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. 2022 Aug 30;121(11):3033–3050. doi: 10.1007/s00436-022-07631-3

Prevalence of free-living amoebae in swimming pools and recreational waters, a systematic review and meta-analysis

Beni Jequicene Mussengue Chaúque 1,2, Denise Leal dos Santos 1, Davood Anvari 3, Marilise Brittes Rott 1,4,✉
PMCID: PMC9424809  PMID: 36040629

Abstract

Free-living amoebae (FLA) are cosmopolitan microorganisms known to be pathogenic to humans who often have a history of contact with contaminated water. Swimming pools and recreational waters are among the environments where the greatest human exposure to FLA occurs. This study aimed to determine the prevalence of FLA in swimming pools and recreational waters, through a systematic review and meta-analysis that included studies published between 1977 and 2022. A total of 106 studies were included and an overall prevalence of FLA in swimming pools and recreational waters of 44.34% (95% CI = 38.57–50.18) was found. Considering the studies published up to 2010 (1977–2010), between 2010 and 2015, and those published after 2010 (> 2010–2022), the prevalence was 53.09% (95% CI = 43.33–62.73) and 37.07% (95% CI = 28.87–45.66) and 45.40% (95% CI = 35.48–55.51), respectively. The highest prevalence was found in the American continent (63.99%), in Mexico (98.35%), and in indoor hot swimming pools (52.27%). The prevalence varied with the variation of FLA detection methods, morphology (57.21%), PCR (25.78%), and simultaneously morphology and PCR (43.16%). The global prevalence by genera was Vahlkampfia spp. (54.20%), Acanthamoeba spp. (33.47%), Naegleria spp. (30.95%), Hartmannella spp./Vermamoeba spp. (20.73%), Stenamoeba spp. (12.05%), and Vannella spp. (10.75%). There is considerable risk of FLA infection in swimming pools and recreational waters. Recreational water safety needs to be routinely monitored and, in case of risk, locations need to be identified with warning signs and users need to be educated. Swimming pools and artificial recreational water should be properly disinfected. Photolysis of NaOCl or NaCl in water by UV-C radiation is a promising alternative to disinfect swimming pools and artificial recreational waters.

Graphical abstract

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Supplementary information

The online version contains supplementary material available at 10.1007/s00436-022-07631-3.

Keywords: Free-living amoebae, Risk of infection, Swimming pool, Recreational waters

Introduction

Free-living amoebae (FLA) are cosmopolitan and ubiquitous microorganisms widely distributed in the environment and can be opportunistic and/or pathogenic (Visvesvara et al. 2007; Bellini et al. 2022). They have been isolated from many natural and anthropogenic environmental matrices, including plants, soil, air conditioning dust, bottled mineral water, drinking water treatment and distribution system, and cooling towers (Landell et al. 2013; Maschio et al. 2015; Javanmard et al. 2017; Soares et al. 2017; Wopereis et al. 2020; Pazoki et al. 2020). They have also been isolated from contact lenses, swimming pools, and other recreational waters (Fabres et al. 2016; Bunsuwansakul et al. 2019; Santos et al. 2021; Fabros et al. 2021).

Among its representatives with importance for human health, the genera Acanthamoeba, Naegleria, and Balamuthia stand out. Acanthamoeba spp. and its abundance in water bodies seem to be favored by higher temperatures (Kang et al 2020). These protozoa can cause illnesses in healthy people, such as Acanthamoeba keratitis (AK) which primarily affects contact lens wearers, usually due to lens wear while swimming or improper lens cleaning (Dos Santos et al. 2018). In immunosuppressed individuals, it can cause granulomatous amebic encephalitis (GAE), which can be fatal (Visvesvara et al. 2007; Sarink et al. 2022). Acanthamoeba spp. have also been reported to cause skin infections (Murakawa et al. 1995; Paltiel et al. 2004). In addition, it was isolated from 26% (17/63) of critically ill patient urine samples (Santos et al. 2009); similarly, Acanthamoeba (T4) was isolated from 22% (11/50) of urine samples collected from patients with recurrent urinary tract infection (Saberi et al. 2021).

Naegleria fowleri is known as a “brain-eating amoeba” and primarily affects healthy young people using recreational waters, causing primary amoebic meningoencephalitis (PAM) (Fowler and Carter, 1965). PAM is a serious and usually fatal disease if adequate treatment is not initiated at the onset of symptoms (Król-Turmińska and Olender 2017). The rapid deterioration in the health status of patients affected by PAM, combined with the ease of being confused with bacterial meningoencephalitis (since the symptoms are similar), as well as erratic or late diagnosis, contributes to a high prevalence of deaths (> 97%) (Capewell et al. 2015; Johnson et al. 2016). Balamuthia mandrillaris and Sappinia pedatta also cause encephalitis (Gelman et al. 2001; Visvesvara et al. 2007; Cope et al. 2019); however, there are no reports of the isolation of S. diploidea/pedatta from swimming pools and recreational waters.

