Skip to main content

Advertisement

Log in

Review: Occurrence of the pathogenic amoeba Naegleria fowleri in groundwater

Revue: Présence de l’amibe pathogène Naegleria fowleri dans les eaux souterraines

Revisión: Presencia de la ameba patógena Naegleria fowleri en el agua subterránea

回顾 : 地下水中的致病性变形虫—福氏纳格里阿米巴原虫

Revisão: Ocorrência do patógeno ameba Naegleria fowleri em águas subterrâneas

  • Paper
  • Published:
Hydrogeology Journal Aims and scope Submit manuscript

Abstract

Naegleria fowleri is a thermophilic free-living amoeba found worldwide in soils and warm freshwater. It is the causative agent of primary amebic meningoencephalitis, a nearly always fatal disease afflicting mainly children and young adults. Humans are exposed to the organism via swimming, bathing, or other recreational activity during which water is forcefully inhaled into the upper nasal passages. Although many studies have looked at the occurrence of N. fowleri in surface waters, limited information is available regarding its occurrence in groundwater and geothermally heated natural waters such as hot springs. This paper reviews the current literature related to the occurrence of N. fowleri in these waters and the methods employed for its detection. Case reports of potential groundwater exposures are also included. Despite increased interest in N. fowleri in recent years due to well-publicized cases linked to drinking water, many questions still remain unanswered. For instance, why the organism persists in some water sources and not in others is not well understood. The role of biofilms in groundwater wells and plumbing in individual buildings, and the potential for warming due to climate change to expand the occurrence of the organism into new regions, are still unclear. Additional research is needed to address these questions in order to better understand the ecology of N. fowleri and the conditions that result in greater risks to bathers.

Resume

Naegleria fowleri est. une amibe thermophile libre trouvé dans les sols et eaux douce chaude du monde entier. Il s’agit de l’agent responsable de la méningoencéphalite amibienne primaire, une maladie presque toujours mortelle qui touche principalement les enfants et les jeunes adultes. Les humains sont exposés à l’organisme par la natation, le bain, ou toute autre activité récréative au cours de laquelle l’eau est. fortement inhalée dans les passages nasaux supérieurs. Bien que de nombreuses études aient porté sur la présence de N. fowleri dans les eaux de surface, on dispose de peu d’informations concernant sa présence dans les eaux souterraines et dans les eaux naturelles géothermales telles que les sources thermales. Cet article passe en revue la littérature actuelle relative à la présence de N. fowleri dans ces eaux et aux méthodes employées pour sa détection. Des rapports de cas d’exposition potentielle aux eaux souterraines sont également inclus. Malgré un intérêt accru pour N. fowleri au cours des dernières années au regard des cas bien médiatisés associés à l’eau potable, de nombreuses questions restent sans réponse. Par exemple, la persistance de l’organisme dans certaines sources d’eau et pas dans d’autres n’est. pas bien comprise. Le rôle des biofilms dans les puits d’eau souterraine et dans la plomberie de bâtiments individuels, et le potentiel réchauffement dû au changement climatique sur l’extension de la présence de l’organisme dans de nouvelles régions, ne sont toujours pas clairs. Des recherches supplémentaires sont nécessaires pour aborder ces questions afin de mieux comprendre l’écologie de N. fowleri et les conditions qui entraînent des risques plus importants pour les baigneurs.

