Parasitology Research

, Volume 108, Issue 3, pp 621–627 | Cite as

Prevalence of Acanthamoeba spp. and other free-living amoebae in household water, Ohio, USA—1990–1992

  • Lauren J. Stockman
  • Carolyn J. Wright
  • Govinda S. Visvesvara
  • Barry S. Fields
  • Michael J. Beach
Original Paper

Abstract

Knowledge of the prevalence of free-living amoebae (FLA) in US household water can provide a focus for prevention of amoeba-associated illnesses. Household water samples from two Ohio counties, collected and examined for amoebae during 1990–1992, were used to describe the prevalence of Acanthamoeba and other FLA in a household setting. Amoebae were isolated and identified by morphologic features. A total of 2,454 samples from 467 households were examined. Amoebae were found in water samples of 371 (79%) households. Sites most likely to contain amoeba were shower heads (52%) and kitchen sprayers (50%). Species of Hartmannella, Acanthamoeba, or Vahlkampfia were most common. Detection was higher in biofilm swab samples than in water samples. Detection of FLA and Acanthamoeba, at 79% and 51%, respectively, exceed estimates that have been published in previous surveys of household sources. We believe FLA are commonplace inhabitants of household water in this sample as they are in the environment.

Introduction

Free-living amoebae (FLA), such as those belonging to the genera Acanthamoeba, Echinamoeba, Hartmannella, Naegleria, Mastigina, Vahlkampfia, Vannella, and Vexillifera, are small free-living organisms which feed on bacteria, fungi, and other particulate matter and are highly adaptable to their environment. Known to be ubiquitous and found worldwide, FLA can be isolated from air, soil, and water of both natural sources as well as institutional and domestic water systems (Visvesvara and Stehr-Green 1990; Rodriguez-Zaragoza 1994; Thomas et al. 2006). While many FLA are ubiquitous and harmless to humans, several genera are pathogenic. Acanthamoeba species (genotype) Acanthamoeba castellanii (T4), Acanthamoeba culbertsoni (T10), Acanthamoeba hatchetti (T11), Acanthamoeba polyphaga (T4), Acanthamoeba rhysodes (T4), and Acanthamoeba healyi (T12) have the potential to cause disease such as central nervous system (CNS), skin, and sinus infections, most often in immunocompromised individuals (Visvesvara et al. 2007). In otherwise healthy hosts, Acanthamoeba, Vahlkampfia, and Hartmannella have been associated with corneal infections (Aitken et al. 1996; Lorenzo-Morales et al. 2007; Visvesvara et al. 2007) although causality has not been demonstrated for Vahlkampfia and Hartmannella. Naegleria fowleri has been the cause of fatal CNS infections in children and young adults (CDC 2008; Yoder et al. 2009). Although disease is relatively rare compared with their environmental abundance, these illnesses caused by pathogenic FLA are severe, often challenging to treat, and hence a more complete understanding of their ecologic niche and the places in which human interactions with FLA occur is necessary.

A national outbreak of Acanthamoeba keratitis (AK) detected in the USA in 2007, caused by various Acanthamoeba spp., has drawn attention to Acanthamoeba (Verani et al. 2009). AK affects 1.65 to 2.01 per million contact lens wearers per year in the USA (Schaumberg et al. 1998) and has been described in numerous case reports and outbreaks worldwide. In 2007, investigation of the national outbreak found a multipurpose contact lens cleaning solution that has been associated with this illness (Verani et al. 2009) while behavior and environmental factors such as overnight wear, trauma to the cornea, exposure to lake water and tap water have also been implicated in previous outbreaks and sporadic cases (Stehr-Green et al. 1989; Seal et al. 1992). Although the presence of Naegleria has been studied in water mains in Australia (Puzon et al. 2009) and in well water in Arizona (Blair et al. 2008; Bright et al. 2009), Acanthamoeba presence in US water main systems has not been well defined. Knowledge of the extent to which pathogenic amoebae occur in US household water sources can provide theoretical clues to etiologies of amoeba-associated illnesses and suggest a focus for prevention measures. We present the results from a collection of household water samples that were collected and analyzed from two counties in Ohio between December 1990 and October 1992 to describe the prevalence of Acanthamoeba and other FLA in a US household setting.