The FLA essentially have three forms of life, namely, the trophozoite form (with or without flagellum) and the flagellated form which are the active forms of the protozoan, in which it may feed, reproduce, and express pathogenicity, and the form of cysts (which is the form of environmental resistance). Cysts have a double-layer wall made essentially of cellulose (Garajová et al. 2019) that protects the protozoan against unfavorable conditions (e.g., food shortages, dissection, extreme pH, and temperatures) or antimicrobial agents (e.g., NaCl, chlorine, drugs, UV, heat) (Aksozek et al. 2002; Thomas et al. 2008; Chaúque and Rott 2021a, b; Chaúque et al. 2021). FLA are considered the “Trojan Horse” of the microbial world, as phylogenetically diverse microorganisms including bacteria, fungi, and viruses survive and multiply within them; these microorganisms are called amoeba-resistant microorganisms (ARM) (Greub and Raoult 2004; Scheid 2014; Delafont et al. 2016; Hubert et al. 2021; Rayamajhee et al. 2021). A wide range of pathogens of public health importance have been described as being ARM, including Legionella pneumophila, Mycobacterium leprae, Pseudomonas spp., Candida auris, and various viruses (Maschio et al. 2015; Staggemeier et al. 2016; Balczun and Scheid 2017; Turankar et al. 2019; Nisar et al. 2020; Hubert et al. 2021). The participation of FLA in the environmental persistence of severe acute respiratory syndrome 2 (SARS-CoV-2) has also been proposed (Chaúque et al. 2022; Dey et al 2022). All these aspects that characterize the profile of FLA constitute the main attributes that determine the great importance of these protozoa for human health and the environment.

Although increasingly prevalent, diseases caused by FLA remain rare; however, the presence of these protozoa, especially in the aquatic environment, is well documented (Milanez et al. 2022; Stapleton 2021; Saburi et al. 2017; Caumo et al. 2009). The presence of FLA in swimming pools and other recreational waters is of concern, as they can be pathogenic or opportunistic and/or lead to the persistence of non-amoebic pathogens in the water, including waters treated with chlorine-based disinfectants (Siddiqui and Khan 2014; Kiss et al. 2014; Dey et al. 2021). It was determined that the prevalence of Naegleria spp. in different water sources around the world (considering data from 35 countries) was 26.42%, in recreational water it was 21.27% (10.80–34.11), and in swimming pools was 44.80% (16.19–75.45) (Saberi et al. 2020); however, the global prevalence of FLA in swimming pools and recreational waters remains to be determined. The present systematic review and meta-analysis aimed to determine the prevalence of FLA in swimming pools and recreational waters worldwide.

Methods

Article search strategy

The present study, which aimed to determine the prevalence of FLA in swimming pools and recreational waters, was planned and carried out based on the PRISMA 2020 guidelines (Page et al. 2021) (Fig. 1). The search for scientific articles was performed in different databases, including Web of Science, Scopus, PubMed, ScienceDirect, EMBASE, ProQuest, and CAPES periódicos, between July 4 and 9, 2022. In these databases, articles were retrieved using a combination of the following search terms combined with appropriate Boolean operators: “Free-living amoeba,” “swimming pool,” “recreational water,” “prevalence,” “epidemiology,” and “hot springs.” The references of the selected articles were examined in search of some interesting literature. The search for articles in the database was performed by B.J.M.C, and the accuracy of the searches was verified by D.L.S.

Fig. 1.

Fig. 1

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Details of the article retrieval and selection steps based on PRISMA 2020

Selection and exclusion criteria

The screening focused essentially on the title and then on the abstract of the articles. All retrieved articles written in English (reporting primary data), with accessible full text, dealing with the presence of FLA in swimming pools and human recreation waters were selected. Studies based on natural surface waters that do not clearly state that the samples were collected in places where human recreational activities certainly take place were not selected. Studies whose data were insufficient, unclear, or duplicated were excluded. Case studies that do not report the prevalence of FLA in swimming pools and human recreation waters were also excluded.

Data analysis procedure

Data were independently extracted and verified by two authors (B.J.M.C and D.L.S); data verification was performed three times. Data extracted from all articles that met the inclusion criteria were included in the calculation of the global prevalence of FLA in swimming pools and recreational waters. To calculate the prevalence of each FLA genera, only data extracted from articles that included molecular methods for the identification of FLA were used. Data analysis was performed by two authors (D.A and B.J.M.C) using Stata software (version 14; Stata Corp, College Station, TX, USA) and GraphPad prism 8.02. A random-effects model meta-analysis was performed to estimate the combined and weighted prevalence of FLA in swimming pools and recreational waters, using a 95% confidence interval, and the results are visualized using a forest plot. Cochran’s Q test (chi-square) and the Higgins I2 statistic were used to calculate the heterogeneity index among the selected studies. I2 values < 25%, 25%–50%, and > 50% meant low, moderate, and high heterogeneity, respectively. The Egger’s test was used to assess the significance of publication bias among the selected studies; P < 0.001 was considered significant.

Results

From the total of 2034 documents returned by the databases accessed, using the search strategy and inclusion criteria described above, 106 articles were selected (Table 1). These studies are distributed in a total of 30 countries, namely Iran (33), Taiwan (12), Egypt (8), Malaysia (6), Brazil (4), Italy (4), Turkey (4), USA (4), Mexico (3), Saudi Arabia (3), China (2), France (2), Philippines (2), Spain (2), and Thailand (2). One study was included from each of the following countries: Belgium, Bulgaria, Cape Verde, Chile, Finland, Germany, Hungary, India, Jamaica, Japan, Norway, Poland, Portugal, Sweden, and Switzerland. Among the studies, 74.52% (79/106) used or included molecular methods to identify FLA, while 25.47% (27/106) used only morphological methods.

Table 1.