Resumen

Naegleria fowleri es una ameba termófila de vida libre encontrada en todo el mundo en suelos y agua dulce cálida. Es el agente causal de la meningoencefalitis amebiana primaria, una enfermedad casi siempre fatal que afecta principalmente a niños y adultos jóvenes. Los seres humanos son expuestos al organismo a través de la natación, el baño, u otra actividad recreativa durante la cual el agua se inhala con fuerza en los pasajes nasales superiores. Aunque muchos estudios han examinado la presencia de N. fowleri en aguas superficiales, se dispone de información limitada sobre su presencia en aguas subterráneas y aguas naturales geotérmicamente calientes, como las aguas termales. Este trabajo revisa la literatura actual relacionada con la aparición de N. fowleri en estas aguas y los métodos empleados para su detección. También se incluyen informes de casos de posibles exposiciones al agua subterránea. A pesar del creciente interés en N. fowleri en los últimos años debido a los casos bien publicitados relacionados con el agua potable, muchas preguntas siguen sin respuesta. Por ejemplo, no se comprende bien por qué el organismo persiste en algunas fuentes de agua y no en otras. Aún no están claros el papel de los biofilms en pozos de agua subterránea y la plomería en edificios individuales, y el potencial de calentamiento debido al cambio climático para expandir la ocurrencia del organismo en nuevas regiones. Se necesitan más investigaciones para abordar estas cuestiones con el fin de comprender mejor la ecología de N. fowleri y las condiciones que dan lugar a mayores riesgos para los bañistas.

摘要

福氏纳格里阿米巴原虫是世界范围内广见于土壤和温淡水中嗜热、独立生存的变形虫。它是引起主要阿米巴脑膜脑炎的载体,这种病几乎是折磨儿童和年轻人的致命疾病。人类在游泳、洗浴或其它娱乐活动中被迫吸入水至鼻腔通道中而接触有机体。尽管许多研究发现在地表水中存在着福氏纳格里阿米巴原虫,但有关其存在于地下水及地热天然水如温泉中的信息非常有限。本文回顾了目前有关这些水中存在福氏纳格里阿米巴原虫的文献及所使用的探测方法。也包括潜在地下水接触的实例报告。由于和饮用水相关联的案例宣传的很到位,近年来人们对福氏纳格里阿米巴原虫的研究兴趣在增加,但许多问题依然没有答案。例如,还没有弄清为什么有机体存留在一些水源中而不存留在其它的水源中。地下水井中的生物膜及单个建筑物的水暖管道的作用以及由于气候变化而升温造成有机体扩展到新的区域等问题仍然还不清楚。需要额外的研究来注重这些问题以便更好地了解福氏纳格里阿米巴原虫的生态环境以及对洗浴者造成更大风险的条件。.

Resumo

Naegleria fowleri é uma ameba termófila de vida livre encontrada mundo afora em solos e águas doces mornas. Esse é o agente causal primário de amebíase meningoencefálica, uma doença quase sempre fatal afligindo principalmente crianças e jovens adultos. Humanos são expostos ao organismo por meio de natação, banhos, ou outras atividades recreacionais nas quais durante a água é forçadamente aspirado para dentro das cavidades nasais superiores. Apesar de diversos estudos terem procurado pela ocorrência de N. fowleri em águas superficiais, estão disponíveis informações limitadas sobre sua ocorrência em águas subterrâneas e águas naturais aquecidas geotermalmente, como nascentes quentes. Esse artigo revisa a literatura atual relacionada com a ocorrência de N. fowleri nessas águas e os métodos aplicados para sua detecção. Casos reportados da exposição potencial das águas subterrâneas também são incluídos. Apesar do interesse crescente em N. fowleri em anos recentes devido a casos bem divulgados ligados a água de beber, muitas questões ainda permanecem sem resposta. Por exemplo, porque o organismo persiste em algumas fontes de água e não em outras ainda não é entendido. O papel dos biofilmes em poços de águas subterrâneas e encanamentos em prédios individuais, e o potencial de aquecimento devido a mudança climática para expandir a ocorrência do organismo para novas regiões ainda são obscuros. Pesquisa adicional é necessária para acessar essas questões no intuito de melhor entender a ecologia da N. fowleri e as condições que resultam em maiores riscos aos banhistas.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abrahams-Sandi E, Retana-Moreira L, Castro-Castillo A, Reyes-Batlle M, Lorenzo-Morales J (2015) Fatal meningoencephalitis in child and isolation of Naegleria fowleri from hot springs in Costa Rica. Emerg Infect Dis 21(2):382–384

