Skip to main content

Advertisement

SpringerLink
Log in

Survey of Naegleria and its resisting bacteria-Legionella in hot spring water of Taiwan using molecular method

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Naegleria is a free-living amoebae existing in soil and aquatic environments. Within the genus Naegleria, N. fowleri is most recognized as potential human pathogen causing primary amoebic meningoencephalitis (PAM). Furthermore, the Naegleria spp. can serve as vehicles for facultative pathogens, such as Legionella. In this study, we identified Naegleria and Legionella based on the PCR amplification with a genus-specific primer pair and investigated the distribution of Naegleria and Legionella at five spring recreation areas in Taiwan. In this study of hot spring and other water sources in Taiwan, five Naegleria spp. were detected in 15 (14.2%) of the water samples. The most frequently detected was N. lovaniensis (n = 6), followed by N. australiensis (n = 5), and then N. clarki (n = 2). N. americana and N. pagei were detected once, respectively. The pathogenic species N. fowleri was not detected; however, N. australiensis considered to be a potential pathogen species in humans was found. Legionella spp., an endosymbiont of Naegleria, was detected in 19 (17.9%) of the water samples in this study. Overall, 5.7% of the water samples contained both Naegleria and Legionella. The Legionella spp. identified were L. pneumophila and L. erythra. Results of this survey confirm the existence of Naegleria and Legionella in Taiwan spring recreation areas. It should be considered a potential threat for health associated with human activities in spring recreation areas of Taiwan.

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.

Fig. 1

Similar content being viewed by others

References

  • APHA (1995) Standard method for the examination of water and wastewater, 15th edn. APHA, WEF and AWWA, Washington

    Google Scholar 

  • Apley J, Clarke SK, Roome AP, Sandry SA, Saygi G, Silk B, Warhurst DC (1970) Primary amoebic meningoencephalitis in Britain. Br Med J 1:596–599

    Article  CAS  PubMed  Google Scholar 

  • Brown TJ, Cursons RT, Keys EA, Marks M, Miles DM (1983) The occurrence and distribution of pathogenic free-living amoebae in thermal areas of the North Island of New Zealand. NZ J Mar Freshw Res 17:59–69

    Article  Google Scholar 

  • CDC (2008) Primary amebic meningoencephalitis—Arizona, Florida, and Texas (2007). Morb Mortal Wkly Rep 57(21):573–577

    Google Scholar 

  • Cerva L, Novak K, Culbertson CG (1968) An outbreak of amoebic meningoencephalitis. Am J Epidemiol 88:436–444

    CAS  PubMed  Google Scholar 

  • Chang CW, Kao CH, Liu YF (2009) Heterogeneity in chlorine susceptibility for Legionella pneumophila released from Acanthamoeba and Hartmannella. J Appl Microbiol 106:97–105

    Article  CAS  PubMed  Google Scholar 

  • Chou SA (2004) The study on the investigation, exploitation and utilization of hot-spring resources in Taiwan (IV) (In Chinese). Taiwan Water Resource Agency, Ministry of Economic Affairs, Taipei

    Google Scholar 

  • De Jonckheere JF (2002) A century of research on the Amoeboflagellate Genus Naegleria. Acta Protozool 41:309–342

    Google Scholar 

  • De Jonckheere JF (2004) Molecular definition and the ubiquity of species in the genus Naegleria. Protist 155:89–103

    Article  PubMed  Google Scholar 

  • Declerck P, Behets J, Delaedt Y, Margineanu A, Lammertyn E, Ollevier F (2005) Impact of non-Legionella bacteria on the uptake and intracellular replication of Legionella pneumophila in Acanthamoeba castellanii and Naegleria lovaniensis. Microb Ecol 50:536–549

    Article  CAS  PubMed  Google Scholar 

  • Declerck P, Behets J, van Hoef V, Ollevier F (2007) Replication of Legionella pneumophila in floating biofilms. Curr Microbiol 55:435–440

