Skip to main content

Advertisement

SpringerLink
Log in

Vermamoeba vermiformis as etiological agent of a painful ulcer close to the eye

  • Protozoology - Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In the present article, we report on the identification of Vermamoeba (Hartmannella) vermiformis as the etiological agent of a tissue infection close to the eye of a female patient. Laboratory examination revealed no involvement of any pathogenic bacteria or fungi in the tissue infection. V. vermiformis was identified by cultivation and morphology of trophozoites and cysts as well as phylogenetic analysis of nuclear 18S rDNA. The lesion improved in the course of 4 weeks by application of zinc paste.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Abedkhojasteh H, Niyyati M, Rahimi F, Heidari M, Farnia S, Rezaeian M (2013) First report of Hartmannella keratitis in a cosmetic soft contact lens wearer in Iran. Iran J Parasitol 8:481–485

    PubMed  PubMed Central  Google Scholar 

  • Adl SM, Bass D, Lane CE et al (2019) Revision to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Micobiol 66:4–119

    Article  Google Scholar 

  • Aitken D, Hay J, Kinnear F, Kirkness C, Lee W, Seal D (1996) Amebic keratitis in a wearer of disposable contact lenses due to a mixed Vahlkampfia and Hartmannella infection. Ophthalmology 103:485–494

    Article  CAS  PubMed  Google Scholar 

  • Altschul S, Madden T, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  PubMed Central  Google Scholar 

  • Balczun C, Scheid PL (2016) Detection of Balamuthia mandrillaris DNA in the storage case of contact lenses in Germany. Parasitol Res 115:2111–2114

    Article  PubMed  Google Scholar 

  • Balczun C, Scheid P (2017) Free-living amoebae as hosts for and vectors of intracellular microorganisms with public health significance. Viruses 9:E65

    Article  PubMed Central  Google Scholar 

  • Bouchoucha I, Aziz A, Hoffart L, Drancourt M (2016) Repertoire of free-living protozoa in contact lens solutions. BMC Ophthalmol 16:191

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brieland JK, Fantone JC, Remick DG, LeGendre M, McClain M, Engleberg NC (1997) The role of Legionella pneumophila - infected Hartmannella vermiformis as an infectious particle in a murine model of Legionaires’ disease. Infect Immun 65:5330–5333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabello-Vílchez A, Mena R, Zuñiga J, Cermeño P, Martín-Navarro C, González A, López-Arencibia A, Reyes-BatlleM PJE, Valladares B, Lorenzo-Morales J (2014) Endosymbiotic Mycobacterium chelonae in a Vermamoeba vermiformis strain isolated from the nasal mucosa of an HIV patient in Lima, Peru. Exp Parasitol 145(Suppl):S127–S130

    Article  PubMed  CAS  Google Scholar 

  • Cateau E, Delafont V, Hechard Y, Rodier MH (2014) Free-living amoebae: what part do they play in healthcare-associated infections? J Hosp Infect 87:131–140

    Article  CAS  PubMed  Google Scholar 

  • De Jonckheere JF, Brown S (1998a) There is no evidence that the free-living ameba Hartmannella is a human parasite. Clin Infect Dis 26:773

    Article  PubMed  Google Scholar 

  • De Jonckheere JF, Brown S (1998b) Is the free-living ameba Hartmannella causing keratitis? Clin Infect Dis 27:1337–1338

    PubMed  Google Scholar 

  • De Jonckheere J, Brown S (1999) Non-Acanthamoeba amoebic keratitis. Cornea 18:499–501

    Article  PubMed  Google Scholar 

  • Delafont V, Rodier M-H, Maisonneuve E, Cateau E (2018) Vermamoeba vermiformis: a free-living amoeba of interest. Microb Ecol 76:991–1001

    Article  PubMed  Google Scholar 

  • Dykova I, Pindova Z, Fiala I, Dvorakova H, Machackova B (2005) Fish-isolated strains of Hartmannella vermiformis Page, 1967: morphology, phylogeny and molecular diagnosis of the species in tissue lesions. Folia Parasitol 52:295–303

    Article  CAS  Google Scholar 

  • Fields B, Nerad T, Sawyer T, King CH, Barbaree JM, Martin WT, Morrill WE, Sanden GN (1990) Characterization of an axenic strain of Hartmannella vermiformis obtained from an investigation of nosocomial legionellosis. J Protozool 37:581–583