    Article  Google Scholar 

  • Baquero RA, Reyes-Batlle M, Nicola GG, Navarro CM, Lop’ez-Arencibia A, Esteban JG, Valladares B, Martı’nez-Carretero E, Pinero JE, Lorenzo-Morales J (2014) Presence of potentially pathogenic free-living amoebae strains from well water samples in Guinea-Bissau. Pathogens Glob Health 108(4):206–211

    Article  Google Scholar 

  • Booth PJ, Bodager D, Slade TA, Jett S (2015) Primary amebic meningoencephalitis associated with hot spring exposure during international travel: Seminole County, Florida, July 2014. MMWR 64(43):1226

    Google Scholar 

  • Bright KR, Marciano-Cabral F, Gerba CP (2009) Occurrence of Naegleria fowleri in Arizona drinking water supply wells. J AWWA 101(11):43–50

    Google Scholar 

  • Cain ARR, Wiley PF, Brownell B, Warhurst DC (1981) Primary amoebic meningoencephalitis. Arch Dis Child 56:140–143

    Article  Google Scholar 

  • Centers for Disease Control and Prevention (2013) Primary amebic meningoencephalitis associated with ritual nasal rinsing: St. Thomas, U.S. Virgin Islands, 2012. MMWR 62(45):904

    Google Scholar 

  • Centers for Disease Control and Prevention (2017) Naegleria fowleri: primary amebic meningoencephalitis (PAM)—amebic encephalitis. https://www.cdc.gov/parasites/naegleria/index.html. http://www.cdc.gov/parasites/naegleria/graphs.html#exposure. Accessed 10 February 2017

  • Cope JR, Ratard RC, Hill VR, Sokol T, Causey JJ, Yoder JS, Mirani G, Mull B, Mukerjee KA, Narayanan J, Doucet M, Qvarnstrom Y, Poole CN, Akingbola OA, Ritter J, Xiong Z, da Silva A, Roellig D, Van Dyke R, Stern H, Xiao L, Beach MJ (2015) The first association of a primary amebic meningoencephalitis death with culturable Naegleria fowleri in tap water from a U.S. treated public drinking water system. Clin Infect Dis 60(8):e36–e42

    Article  Google Scholar 

  • Cope JR, Conrad DA, Cohen N, Cotilla M, DaSilva A, Jackson J, Visvesvara GS (2016) Use of the novel therapeutic agent Miltefosine for the treatment of primary amebic Meningoencephalitis: report of 1 fatal and 1 surviving case. Clin Infect Dis 62(6):774–776

    Article  Google Scholar 

  • Cursons R, Sleigh J, Hood D, Pullon D (2003) A case of primary amoebic Meningoencephalitis: North Island, New Zealand. N Z Med J 116(1187):U712

    Google Scholar 

  • Di Filippo MM, Santoro M, Lovreglio P, Monno R, Capolongo C, Calia C, Fumarola L, D’Alfonso R, Berrilli F, Di Cave D (2015) Isolation and molecular characterization of free-living amoebae from different water sources in Italy. Int J Environ Res Public Health 12:3417–3427

    Article  Google Scholar 

  • Gautam PL, Sharma S, Puri S, Kumar R, Midha V, Bansal R (2012) A rare case of survival from primary amebic meningoencephalitis. Indian J Crit Care Med 16:34–36

    Article  Google Scholar 

  • Goldschmidt D, Scutti S (2016) Rare recovery: Florida teen survives brain-eating amoeba. http://www.cnn.com/2016/08/23/health/brain-eating-amoeba-florida-teen-survives/index.html. Accessed 23 August 2016

  • Goudot S, Herbelin P, Mathieu L, Soreau S, Banas S, Jorand FPA (2014) Biocidal efficacy of monochloramine against planktonic and biofilm-associated Naegleria fowleri cells. J Appl Microbiol 116(4):1055–1065

    Article  Google Scholar 

  • Gupta R, Parashar MK, Kale A (2015) Primary amoebic Meningoencephalitis. J Assoc Physicians India 63(4):69–72

    Google Scholar 

  • Huizinga HW, McLaughlin GL (1990) Thermal ecology of Naegleria fowleri from a power plant cooling reservoir. Appl Environ Microbiol 56(7):2200–2205