    Article  CAS  PubMed  Google Scholar 

  • Donlan RM, Forster T, Murga R, Brown E, Lucas C, Carpenter J, Fields B (2005) Legionella pneumophila associated with the protozoan Hartmannella vermiformis in a model multi-species biofilm has reduced susceptibility to disinfectants. Biofouling 21:1–7

    Article  CAS  PubMed  Google Scholar 

  • Edagawa A, Kimura A, Kawabuchi-Kurata T, Kusuhara Y, Karanis P (2009) Isolation and genotyping of potentially pathogenic Acanthamoeba and Naegleria species from tap-water sources in Osaka, Japan. Parasitol Res 105(4):1109–1117

    Article  Google Scholar 

  • González-Robles A, Guadalupe CG, Cristóbal-Ramos AR, Hernández-Ramírez VI, Omaña-Molina M, Martínez-Palomo A (2007) Cell surface differences of Naegleria fowleri and Naegleria lovaniensis exposed with surface markers. Exp Parasitol 117(4):399–404

    Article  PubMed  CAS  Google Scholar 

  • Greub G, Raoult D (2003) Biocides currently used for bronchoscope decontamination are poorly effective against free-living amoebae. Infect Control Hosp Epidemiol 24:784–786

    Article  PubMed  Google Scholar 

  • Guzman-Fierros E, De Jonckheere JF, Lares-Villa F (2008) Identification of Naegleria species in recreational areas in Hornos. Sonora Revista Mexicana de Biodiversidad 79(1):1–5

    Google Scholar 

  • Hoffmann R, Michel R (2001) Distribution of free-living amoebae (FLA) during preparation and supply of drinking water. Int J Hyg Environ Health 203(3):215–219

    Article  CAS  PubMed  Google Scholar 

  • Hsu BM, Chen CH, Wan MT (2008) Enteroviruses prevalence in hot spring recreation areas of Taiwan. FEMS Immunol Med Microbiol 52:253–259

    Article  CAS  PubMed  Google Scholar 

  • Hsu BM, Lin CL, Shih FC (2009) Survey of pathogenic free-living amoebae and Legionella spp. in mud spring recreation area. Wat Res 43(11):2817–2828

    Article  CAS  Google Scholar 

  • Izumiyama S, Yagita K, Furushima-Shimogawara R, Asakura T, Karasudani T, Endo T (2003) Occurrence and distribution of Naegleria species in thermal waters in Japan. J Eukaryot Microbiol 50:514–515

    Article  CAS  PubMed  Google Scholar 

  • Lares-Villa F, De Jonckheere JF, De Moura H, Rechi-Iruretagoyena A, Ferreira-Guerrero E, Fernandez-Quintanilla G, Ruiz-Matus C, Visvesvara GS (1993) Five cases of primary amebic meningoencephalitis in Mexicali, Mexico: study of the isolates. J Clin Microbiol 31:685–688

    CAS  PubMed  Google Scholar 

  • Lee SH, Levy DA, Craun GF, Beach MJ, Calderon RL (2002) Surveillance for waterborne-disease outbreaks—United States, 1999–2000. Morb Mortal Wkly Rep Surveill Summ 51:1–47

    CAS  Google Scholar 

  • Maclean RC, Richardson DJ, Lepardo R, Marciano-Cabral F (2004) The identification of Naegleria fowleri from water and soil samples by nested PCR. Parasitol Res 93(3):211–217

    Article  PubMed  Google Scholar 

  • Marciano-Cabral FM (1988) Biology of Naegleria spp. Microbiol Rev 52:114–133

    CAS  PubMed  Google Scholar 

  • Marciano-Cabral FM, Fulford DE (1986) Cytopathology of pathogenic and nonpathogenic Naegleria species for cultured neuroblastoma cells. Appl Environ Microbiol 51:1133–1137

    CAS  PubMed  Google Scholar 

  • Marciano-Cabral F, Maclean R, Mensah A, Lapat-Polasko L (2003) Identification of Naegleria fowleri in domestic water sources by nested PCR. Appl Environ Microbiol 69:5864–5869