Methods

Study design

We used an available dataset which contained FLA identified from water samples collected between December 1, 1990 and November 30, 1992. At that time, data were acquired for a case–control study by Straus et al. where cases of legionnaire’s disease were systematically identified and each matched to two hospitalized controls without pneumonia (Straus et al. 1996). Detailed methods have been previously described (Straus et al. 1996). Briefly, the dataset contains data for water samples and amoeba detections from households of patients 18 years of age or older who were hospitalized at any of 15 acute care hospitals in Franklin and Summit counties, Ohio and participated in a household water survey. Household data collected (Straus et al. 1996) including case status, water heater type, water pH level, chlorine level, and temperature were lost prior to the current analysis. However, Straus et al. found water from case and control patient homes to be equally likely to contain Legionella spp. and amoebae. Therefore, all households were treated as one stratum, regardless of original case or control status, to describe the prevalence of amoeba within household water samples in Franklin and Summit counties.

Sample collection

Each home was visited by a study technician. Samples were collected from the kitchen sink, shower, and bathroom sinks that were most often used by the subject, hot water tank, and other water reservoirs (i.e., air conditioners, humidifiers, pools) if present. Shower most used by the subject: (1) the shower head was swabbed, (2) residual water in the shower head was collected, and (3) the next 0.5 l of warm water was collected. Kitchen sink: (1) the faucet and kitchen sprayer, when present, was swabbed and the swabs placed in a vial with the initial 50 ml of hot water and (2) the next 0.5 l sample of hot water was collected. Bathroom sink most often used by the subject: (1) The faucet was swabbed and the swab placed in a vial with the initial 50 ml of hot water and (2) the next 0.5 l of water was collected. Hot water tank: (1) a 0.5 l sample of water was taken from the drain. All samples were transported and stored at ambient temperature and cultured for amoebae within 3 days.

Laboratory procedures

All FLA were identified as samples were collected during the original study in 1990–1992. Polymerase chain reaction (PCR) method for identification of FLA was not available and no samples were retained for such testing. At the time of the original study, aliquots were split, centrifuged, stored at room temperature, and evaluated at Ohio State University for Legionella and at CDC, Atlanta for amoebae. Sample aliquots for 50 ml samples were plated in addition to the a portion of the sediment following centrifugation of the 50 and 500 ml samples as described (Straus et al. 1996). Samples were plated at CDC using methods previously described (Barbaree et al. 1986). Isolation of amoebae was performed by the CDC laboratory and identification of species of amoeba was performed by Thomas K. Sawyer, Rescon Associates, Royal Oak, MD. The samples were inoculated into nonnutrient agar plates coated with a layer of Escherichia coli and incubated at room temperature. Plates were examined every day for at least 2 weeks for the presence of amoebae (Bovee and Sawyer 1979) since medium sized and large amoebae may appear only after 1 to 2 weeks of culture (Sawyer et al. 1977). If fungi were seen on the plates, small pieces of agar where no fungal hyphae were present were cut out using a sterile scalpel and placed upside down on a fresh agar plate coated with bacteria as above. Once amoebic trophozoites and cysts were seen, they were collected with a sterile bacteriological loop and placed on a slide with a drop of amoeba saline and examined for their characteristic shape, movement of the trophozoites, and cyst morphology and classified to genera level. Amoebae and cysts showing characteristic morphology were subcultured on fresh agar plates and identified to the species level whenever possible (Sawyer et al. 1977). If vahlkampfiid amoebae were cultured they were subjected to an in vitro enflagellation test by suspending a loopfull of trophozoites in distilled water and observing the trophozoites microscopically every 10 min for 2 h. If flagellates were seen then the amoebae were identified as Naegleria (Sawyer et al. 1977).