    Google Scholar 

  • John DT (1982) Primary amebic meningoencephalitis and the biology of Naegleria fowleri. Annu Rev Microbiol 36:101–123

    Article  Google Scholar 

  • Johnson RO, Cope JR, Moskowitz M, Kahler A, Hill V, Behrendt K, Molinal L, Fullerton KE, Beach MJ (2016) Primary amebic meningoencephalitis associated with exposure to swimming pool water supplied by an overland pipe: Inyo County, California, 2015. MMWR 65(16):424

    Google Scholar 

  • Kuroki T, Yagita K, Yabuuchi E, Agata K, Ishima T, Katsube Y, Endo T (1998) Isolation of Legionella and free-living amoebae at hot spring spas in Kanagawa, Japan. Kansenshogaku Zasshi 72(10):1050–1055

    Article  Google Scholar 

  • Laseke I, Korte J, Lamendella R, Kaneshiro ES, Marciano-Cabral F, Oerther DB (2010) Identification of Naegleria fowleri in warm ground water aquifers. J Environ Qual 39:147–153

    Article  Google Scholar 

  • Latifi AR, Niyyati M, Lorenzo-Morales J, Haghighi A, Tabaei SJ, Lasjerdi Z, Azargashb E (2017) Occurrence of Naegleria species in therapeutic geothermal water sources, northern Iran. Acta Parasitol 62(1):104–109

    Article  Google Scholar 

  • Lee SH, Levy DA, Craun GF, Beach MJ, Calderon RL (2002) Surveillance for waterborne-disease outbreaks: United States, 1999–2000. MMWR Surveill Summ 51(8):1–47

    Google Scholar 

  • Lekkla A, Sutthikornchai C, Bovornkitti S, Sukthana Y (2005) Free-living ameba contamination in natural hot springs in Thailand. Southeast Asian J Trop Med Public Health 36(Suppl 4):5–9

    Google Scholar 

  • Linam WM, Ahmed M, Cope JR, Chu C, Visvesvara GS, da Silva AJ, Qvarnstrom Y, Green J (2015) Successful treatment of an adolescent with Naegleria fowleri primary amebic Meningoencephalitis. Pediatrics 135(3):e744–e748

    Article  Google Scholar 

  • Mackowiak PA (2010) Another killer of the Australian bush: a rapidly fatal meningoencephalitis in a child. Clin Infect Dis 50(10):1375–1376

    Article  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  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(10):5864–5869

    Article  Google Scholar 

  • Marshall M, Naumovitz D, Ortega Y, Sterling CR (1997) Water-borne protozoan pathogens. Clin Microbiol Rev 10(1):67–85

    Google Scholar 

  • Martinez AJ, Visvesvara GS (1997) Free-living, amphizoic and opportunistic amebas. Brain Pathol 7(1):583–598

    Article  Google Scholar 

  • Miller HC, Wylie J, Dejean G, Kaksonen A, Sutton D, Braun K, Puzon G (2015) Reduced efficiency of chlorine disinfection of Naegleria fowleri in drinking water distribution biofilm. Environ Sci Technol 49(18):11125–11131

    Article  Google Scholar 

  • Miller HC, Morgan MJ, Wylie JT, Kaksonen AH, Sutton D, Braun K, Puzon GJ (2017) Elimination of Naegleria fowleri from bulk water and biofilm in an operational drinking water distribution system. Water Res 110:15–26

    Article  Google Scholar 

  • Moussa M, De Jonckheere JF, Guerlotte J, Richard V, Bastaraud A, Romana M, Talarmin A (2013) Survey of Naegleria fowleri in geothermal recreational waters of Guadeloupe (French West Indies). PLoS One 8(1):1–11

    Article  Google Scholar 

  • Moussa M, Tissot O, Guerlotté J, De Jonckheere JF, Talarmin A (2015) Soil is the origin for the presence of Naegleria fowleri in the thermal recreational waters. Parasitol Res 114(1):311–315