    Article  CAS  PubMed  Google Scholar 

  • Martinez AJ, Visvesvara GS (1997) Free-living, amphizoic and opportunistic amebas. Brain Pathol 7:583–598

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Cullity G, Walpole I, O’Connor J, Masters P (1982) Primary amoebic meningoencephalitis in Western Australia. Med J Aust 1:352–357

    CAS  PubMed  Google Scholar 

  • Miyamoto H, Yamamoto H, Arima K, Fujii J, Maruta K, Izu K, Shiomori T, Yoshida S (1997) Development of a new seminested PCR method for detection of Legionella species and its application to surveillance of Legionellae in hospital cooling tower water. Appl Environ Microbiol 63:2489–2494

    CAS  PubMed  Google Scholar 

  • Morio F, Corvec S, Caroff N, Gallou FL, Drugeon H, Reynaud A (2008) Real-time PCR assay for the detection and quantification of Legionella pneumophila in environmental water samples: utility for daily practice. Int J Hyg Environ Health 211:403–411

    Article  PubMed  Google Scholar 

  • Pelandakis M, Serre S, Pernin P (2000) Analysis of the 5.8S rRNA gene and the internal transcribed spacers in Naegleria spp. and in N. fowleri. J Eukaryot Microbiol 47:116–121

    Article  CAS  PubMed  Google Scholar 

  • Rivera F, Lares F, Gallegos E, Ramirez E, Bonilla P, Calderon A, Martinez JJ, Rodriguez S, Alcocer J (1989) Pathogenic amoebae in natural thermal waters of three resorts of Hidalgo. Mexico Environ Res 50(2):289–295

    Article  CAS  Google Scholar 

  • Rivera F, Ramirez E, Bonilla P, Calderon A, Gallegos E, Rodriguez S, Ortiz R, Zaldivar B, Ramirez P, Duran A (1993) Pathogenic and free-living amoebae isolated from swimming pools and physiotherapy tubs in Mexico. Environ Res 62:43–52

    Article  CAS  PubMed  Google Scholar 

  • Schuster FL (2002) Cultivation of pathogenic and opportunistic free-living amebas. Clin Microbiol Rev 15:342–354

    Article  PubMed  Google Scholar 

  • Stevens AR, De Jonckheere JF, Willaert E (1980) Naegleria lovaniensis new species: isolation and identification of six thermophilic strains of a new species found in association with Naegleria fowleri. Int J Parasitol 10:51–54

    Article  CAS  PubMed  Google Scholar 

  • Sugita Y, Fujii T, Hayashi I, Aoki T, Yokoyama T, Morimatsu M, Fukuma T, Takamiya Y (1999) Primary amebic meningoencephalitis due to Naegleria fowleri: an autopsy case in Japan. Pathol Int 49(5):468–470

    Article  CAS  PubMed  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(10):2728–2745

    Article  CAS  PubMed  Google Scholar 

  • 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):1–26

    Article  CAS  PubMed  Google Scholar 

  • Yáňez M, Carrasco-Serrano AC, Barberá VM, Catalán V (2005) Quantitative detection of Legionella pneumophila in water samples by immunomagnetic purification and real-time PCR amplification of the dotA gene. Appl Environ Microbiol 71(7):3433–3441

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Center for Disease Control Taiwan, ROC (DOH94-DC-1029) and a research grant from the National Science Council of Taiwan, R.O.C. (NSC95-2116-M-194-004).

Author information

Authors and Affiliations

  1. Department of Earth and Environmental Sciences, National Chung Cheng University, 168, University Rd, Min-Hsiung, Chiayi, Taiwan, Republic of China

    Shih-Wei Huang & Bing-Mu Hsu

Authors
  1. Shih-Wei Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bing-Mu Hsu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bing-Mu Hsu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, SW., Hsu, BM. Survey of Naegleria and its resisting bacteria-Legionella in hot spring water of Taiwan using molecular method. Parasitol Res 106, 1395–1402 (2010). https://doi.org/10.1007/s00436-010-1815-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-010-1815-0

Keywords

Search

Navigation