Analysis

Data were analyzed using SAS version 9.1 (SAS Institute, Cary, NC, USA). If an amoeba was identified in any sample collected from a site, the site was considered positive. Where swab and water specimens were collected from the same site, McNemar’s test for agreement of paired data was applied to determine differences in detection attributable to the sample type. Differences in presence at household site were evaluated by Chi-square test and given a corresponding p value. A p value of less than 0.05 was considered significant.

Results

Household-based analysis

A total of 2,454 samples from 467 households collected, tested and characterized for amoeba from 1990 to 1992 were included. On average, samples from five sites were obtained from each household (range, 2–11 sites sampled). Amoebae were identified in samples from at least one site in 371 (79%) households (Table 1.) Three-quarters (75%) of the positive households had one, two, or three sites positive and one household (<1%) had eight sites (of eight sampled) that were positive. Hartmannella, Acanthamoeba, or Vahlkampfia species were identified by microscopy in at least one site in 247 (53%), 237 (51%), and 149 (32%) of households, respectively. Of Acanthamoeba isolates, the most common species identified was A. hatchetti, found in at least one site in 165 (35%) of households, followed by A. polyphaga in at least one site in 155 (33%) of households.
Table 1

Results from the household-based analysis: amoeba and amoeba species identified from at least one site in the household from water and biofilm samples collected during 1990–1992, Ohio

 

Number of households with amoeba identified (percent of 467 houses)

Amoeba (all genera)

371 (79)

Acanthamoeba (all species)

237 (51)

 A. species unknown

26 (6)

 A. astronyxis

3 (1)

 A. castellanii

18 (4)

 A. culbertsoni

6 (1)

 A. hatchetti

165 (35)

 A. polyphaga

155 (33)

 A. royreba

1 (0)

 A. rhysodes

25 (5)

Echinamoeba

2 (0)

Filamoeba

1 (0)

Hartmannella

247 (53)

Mastigina

22 (5)

Naegleria

15 (3)

 N. species unknown

14 (3)

 N. gruberi

1 (0)

Vahlkamphia

149 (32)

 V. species unknown

146 (31)

 V. avara

2 (0)

 V. inornata

1 (0)

Vannella

36 (8)

Vexillifera

41 (9)

Othera

47 (10)

New/unknown genus

28 (6)

aIncludes Platyamoeba, Comandonia, and Willaertia

Among 358 (77%) households with a date of collection available, there was a trend of increased amoeba detections in summer months (p value for trend = <0.01). For the months of January through May, detections across all households averaged 65% (range, 61–76%); this proportion increased in June through October to average 91% of households positive for amoeba (range, 88–94%). The increase in detections from spring to summer months was seen in all genera except for Naegleria in which case the percentage of households positive was lower than it was in the spring and fall (Fig. 1). There was no appreciable difference in detections across the years of the study.
Fig. 1

Percent of households positive for amoeba species in water or biofilm samples, by season of sample collection, 1990–1992, Ohio

Site-specific analysis

A variety of sites were positive for amoebae (Table 2). Of the primary sites sampled from each home, the shower and kitchen sprayer were most often positive with 52% of showers and 50% of kitchen sprayers containing an amoeba species. Specifically, 22% of showers and 26% of kitchen sprayers contained an Acanthamoeba species. Of 406 sites of any kind positive for Acanthamoeba species, 152 (37%) were found mixed with another genus. Of these, Acanthamoeba was found with Hartmannella (53%) Vahlkampfia (42%), or another genus (5%).
Table 2

Results from the household site-based analysis: location of amoeba and amoeba species identified in the household from water and biofilm samples collected during 1990–1992, Ohio

 

Bathroom sink

Kitchen sink

Shower

Hot water heater

Kitchen sprayer

Otherb

N = 629

N = 473

N = 469

N = 432

N = 137

N = 314

# (%)

# (%)

# (%)

# (%)

# (%)

# (%)

Amoeba (all genera)a

253 (40)