    Article  Google Scholar 

  • Okuda DT, Hanna HJ, Coons SW, Bodensteiner JB (2004) Naegleria fowleri hemorrhagic Meningoencephalitis: report of two fatalities in children. J Child Neurol 19(3):231–233

    Google Scholar 

  • Schoeman CJ, van der Vyver AE, Visvesvara GS (1993) Primary amoebic meningo-encephalitis in southern Africa. J Infect 26(2):211–214

    Article  Google Scholar 

  • Schuster F, Visvesvara GS (2004) Opportunistic amoebae: challenges in prophylaxis and treatment. Drug Resist Updat 7(1):41–51

    Article  Google Scholar 

  • Seidel JS, Harmatz P, Visvesvara GS, Cohen A, Edwards J, Turner J (1982) Successful treatment of primary amebic Meningoencephalitis. New Engl J Med 306(6):346–348

    Article  Google Scholar 

  • Shakoor S, Beg MA, Mahmood SF, Bandea R, Sriram R, Noman F, Ali F, Visvesvara GS, Zafar A (2011) Primary amebic meningoencephalitis caused by Naegleria fowleri, Karachi, Pakistan. Emerg Infect Dis 17(2):258–261

    Article  Google Scholar 

  • Sheehan KB, Fagg JA, Ferris MJ, Henson JM (2003) PCR detection and analysis of the free-living amoeba Naegleria in Hot Springs in Yellowstone and Grand Teton National Parks. Appl Environ Microbiol 69(10):5914–5918

    Article  Google Scholar 

  • Siddiqui R, Khan NA (2014) Primary amoebic meningoencephalitis caused by Naegleria fowleri: an old enemy presenting new challenges. PLOS Neglected Trop Dis 8(8):1–8

    Article  Google Scholar 

  • Sifuentes LY, Choate BL, Gerba CP, Bright KR (2014) The occurrence of Naegleria fowleri in recreational waters in Arizona. J Environ Sci Health, Pt A 49:1322–1330

    Article  Google Scholar 

  • Su MY, Lee MS, Shyu LY, Lin WC, Hsiao PC, Wang CP, Ji DD, Chen KM, Lai SC (2013) A fatal case of Naegleria fowleri meningoencephalitis in Taiwan. Korean J Parasitol 51(2):203–206

    Article  Google Scholar 

  • Tyndall RL, Ironside KS, Metler PL, Tan EL, Hazen TC, Fiermans CB (1989) Effects of thermal additions on the density and distributions of thermophilic amoebae and pathogenic Naegleria fowleri in a newly created cooling lake. Appl Environ Microbiol 55(3):722–732

    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  Google Scholar 

  • Wang A, Kay R, Poon WS, Ng HK (1993) Successful treatment of amoebic meningoencephalitis in a Chinese living in Hong Kong. Clin Neurol Neurosurg 95(3):249–252

    Article  Google Scholar 

  • Wellings FM, Amuso PT, Chang SL, Lewis AL (1977) Isolation and Identification of pathogenic Naegleria from Florida lakes. Appl Environ Microbiol 34(6):661–667

    Google Scholar 

  • Yoder JS, Straif-Bourgeois S, Roy SL, Moore TA, Visvesvara GS, Ratard RC, Hill VR, Wilson JD, Linscott AJ, Crager R, Kozak NA, Sriram R, Narayanan J, Mull B, Kahler AM, Schneeberger C, da Silva AJ, Poudel M, Baumgarten KL, Xiao L, Beach MJ (2012) Primary amebic meningoencephalitis deaths associated with sinus irrigation using contaminated tap water. Clin Infect Dis 55(9):e79–e85

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kelly R. Bright.

Additional information

Published in the special issue “Hydrogeology and Human Health”

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bright, K.R., Gerba, C.P. Review: Occurrence of the pathogenic amoeba Naegleria fowleri in groundwater. Hydrogeol J 25, 953–958 (2017). https://doi.org/10.1007/s10040-017-1582-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10040-017-1582-4

Keywords

Navigation