Description of included studies reporting the prevalence of live amoebae in swimming pools and recreational waters

References Country Sample source (total) Analyzed samples Positive samples Methods Identity
Brown And Cursons (1977) Norway Swimming area 50 34 Morphology Acanthamoeba spp., Naegleria fowleri, and Naegleria gruberi
Lyons and Kapur (1977) USA Swimming pool 30 27 Morphology Acanthamoeba spp. and/or Hartmannella spp.
Pernin and Riany (1978) France Swimming pool (9) 44 39 Morphology Acanthamoeba spp., Hartmannella spp., and Naegleria spp.
De Jonckheere (1979) Belgium Swimming pool 16 13 Morphology Acanthamoeba spp. and Naegleria spp.
Janitschke et al. (1980) Germany Swimming pool 14 10 Morphology Acanthamoeba spp.
Scaglia et al. 1983 Italy Thermal pool and mud basin spa 30 7 Morphology, fluorescent-antibody technique N. australiensis
Gogate and Deodhar (1985) India Public swimming pool 12 1 Morphology N. fowleri
Scaglia et al. 1987 Italy Thermal bath and mud basin (34) 51 34 Morphology, pathogenicity test Naegleria spp., Acanthamoeba spp., Vahlkampfia spp., and Hartmannella spp.
Hamadto et al. 1993 Egypt Swimming pool (16) 16 12 Morphology, pathogenicity test Naegleria spp. and Acanthamoeba spp.
Penas-Ares et al. 1994 Spain Thermal spa water (12) 12 8 Morphology Vahlkampfia longicauda, Vahlkampfia salina, Vahlkampia baltica, Vahlkampfia sp., A. polyphaga, Acanthamoeba lenticulata, Naegleria sp., Lingulamoeba sp., Paramoeba aesturina, and Flabellula sp.
Vesaluoma et al. (1995) Finland Public swimming pool and whirlpool (21) 34 14 Morphology Acanthamoeba spp., Vexillifera spp., Flabellula spp., Hartmannella spp., and Rugipes spp.
Munoz et al. 2003 Chile Swimming pool 8 5 Morphology, PCR H. vermiformes, Vanella spp., Naegleria spp., and Acanthamoeba spp.
Sheehan et al. 2003 USA Hot spring (22) 22 12 Morphology, PCR N. australiensis, N. dobsoni, N. americana, N.pagei, N. polaris, and N. fultoni
Izumiyama et al. 2003 Japan Whirlpool bath and hot spring spa (251) 549 197 Morphology, PCR N. fowleri, N. lovaniensis, and N. australiensis
Górnik and Kuźna-Grygiel (2004) Poland Public swimming pools (13) 72 42 Morphology Acanthamoeba spp.
Tsvetkova et al. 2004 Bulgaria Swimming pool (6) 31 15 Morphology, PCR Acanthamoeba spp. and Hartmannella spp.
Lekkla et al. (2005) Thailand Hot spring (13) 68 26 Morphology Acanthamoeba spp. and Naegleria spp.
Sukthana et al. 2005 Thailand Hot spring 57 15 Morphology Naegleria spp. and Acanthamoeba spp.
Rezaeian et al 2008 Iran Swimming pool 2 2 Morphology Acanthamoeba spp.
Caumo et al. (2009) Brazil Swimming pool 65 13 Morphology, PCR Acanthamoeba spp.
Gianinazzi et al. (2009) Switzerland Indoor hot swimming pool 1 1 Morphology, PCR Acanthamoeba lenticulata
Hsu et al. (2009a, b) Taiwan Recreational hot spring 55 9 PCR Acanthamoeba griffini and Acanthamoeba jacobsi
Hsu et al. (2009a) Taiwan Mud recreation area water 34 20 Morphology, PCR Acanthamoeba spp., Hartmannella spp., and Naegleria spp.
Gianinazzi et al. (2010) Sweden Hot springs (4) 31 9 Morphology, PCR Acanthamoeba healyi, Stenoamoeba sp., Hartmannella vermiformis, and Echinamoeba exundans
Huang and Hsu (2010a, b) Taiwan Hot spring and waste water in recreation area 52 11 PCR Acanthamoeba T1, Acanthamoeba T2, Acanthamoeba T3, Acanthamoeba T4, Acanthamoeba T5, Acanthamoeba T6, and Acanthamoeba T15
Huang and Hsu (2010a) Taiwan Hot spring and hot spring facilities 106 15 Morphology, PCR Naegleria lovaniensis, Naegleria australiensis, Naegleria clarki, Naegleria americana, and Naegleria pagei
Init et al. (2010) Malaysia Public swimming pool (14) 14 14 Morphology Acanthamoeba spp. and Naegleria spp.
Lares-Villa et al. 2010 Mexico Natural recreational water (2) 24 24 PCR Thermophilic amoebae, thermophilic Naegleria spp., and N. fowleri
Badirzadeh et al. (2011) Iran Recreational hot spring 28 12 Morphology, PCR Vahlkampfiid and Acanthamoeba castellanii T4
Huang and Hsu (2011) Taiwan Recreational water 107 19 PCR Naegleria spp.
Ithoi et al. (2011) Malaysia Recreational pool, lake, and stream 33 33 Morphology, PCR Naegleria spp.
Nazar et al. 2011 Iran Water in recreation area 50 16 Morphology, PCR Acanthamoeba spp. T4 and Acanthamoeba spp. T5