    Article  CAS  PubMed  Google Scholar 

  • Fouque E, Héchard Y, Hartemann P, Humeau P, Trouilhé M (2015) Sensitivity of Vermamoeba (Hartmannella) vermiformis cysts to conventional disinfectants and protease. J Water Health 13:302–310

    Article  PubMed  Google Scholar 

  • Garcia A, Goñi P, Cieloszyk J, Fernandez M, Calvo-Beguería L, Rubio E, Fillat M, Peleato M, Clavel A (2013) Identification of free-living amoebae and amoeba-associated bacteria from reservoirs and water treatment plants by molecular techniques. Environ Sci Technol 47:3132–3140

    Article  CAS  PubMed  Google Scholar 

  • Gast R, Fuerst PA, Byers TJ (1994) Discovery of group I introns in the nuclear small subunit ribosomal genes of Acanthamoeba. Nucl Acids Res 22:592–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray TB, Cursons RT, Sherwan JF, Rose PR (1995) Acanthamoeba, bacterial, and fungal contamination of contact lens storage cases. Brit J Ophthalmol 79:601–605

    Article  CAS  Google Scholar 

  • Hsu B, Lin C, Shih F (2009) Survey of pathogenic free-living amoebae and Legionella spp. in mud spring recreation area. Water Res 43:2817–2828

    Article  CAS  PubMed  Google Scholar 

  • Inoue T, Asari S, Tahara K, Hayashi K, Kiritoshi A, Shimomura Y (1998) Acanthamoeba keratitis with symbiosis of Hartmannella ameba. Am J Ophthalmol 125:721–723

    Article  CAS  PubMed  Google Scholar 

  • Kennedy SM, Devine P, Hurley C, Ooi YS, Collum LMT (1995) Corneal infection associated with Hartmannella vermiformis in contact-lens wearer. Lancet 346:637–638

    Article  CAS  PubMed  Google Scholar 

  • Kinnear FB (2001) Non-Acanthamoeba amoebic keratitis. J Inf 42:218–219

    Article  CAS  Google Scholar 

  • Kinnear FB (2003) Cytopathogenicity of Acanthamoeba, Vahlkampfia and Hartmannella: quantative and qualitative in vitro studies on keratocytes. J Inf 46:228–237

    Article  CAS  Google Scholar 

  • Kuiper M, Wullings B, Akkermans A, Beumer RR, van der Kooij D (2004) Intracellular proliferation of Legionella pneumophila in Hartmannella vermiformis in aquatic biofilms grown on plasticized polyvinyl chloride. Appl Environ Microbiol 70:6826–6833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorenzo-Morales J, Martínez-Carretero E, Batista N, Àlvarez-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

    Article  PubMed  Google Scholar 

  • Masangkay F, Milanez G, Karanis P, Nissapatorn V (2018) Vermamoeba vermiformis—global trend and future perspective. In: Reference module in earth systems and environmental sciences. https://doi.org/10.1016/b978-0-12-409548-9.11005-x

    Chapter  Google Scholar 

  • Muchesa P, Leifels M, Jurzik L, Hoorzok K, Barnard T, Bartie C (2017) Coexistence of free-living amoebae and bacteria in selected South African hospital water distribution systems. Parasitol Res 116:155–165

    Article  CAS  PubMed  Google Scholar 

  • Murga R, Forster T, Brown E, Pruckler JM, Fields BS, Donlan RM (2001) Role of biofilms in the survival of Legionella pneumophila in a model potable-water system. Microbiol Read Engl 147:3121–3126

    Article  CAS  Google Scholar 

  • Nicholas K, Nicholas H, Deerfield D (1997) GeneDoc: analysis and visualization of genetic variation. Embnew News 4:14

    Google Scholar 

  • Page FC (1988) A new key to freshwater and soil Gymnamoebae with instructions for culture. Freshwater Biological Association, Ambleside, UK

    Google Scholar 

  • Page FC (1991) Nackte Rhizopoda. In: Page FC, Siemensma FJ (eds) Nackte Rhizopoda und Heliozoa, Protozoenfauna Band 2. Gustav Fischer Verlag, Stuttgart, New York, pp 7–170

