https://doi.org/10.1007/s00436-011-2287-6 CrossRefPubMedGoogle Scholar
  34. Scheid P, Hauröder B, Michel R (2010) Investigations of an extraordinary endocytobiont in Acanthamoeba sp.: development and replication. Parasitol Res 106:1371–1377.  https://doi.org/10.1007/s00436-010-1811-4 CrossRefPubMedGoogle Scholar
  35. Scheid P, Balczun C, Schaub GA (2014) Some secrets are revealed: parasitic keratitis amoebae as vectors of the scarcely described pandoraviruses to humans. Parasitol Res 113:3759–3764.  https://doi.org/10.1007/s00436-014-4041-3 CrossRefPubMedGoogle Scholar
  36. Schroeder JM, Booton GC, Hay J, Niszl IA, Seal DV, Markus MB, Fuerst PA, Byers TJ (2001) Use of subgenic 18s ribosomal DNA PCR and sequencing for genus and genotype identification of Acanthamoebae from humans with keratitis and from sewage sludge. J Clin Microbiol 39:1903–1911.  https://doi.org/10.1128/JCM.39.5.1903-1911.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sengupta J, Khetan A, Saha S, Banerjee D, Gangopadhyay N, Pal D (2012) Candida keratitis: emerging problem in India. Cornea 31:371–375.  https://doi.org/10.1097/ICO.0b013e31823f8a71 CrossRefPubMedGoogle Scholar
  38. Siddiqui R, Khan NA (2012a) Biology and pathogenesis of Acanthamoeba. Parasit Vectors 5:6.  https://doi.org/10.1186/1756-3305-5-6 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Siddiqui R, Khan NA (2012b) War of the microbial worlds: who is the beneficiary in Acanthamoeba-bacterial interactions? Exp Parasitol 130:311–313.  https://doi.org/10.1016/j.exppara.2012.01.021 CrossRefPubMedGoogle Scholar
  40. Stapleton F, Carnt N (2012) Contact lens-related microbial keratitis: how have epidemiology and genetics helped us with pathogenesis and prophylaxis. Eye (Lond) 26:185–193.  https://doi.org/10.1038/eye.2011.288 CrossRefGoogle Scholar
  41. Thomas PA (2003) Fungal infections of the cornea. Eye (Lond) 17:852–862.  https://doi.org/10.1038/sj.eye.6700557 CrossRefGoogle Scholar
  42. Tice AK, Shadwick LL, Fiore-Donno AM, Geisen S, Kang S, Schuler GA, Spiegel FW, Wilkinson KA, Bonkowski M, Dumack K, Lahr DJG, Voelcker E, Clauß S, Zhang J, Brown MW (2016) Expansion of the molecular and morphological diversity of Acanthamoebidae (Centramoebida, Amoebozoa) and identification of a novel life cycle type within the group. Biol Direct 11:69.  https://doi.org/10.1186/s13062-016-0171-0 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Vieira A, Ramesh A, Seddon AM, Karlyshev AV (2017) CmeABC multidrug efflux pump contributes to antibiotic resistance and promotes campylobacter Jejuni survival and multiplication in Acanthamoeba polyphaga. Appl Environ Microbiol 83(Sep 15).  https://doi.org/10.1128/aem.01600-17
  44. Visvesvara GS (2013) Infections with free-living amebae. Handb Clin Neurol 114:153–168.  https://doi.org/10.1016/b978-0-444-53490-3.00010-8 CrossRefPubMedGoogle Scholar
  45. Visvesvara GS, Moura H, Schuster FL (2007) Pathogenic and opportunistic free-living amoebae: Acanthamoeba Spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol Med Microbiol 50:1–26.  https://doi.org/10.1111/j.1574-695X.2007.00232.x CrossRefPubMedGoogle Scholar
  46. Walochnik J, Scheikl U, Haller-Schober EM (2015) Twenty years of acanthamoeba diagnostics in Austria. J Eukaryot Microbiol 62:3–11.  https://doi.org/10.1111/jeu.12149 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Maria Luiza Carneiro Buchele
    • 1
  • Débora Borgert Wopereis
    • 1
  • Fabiana Casara
    • 1
  • Jefferson Peres de Macedo
    • 1
  • Marilise Brittes Rott
    • 2
  • Fabíola Branco Filippin Monteiro
    • 1
  • Maria Luiza Bazzo
    • 3
  • Fernando dos Reis Spada
    • 4
  • Jairo Ivo dos Santos
    • 5
  • Karin Silva Caumo
    • 1
  1. 1.Centro de Ciências da Saúde, Departamento de Análises Clínicas, Laboratório de Estudos de Protozoários Emergentes e OportunistasUniversidade Federal de Santa Catarina (UFSC)FlorianópolisBrazil
  2. 2.Instituto de Ciências Básicas da Saúde, Departamento de Microbiologia, Imunologia e ParasitologiaUniversidade Federal do Rio Grande do Sul (UFRGS)Porto AlegreBrazil
  3. 3.Centro de Ciências da Saúde, Departamento de Análises Clínicas, Laboratório de Biologia Molecular, Sorologia e MicobactériasUniversidade Federal de Santa Catarina (UFSC)FlorianópolisBrazil
  4. 4.Hospital Regional de São José - Homero de Miranda Gomes, Setor de oftalmologiaFlorianópolisBrazil
  5. 5.Centro de Ciências da Saúde, Departamento de Análises Clínicas, Laboratório de Micologia ClínicaUniversidade Federal de Santa Catarina (UFSC)FlorianópolisBrazil

Personalised recommendations