Alves et al. (2012) Brazil Public swimming pool (7) 7 7 Morphology, PCR Acanthamoeba spp.
Kao et al. (2012a, b, c) Taiwan Recreation and drinking water source (2) 211 13 PCR Naegleria philippinensis, N. clarki, Naegleria gálica, N. americana, N. australiensis, Naegleria dobsoni, N. gruberi, and Naegleria schusteri
Kao et al. (2012a) Taiwan Recreational hot spring (4) 60 9 Morphology, PCR Acanthamoeba T15, Acanthamoeba T4, Acanthamoeba T2, and Acanthamoeba spp.
Kao et al. (2012b) Taiwan Hot spring 60 26 Morphology, PCR N. australiensis, N. lovaniensis, Naegleria mexicana, and N. gruberi
Nazar et al. (2012) Iran Recreational water (22) 50 8 Morphology, PCR Hartmannella vermiformis and Vannella persistens
Niyyati et al. (2012) Iran River recreation area (10) 55 15 Morphology, PCR Acanthamoeba spp. (T4 and T15) and Naegleria spp. (N. pagei, N. clarki, and Naegleria fultoni)
Rahdar et al. 2012 Iran Swimming pool (4) 4 2 Morphology, PCR Acanthamoeba T4
Solgi et al. (2012a, b) Iran Hot spring 30 8 Morphology, PCR Hartmannella vermiformis and Naegleria (N. carteri and Naegleria spp.)
Solgi et al. (2012a) Iran Therapeutic hot spring 60 12 Morphology, PCR Acanthamoeba T4 and T3
Kao et al. 2013a, b China Thermal spring water 48 4 PCR Naegleria spp.
Kao et al. 2013a China Thermal spring 48 5 PCR Acanthamoeba spp.
Moussa et al. (2013) France Recreational geothermal waters (6) 73 35 Morphology, PCR N. fowleri and N. lovaniensis
Tung et al. (2013) Taiwan Hot spring (1) 25 13 Morphology, PCR Naegleria spp. (N. fowleri) and Acanthamoeba spp.
Al-Herrawy et al. (2014) Egypt Swimming pool (10) 120 59 Morphology, PCR Acanthamoeba spp.
Ji et al. (2014) Taiwan Hot spring 61 29 Morphology, PCR Acanthamoeba spp.
Ji et al. (2014) Taiwan Hot spring 61 17 Morphology, PCR Naegleria spp.
Ji et al. (2014) Taiwan Hot spring 61 11 Morphology, PCR Vermamoeba vermiformis
Kiss et al. (2014) Hungary Swimming pool (20) 164 68 Morphology, PCR Acanthamoeba spp.
Onichandran et al. 2014 Philippines Recreational river (4) 23 12 Morphology, PCR Acanthamoeba spp. and Naegleria spp.
Sifuentes et al. (2014) USA Recreational water (33) 103 18 PCR Thermophilic amoebae and N. fowleri
Behniafar et al. (2015) Iran Recreational water and hot spring 40 7 Morphology, PCR Acanthamoeba spp.
Evyapan et al. (2015) Turkey Swimming pool and hot spring 50 21 Morphology, PCR Acanthamoeba spp., Acanthamoeba griffini T3, Acanthamoeba castellanii T4, and A. jacobsi T15
Niyyati et al. (2015a, b) Iran Recreational water (lakes, pools, and streams) 60 9 Morphology, PCR N. australiensis and N. pagei
Niyyati et al. (2015a) Iran Recreational water 50 15 Morphology, PCR A. castellanii T4
Todd et al. (2015) Jamaica Recreational water 83 42 Morphology, PCR Acanthamoeba T4, Acanthamoeba T5, Acanthamoeba T10, and Acanthamoeba T11
Al-Herrawy et al. (2016) Egypt Swimming pool (1) 48 30 Morphology, PCR Acanthamoeba spp., Naegleria spp., and Hartmannella
Armand et al. (2016) Iran Swimming pool 17 12 Morphology, PCR Vermamoeba spp. and Acanthamoeba spp.
Azlan et al. 2016 Malaysia Recreational lake 7 7 Morphology Acanthamoeba spp.
Fabres et al. (2016) Brazil Hot tubs and thermal pool 72 20 Morphology, PCR Acanthamoeba T3, Acanthamoeba T4, Acanthamoeba T5, and Acanthamoeba T15
Latifi et al. (2016) Iran Hot spring 66 2 Morphology, PCR Balamuthia mandrillaris
Niyyati et al. (2016a, b) Iran Geothermal water source 40 20 PCR Acanthamoeba T4 and T2
Niyyati et al. (2016a) Iran Recreational water 25 25 Morphology Vahlkampfidae spp., Acanthamoeba spp., Thecamoeba spp., and Miniamoebae spp.
Al-Herrawy et al. (2017) Egypt Swimming pool (2) 144 37 Morphology, PCR Acanthamoeba spp. and Naegleria spp.
Di Filippo et al. (2017) Italy Geothermal spring 36 26 Morphology, PCR N. australiensis, Naegleria itálica, N. lovaniensis, and Naegleria spp.
Javanmard et al. (2017) Iran Swimming pool and hot spring 33 6 Morphology, PCR N. pagei and N. gruberi
Latifi et al. (2017) Iran Recreation hot spring 22 12 Morphology, PCR Naegleria spp. (N. australiensis, N. americana, N. dobsoni, N. pagei, N. polaris, and N. fultoni)