    Google Scholar 

  • Qvarnstrom Y, Visvesvara G, Sriram R, da Silva A (2006) Multiplex real-time PCR assay for simultaneous detection of Acanthamoeba spp., Balamuthia mandrillaris, and Naegleria fowleri. J Clin Microbiol 44:3589–3595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rohr U, Weber S, Michel R, Selenka F, Wilhelm M (1998) Comparison of free-living amoebae in hot water systems of hospitals with isolates from moisty sanitary areas by identifying genera and determining temperature tolerance. Appl Environ Microbiol 64:1822–1824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheid P (2014) Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms. Parasitol Res 113:2407–2414

    Article  PubMed  Google Scholar 

  • Scheid P (2018) Free-living amoebae and their multiple impacts on environmental health. In: Encyclopedia of environmental health, 2nd Edtion. https://doi.org/10.1016/B978-0-12-409548-9.10969-8

    Chapter  Google Scholar 

  • Smirnov AV, Chao E, Nassonova ES, Cavalier-Smith T (2011) A revised classification of naked lobose amoebae (Amoebozoa: Lobosa). Protist 162:545–570

    Article  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas V, Loret JF, Jousset M, Greub G (2008) Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. Environ Microbiol 10:2728–2745

    Article  CAS  PubMed  Google Scholar 

  • Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D (1997) The CLUSTAL_ X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 15:4876–4882

    Article  Google Scholar 

  • Tsvetkova N, Schild M, Panaiotov K-MR, Gottstein B, Walochnik J, Aspöck H, Lucas MS, Müller N (2004) The identification of free-living environmental isolates of amoebae from Bulgaria. Parasitol Res 92:405–413

    Article  PubMed  Google Scholar 

  • Tyson J, Pearce M, Vargas P, Bagchi S, Mulhern B, Cianciotto N (2013) Multiple Legionella pneumophila type II secretion substrates, including a novel protein, contribute to differential infection of the amoebae Acanthamoeba castellanii, Hartmannella vermiformis, and Naegleria lovaniensis. Infect Immun 81:1399–1410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valster R, Wullings B, Bakker G, Smidt H, van der Kooij D (2009) Free-living protozoa in two unchlorinated drinking water supplies, identified by phylogenic analysis of 18S rRNA gene sequences. Appl Environ Microbiol 75:4736–4746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wadowsky RM, Butler LJ, Cook MK, Verma SM, Paul MA, Fields BS, Keleti G, Sykora JL, Yee RB (1988) Growth-supporting activity for Legionella pneumophila in tap water cultures and implication of hartmannellid amoebae as growth factors. Appl Environ Microbiol 54:2677–2682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walochnik J, Scheikl U, Haller-Schober EM (2014) Twenty years of Acanthamoeba diagnostics in Austria. J Eukaryot Microbiol 62:3–11

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang H, Edwards M, Falkinham J, Pruden A (2012) Molecular survey of the occurrence of Legionella spp., Mycobacterium spp., Pseudomonas aeruginosa, and amoeba hosts in two chloraminated drinking water distribution systems. Appl Environ Microbiol 78:6285–6294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The author would like to thank Dr. David Lam (MD, MPH, Shaman Medical Consulting) for review and English language editing of the article and S. Njul for the technical assistance.

Author information

Authors and Affiliations

  1. Laboratory of Medical Parasitology, Department XXI (Med. Microbiology), Central Military Hospital Koblenz, Koblenz, Germany

    Patrick L. Scheid & Carsten Balczun

  2. Institute of Integrated Sciences; Department of Biology, University of Koblenz-Landau, Koblenz, Germany

    Patrick L. Scheid & Ulrich Sinsch

  3. Institute for Hygiene and Microbiology, University of Wuerzburg, Wuerzburg, Germany

    Thiên-Trí Lâm

Authors
  1. Patrick L. Scheid
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thiên-Trí Lâm
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ulrich Sinsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carsten Balczun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carsten Balczun.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Section Editor: Panagiotis Karanis

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Scheid, P.L., Lâm, TT., Sinsch, U. et al. Vermamoeba vermiformis as etiological agent of a painful ulcer close to the eye. Parasitol Res 118, 1999–2004 (2019). https://doi.org/10.1007/s00436-019-06312-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-019-06312-y

Keywords

Search

Navigation