Mafi et al. (2017) Iran Swimming pool and park pond (40) 75 18 Morphology Acanthamoeba spp., Hartmannella spp., and Vahlkampfiids
Reyes-Batlle et al. (2017) Spain Recreational water (10) 10 1 Morphology, PCR Naegleria spp.
Toula and Elahl 2017 Saudi Arabia Swimming pool (6) 16 6 Morphology Acanthamoeba spp. and Naegleria spp.
Dodangeh et al. (2018) Iran Recreational hot spring 24 11 Morphology, PCR Acanthamoeba castellanii T4
Ghaderifar et al. 2018 Iran Parks pond water (13) 90 31 Morphology, PCR Acanthamoeba T4
Hikal et al (2018) Egypt Swimming pool (5) 100 24 Morphology, PCR Naegleria fowleri
Hikal et al. (2018) Egypt Swimming pool (5) 100 79 Morphology, PCR Naegleria spp.
Lares-Jiménez et al. (2018) Mexico Hot spring (1) 8 8 Morphology, PCR N. lovaniensis, A. jacobsi, Stenamoeba sp., and Vermamoeba vermiformis
Latiff et al. (2018) Malaysia Recreational hot spring (5) 52 38 Morphology Acanthamoeba spp. and Naegleria spp.
Poor et al. (2018) Iran Swimming pool and hot tubs (10) 40 8 Morphology, PCR Acanthamoeba T3 and Acanthamoeba T4
Vijayakumar (2018) Saudi Arabia Pools and recreation waters 27 7 Morphology Acanthamoeba spp.
Xue et al. 2018 USA lake recreation areas (10) 160 56 PCR N. fowleri
Gabriel et al. 2019 Malaysia Recreational place 57 40 Morphology, PCR Acanthamoeba spp. and Naegleria spp.
Haddad et al. (2019) Iran Hot springs 54 15 Morphology, PCR Acanthamoeba castellanii T4, Vermamoeba vermiformis, N. australiensis, N. pageii, and N. gruberi
Hussain et al. (2019) Malaysia Recreational hot spring (5) 50 38 Morphology, PCR Acanthamoeba T4, T15, T3, T5, T11, and T17
Maghsoodloorad et al. 2019 Iran Recreational park water 30 8 Morphology, PCR Acanthamoeba spp. T4 and Acanthamoeba spp. T15
Salehi et al. 2019 Iran Park pool and swimming pool 14 12 Morphology, PCR Acanthamoeba T2, T4, T5, and T11
Attariani et al. (2020) Iran Swimming pool 42 3 Morphology, PCR Acanthamoeba spp.
Ballares et al. 2020 Philippines Recreational water (6) 16 6 Morphology, PCR Acanthamoeba T4, Acanthamoeba T5, and Acanthamoeba T9
Bonilla-Lemus et al. 2020 Mexico Recreational water (9) 9 9 Morphology, PCR N. australiensis, N. gruberi, N. fowleri, N. clarki, and N. pagei
Değerli et al. (2020) Turkey Thermal swimming pool 434 148 Morphology, PCR Acanthamoeba spp. and Naegleria spp.
El-Badry et al. 2020 Egypt Swimming pool (7) 28 0 Morphology, PCR
Esboei et al. (2020) Iran Swimming pools 30 12 Morphology, PCR Acanthamoeba T4
Latifi et al. (2020) Iran Hot spring and beach 81 54 Morphology, PCR Acanthamoeba (T3, T4 e T5), V. vermiformis, and Naegleria spp.
Paknejad et al. (2020) Iran Swimming pool and bathtub 166 31 Morphology, PCR Acanthamoeba T3, Acanthamoeba T4, Acanthamoeba T11, Acanthamoeba sp., Protacanthamoeba bohemica, and N. lovaniensis
Sarmadian et al. (2020) Iran Swimming pool (6) 6 1 Morphology Acanthamoeba spp.
Sarmadian et al. (2020) Iran Swimming pool (6) 576 1 Morphology Acanthamoeba spp.
Zeybek and Türkmen 2020 Turkey Swimming pool 25 7 Morphology, FISH
Aykur and Dagci (2021) Turkey Swimming pool 26 3 PCR Acanthamoeba T2, T4, and T5
Bakri et al. 2021 Saudi Arabia Swimming pool 10 4 Morphology, PCR Acanthamoeba spp. and Naegleria spp.
Berrilli et al. (2021) Italy Hot spring (2) 36 33 Morphology, PCR V. vermiformisi, N. australiensisi, Acanthamoeba T4, and Acanthamoeba T15
Eftekhari-Kenzerki et al. (2021) Iran Indoor public swimming pool (20) 80 32 Morphology, PCR Acanthamoeba spp.
Reyes-Batlle et al. (2021) Portugal Swimming pool facilities (20) 20 0 PCR
Nageeb et al. (2022) Egypt Swimming pool (2) 8 0 Morphology, PCR
Rocha et al. 2022 Brazil Swimming pool (9) 36 15 Morphology Acanthamoeba spp. and Naegleria spp.
Salehi et al. 2022 Iran Swimming pool and park pool 20 17 Morphology, PCR Acanthamoeba (T2, T3, T4, T11, and T15)
Sousa-Ramos et al. 2022 Cape Verde Recreational fountain and swimming pool 4 2 Morphology, PCR Acanthamoeba sp. T4 and Vannella sp.
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The included studies were published between 1977 and 2022, and the distribution of studies by year and the average percentage value of positive samples per year are shown in Fig. 2. FLA were detected in at least 1 sample of 97.17% (103/106) of selected studies (Table 1).

Fig. 2.

Fig. 2

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Distribution of selected studies, and mean percentage of positive samples for FLA per year

Publication bias was checked by Egger’s regression test, showing that it may have a substantial impact on total prevalence estimate (Egger bias: 6.8, P < 0.001) (Fig. 3). This suggests that the reported global prevalence may have been impacted by publication bias.

Fig. 3.

Fig. 3

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Result of Egger’s bias assessment for the prevalence of free-living amoebae in swimming pools and recreational waters

Based on the random-effects model meta-analysis, the pooled prevalence of FLA in water sources was 44.34% (95% CI = 38.57–50.18). The included studies demonstrated a strong heterogeneity (Q = 2198.0, df = 102, I2 = 95.4%, P < 0.0001) (Fig. 4).

Fig. 4.

Fig. 4

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Forest plot of the worldwide prevalence of free-living amoebae in swimming pools and recreational waters

The global prevalence of FLA in swimming pools and recreational waters considering studies published up to 2010 (1977–2010) was considerably higher 53.09% (95% CI = 43.33–62.73) than in studies published between 2010 and 2015, 37.07% (95% CI = 28.87–45.66), and those published after 2015 (> 2015–2022) 45.40% (95% CI = 35.48–55.51) (Table 2).

Table 2.

Subgroup analysis of FLA in water sources

Subgroup variable Prevalence (95% CI) I2 (%) Heterogeneity (Q) P-value Interaction test (X2) P-value
Year
  < 2010 53.09 (43.33–62.73) 89.5% 210.4 P < 0.001 449.4 P < 0.001
  2010–2015 37.07 (28.87–45.66) 93.6% 519.5 P < 0.001
  > 2015 45.40 (35.48–55.51) 96.7% 1366.2 P < 0.001
Continent
  Africa 51.27 (35.08–67.33) 93.5% 107.8 P < 0.001 156.7 P < 0.001
  America 63.99 (45.03–80.92) 94.5% 201.7 P < 0.001
  Asia 37.38 (30.12–44.93) 95.7% 1403.3 P < 0.001
  Europe 51.99 (42.52–61.40) 89.5% 190.6 P < 0.001
Country
  Brazil 43.70 (21.99–66.76) 88.7% 26.5 P < 0.001 26.0 P < 0.001
  China 10.15 (4.99–16.87) - 0.1 P = 0.737
  Egypt 51.65 (31.74–71.30) 95.3% 107.0 P < 0.001
  France 69.62 (27.07–97.94) - 22.5 P < 0.001
  Iran 35.11 (24.74–46.26) 95.9% 787.8 P < 0.001
  Italy 64.76 (37.01–87.95) 92.1% 38.2 P < 0.001
  Malaysia 87.38 (73.20–96.72) 85% 33.3 P < 0.001
  Mexico 98.35 (92.56–99.96) 0% 0.1 P = 0.913
  Philippines 46.29 (31.43–61.48) - 0.7 P = 0.377
  Saudi Arabia 32.85 (21.28–45.60) 0% 1.0 P = 0.602
  Spain 37.68 (1.06–88.08) - 7.7 P = 0.005
  Taiwan 26.33 (17.36–36.42) 90.6% 116.4 P < 0.001
  Thailand 32.68 (21.82–44.57) - 1.9 P = 0.160
  Turkey 30.60 (20.92–41.23) 65.6% 8.7 P = 0.033
  USA 48.70 (22.32–75.47) 95.3% 63.7 P < 0.001
Origin
  Hot springs 39.12 (30.48–48.13) 93% 369.0 P < 0.001 51.6 P = 0.224
  Indoor hot swimming pools 52.27 (14.55–88.50) - 1.8 P = 0.169
  Public swimming pools 49.47 (36.87–62.10) 97% 1201.5 P < 0.001
  Recreational waters 44.44 (33.19–55.99) 95% 538.7 P < 0.001
  Thermal swimming pools 46.05 (2674–65.99) 88.8% 26.7 P < 0.001
Diagnostic method
  Morphology 57.21 (37.99–7535) 97.8% 1083.3 P < 0.001 373.5 P < 0.001
  PCR 25.78 (14.18–39.44) 94.6% 183.6 P < 0.001
  Morphology and PCR 43.16 (37.73–48.67) 91.6% 757.6 P < 0.001
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Considering the continents covered by the selected studies, the highest prevalence 63.99% (95% CI = 45.03–80.92) was reported in America and the lowest 37.38% (95% CI = 30.12–44.93) in Asia. Among the countries from which more than one study was included, Mexico had the highest prevalence of FLA in swimming pools and recreational waters 98.35% (95% CI = 92.56–99.96), and the lowest prevalence 10.15% (95% CI = 4.99–16.87) was recorded in China (Table 2).

Considering the different sampling sources, the highest prevalence of FLA 52.27% (95% CI = 14.55–88.50) was obtained in indoor hot swimming pools, and the lowest prevalence 39.12% (95% CI = 30.48–48.13) was obtained in hot springs (Table 2).

The analysis of data from studies that used only morphological methods to identify FLA showed the highest prevalence 57.21% (95% CI = 37.99–7535), the lowest prevalence 25.78% (95% CI = 14.18–39.44) was obtained from studies based only on molecular methods (PCR), and an intermediate prevalence value 43.16% (95% CI = 37.73–48.67) was obtained by analyzing studies that simultaneously used morphological and molecular methods (Table 2).

The subgroup analysis revealed that there were statistically significant differences between the overall prevalence of FLA in water sources and year (X2 = 449.4, P < 0.001), continent (X2 = 156.7, P < 0.001), country (X2 = 26.0, P < 0.001), and diagnostic method (X2 = 373.5, P < 0.001) (Table 2).

The highest values of the global prevalence of different genera of FLA in swimming pools and recreational waters were from Vahlkampfia spp. (54.20%), Acanthamoeba spp. (33.47%), and Naegleria spp. (30.95%). For other genera, Hartmannella spp./Vermamoeba spp., Stenamoeba spp., and Vannella spp., the global prevalence values were 20,73%, 12.05%, and 10.75%, respectively (Table 3). The results of Egger’s regression test, as well as the forest plot of the worldwide prevalence of each of these FLA genera in swimming pools and recreational waters, can be seen in Fig. S1, S2, S3, S4, S5, and S6 of the supplementary material, respectively.

Table 3.

Global prevalence, publication bias, and heterogeneity of FLA in water sources

Genus Prevalence, % (95% CI) Cochran Q df I2 (%) P-value Egger bias P-value
Acanthamoeba spp. 33.47 (28.06–39.11) 429.1 55 87.2%  < 0.001 3.4 0.0002
Hartmannella spp./Vermamoeba spp. 20.73 (7.73–38.39) 30.55 5 83.8% 0.0008 5.9 0.1363
Naegleria spp. 30.95 (22.85–39.69) 676.0 38 94.4%  < 0.001 4.6 0.0054
Stenamoeba spp. 12.05 (0.08–39.61) 3.2 1 - 0.0732 - -
Vahlkampfia spp. 54.20 (27.49–79.67) 12.6 2 84.2% 0.0018 - -
Vannella spp. 10.75 (0.01–37.14) 2.2 1 - 0.133 - -
Open in a new tab

CI, confidence interval; df, degree of freedom

Discussion

FLA are cosmopolitan microorganisms ubiquitous in all matrices of natural and anthropogenic environments, including water resources. The presence of FLA in pools and recreational waters is worrying, since some of these microorganisms are human pathogens/opportunists, as well as being widely implicated in persistence and/or pseudo-resistance of pathogenic bacteria, viruses, and fungi in water, including in water treated with disinfectants (Thomas et al. 2004; Staggemeier et al. 2016; Mavridou et al. 2018; Gomes et al. 2020; Hubert et al. 2021).

The studies included in present review are distributed by five continents; however, they have a heterogeneous spatial distribution within the territories of the continents; this can suggest differences in the level of FLA importance for health in the contexts of different countries, as well as differences in the frequency of cases diseases associated with the FLA. The frequency of cases of FLA-related diseases can be influenced by the difference in the predominance of risk factors and the sensitivity of the health surveillance strategy of each country, as well as the heterogeneous distribution of trained professionals carrying out research in this area. In addition, the ease of confusing symptoms of diseases associated with the FLA with those caused by other microorganisms, combined with some cases of rapid deterioration of the patient’s health and death (Jahangéer et al. 2020) can contribute to the rarity of reports or even the lack of association of diseases with FLA, especially in contexts where post-mortem study policies are not robust.

Our findings show that the global prevalence of FLA in swimming pools and recreational waters is 44.34%; however, a higher (53.09%) and intermediate (45.40%) prevalence value was obtained when considering the data from studies published up to 2010 and studies published after 2015, respectively. A lower prevalence value (37.07%) was obtained when analyzing data from studies published between 2010 and 2015 (Table 2). A similar result was reported in a study that aimed to determine the prevalence of Naegleria spp. in water resources (Saberi et al. 2020). This reduction in the prevalence reported in most recent studies was attributed to the most accurate diagnosis and reduction of false positive results (Jahangeeer et al. 2020; Saberi et al. 2020), as contrary to studies published up to 2010, the vast majority of studies published after 2010 used molecular methods for FLA identification. Curiously, our results show that the overall prevalence of FLA considering studies that used both morphological and molecular methods is close to the mean of the prevalence values obtained from data from studies that used only one of the methods (Table 2). This may suggest that the simultaneous use of these two methods reduces the extreme values obtained separately by each of the methods, and that these methods can be complementary, especially in studies that aim to assess the presence or absence of viable FLA in water samples. The authors agree that the morphological method (generally based on culture) is more laborious and less precise than molecular methods in the identification of FLA (Saberi et al. 2020; Hikal et al. 2018).

The subgroup analysis considering the distribution of the studies by the continents showed that FLA are more prevalent in the swimming pools and recreational water from America (63.99%), followed by Europe (51.99%) and Africa (51.27%). In relation to countries, the highest value of the prevalence of FLA was obtained in Mexico (98.35%), followed by Malaysia (87.38%), France (69.62%), and Italy (64.76%), and the lowest values were obtained in China (10.15%), Taiwan (26.33%), Turkey (30.60), and Thailand (32.68%). As for the sample source, the indoor hot swimming pools presented a higher value (52.27%) of FLA prevalence, followed by public swimming pools (49.47%) and thermal swimming pools (46.05%). The genera Vahlkampfia spp., Acanthamoeba spp., and Naegleria spp. were more prevalent, presenting the following prevalence values, 54.20%, 33.47%, and 30.95%, respectively (Table 3). The lowest prevalence value was for Vannella spp. (10.75%). These results are in accordance with other authors whose studies reported high prevalence of FLA (Acanthamoeba spp. 48.5%, Naegleria spp. 46.0%, Vermamoeba spp. 4.7%, and Balamuthia spp. 0.7%) in hot springs (Fabros et al. 2021). Saberi et al. (2020) reported the following prevalence values for Naegleria spp. 44.80%, 32.88%, and 21.27%, in swimming pools, hot springs, and recreational waters, respectively. The subgroup analysis showed that prevalence values are statistically different (P < 0.001) for all variables studied (Table 2). These findings are in accordance with other studies that reported a variable distribution in abundance and diversity of FLA species around the world (Jahangéer et al. 2020; Saberi et al. 2020; Fabros et al. 2021).

The global prevalence of FLA reported in the present study (44.34%) is worrying, since direct contact between humans and these waters is often established. In addition, several studies have reported the isolation of several potentially pathogenic FLA (Caumo et al. 2009; Alves et al. 2012; Behniafar et al. 2015;) and others with proven pathogenicity in ex vivo and in vivo trials (Brown and Cursons 1977; Janitschke et al. 1980; Rivera et al. 1983, 1993; Gianinazzi et al. 2009). Most of these FLA are identified as N. fowleri, Acanthamoeba spp., and Balamuthia mandrillaris. Most isolates of Acanthamoeba spp. reported as pathogens are distributed among the T5, T11, T15, T3, and T4 genotypes, and among them, the T4 genotype is more prevalent in hot springs (Mahmoudi et al. 2015; Fabros et al. 2021) and is associated with most cases of Acanthamoeba keratitis (Diehl et al. 2021; Bellini et al. 2022). The presence and abundance of FLA in swimming pool water clearly indicate that in addition to these microorganisms being resistant to chlorine in the dosage used in the treatment of drinking water (Thomas et al. 2004; Majid et al. 2017; Gomes et al. 2020), they are also resistant to chlorine and other disinfectants in the dosage used for swimming pools and artificial recreational waters (Rivera et al. 1983; Kiss et al. 2014; Zeybek et al. 2017). Acanthamoeba castellanii trophozoites and cysts have been reported to be resistant to exposure for more than 2 h to NaOCl and NaCl at concentrations up to 8 mg/L and 40 g/L, respectively. On the other hand, exposure to the combined effect of NaOCl or NaCl with ultraviolet C (UV-C) radiation resulted in rapid inactivation of trophozoites even when lower concentrations of NaOCl and NaCl were used (Chaúque and Rott 2021a, b). Cyst inactivation was achieved by twice as long exposure (300 min) to the combined effect of NaOCl or NaCl and UV-C, with redosing of NaOCl. Despite having demonstrated that both methods are effective, and that they have a strong potential to be used in the effective disinfection of swimming pool water, it was found that the use of NaCl is more cost-effective, as it is cheaper and has a residual effect; redosing is not necessary and is simple to apply (Chaúque and Rott 2021a, b). On the other hand, the use of solar UV radiation (UV-A and B) in place of UV-C (which depends on electricity) can further reduce the cost of the disinfection process. The effectiveness of using solar UV to photolyse NaOCl to inactivate chlorine-resistant microorganisms has been previously documented (Zhou et al. 2014). Readers interested in solar water disinfection technology applicable to recreational water treatment are directed to the appropriate literature (Chaúque and Rott 2021a; Chaúque et al. 2022).

The main aspects that constituted limitations for the present study are the following: the lack of studies carried out in most countries of the world; the heterogeneous distribution of the number of studies among the included countries; difference in FLA identification methods among many studies and discrepancy in the number of samples considered positive by the morphological and molecular method in the same study. The loss of isolates from positive samples in some studies, due to fungal contamination of non-nutrient agar plates prior to molecular identification of the amoebae, was also a limitation.

Conclusion

It is concluded that the prevalence of FLA in swimming pools and recreational waters is high and, therefore, of concern, since there is a risk of contracting infection by pathogenic amoebae or other pathogens (such as fungi, bacteria, and viruses) that may be harbored and dispersed by FLA in water (Mavridou et al. 2018). Thus, it is necessary to implement disinfection techniques that are effective in eliminating microorganisms, including FLA, in swimming pools and artificial recreational waters. The use of the combined effect of NaCl and UV-C has great potential to be used to eliminate or minimize the risk of infection by FLA in swimming pools and other artificial recreational waters. The potential risk of infection by FLA in natural recreational waters needs to be routinely quantified by health surveillance. Warning signs need to be placed where there is minimal risk of infection by FLA, and people using these water bodies need to be educated about the potential risk and possible safety measures. These measures include not diving in recreational waters wearing contact lenses, preventing water from entering the airways and eyes, and avoiding jumping into the water. Health care workers (especially those working near recreational water use sites with risk of infection by FLA) need to be trained to be on the lookout for symptoms suggestive of infection by FLA, especially in summer.

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 756 KB) (756.1KB, pdf)

Acknowledgements

The authors would like to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the scholarship granted to Chaúque, BJM, and CNPq for the researcher grant to Rott, MB.

Author contribution

B.J.M.C. conceived the idea, wrote the project, collected and analyzed the data, and wrote the manuscript. D.S. participated in the conception of the idea, performed the data verification, and wrote and revised the manuscript. D.A. performed data analysis and manuscript review. M.B.R. managed the project and reviewed the manuscript. All authors approved the publication of this version of the manuscript.

Data availability

Not applicable.

Declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Footnotes

Publisher's note

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

Contributor Information

Beni Jequicene Mussengue Chaúque, Email: benichauq@gmail.com.

Denise Leal dos Santos, Email: delealsantos@yahoo.com.br.

Davood Anvari, Email: davood_anvari@live.com.

Marilise Brittes Rott, Email: marilise.rott@ufrgs.br.

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