124 (26)

246 (52)

154 (36)

69 (50)

113 (36)

Acanthamoeba (all species)

83 (13)

50 (11)

101 (22)

92 (21)

35 (26)

45 (14)

 A. species unknown

5 (0)

2 (0)

13 (3)

1 (0)

4 (3)

3 (1)

 A. astronyxis

0 (0)

0 (0)

2 (0)

0 (0)

0 (0)

1 (0)

 A. castellanii

2 (0)

2 (0)

8 (2)

1 (0)

4 (3)

2 (1)

 A. culbertsoni

2 (0)

2 (0)

2 (0)

0 (0)

1 (1)

0 (0)

 A. hatchetti

48 (8)

32 (7)

60 (13)

70 (16)

16 (12)

26 (8)

 A. polyphaga

51 (8)

27 (6)

48 (10)

37 (9)

20 (15)

29 (9)

 A. royreba

0 (0)

0 (0)

1 (0)

0 (0)

0 (0)

0 (0)

 A. rhysodes

8 (1)

2 (0)

6 (1)

6 (1)

3 (2)

1 (0)

Echinamoeba

0 (0)

0 (0)

1 (0)

0 (0)

0 (0)

1 (0)

Filamoeba

1 (0)

0 (0)

0 (0)

0 (0)

0 (0)

0 (0)

Hartmannella

160 (25)

53 (11)

144 (31)

49 (11)

28 (20)

48 (15)

Mastigina

8 (1)

3 (1)

9 (2)

0 (0)

6 (4)

1 (0)

Naegleria

2 (0)

1 (0)

1 (0)

1 (0)

0 (0)

11 (4)

Vahlkampfia

53 (8)

31 (7)

47 (10)

45 (10)

16 (12)

25 (8)

Vannella

7 (1)

13 (3)

7 (1)

2 (0)

5 (4)

8 (3)

Vexillifera

21 (3)

5 (1)

12 (3)

1 (0)

5 (4)

5 (2)

Otherc

7 (1)

12 (3)

12 (3)

7 (2)

7 (5)

9 (3)

New/unknown genus

10 (2)

8 (2)

8 (2)

3 (1)

3 (2)

8 (3)

aPercentage of individual genera will not total “all genera” because multiple genera may have been found at each site

bIncludes air conditioner, aquarium, bathtub, bird bath, dehumidifier, drinking fountain, hot tub, humidifier, oxygen tank water, pool, steamer, utility sink, water bucket, water filter, water purifier, water softener, and well water

cIncludes Platyamoeba, Comandonia, and Willaertia

Sample type analysis

The collection of both water and biofilm swabs from sinks and shower sites allowed for a comparison of detection of amoebae by sample type. For each site, amoebae were detected in water samples at a different rate than in swab specimens (p value >0.001), and amoebae were detected in a higher percentage of swab samples than in water samples (Table 3.). However, the number of swab samples that were contaminated with fungus or bacteria was substantial and prevented the identification of the amoeba species. Overall, fungal overgrowth of the sample occurred more often with swabs (41%) than in water (6%) samples.
Table 3

Comparison of amoebae detection by water and biofilm swab sample from household sites where both sample types were collected, 1990–1992, Ohio

Site

Numbera

Type

Positive

Negative

Indeterminate (i.e., contamination with fungal overgrowth, bacteria, rust, or debris)

p value of kappa statistic

Bathroom sink

580

Swab

210 (36%)

128 (22%)

242 (42%)

 

Water

123 (21%)

420 (72%)

37 (6%)

<0.01

Kitchen sink

445

Swab

104 (23%)

114 (26%)

227 (51%)

 

Water

70 (16%)

344 (77%)

31 (7%)

<0.01

Shower

437

Swab

214 (49%)

83 (19%)

140 (32%)

 

Water

136 (31%)

273 (62%)

28 (6%)

<0.01

aOnly sites with both samples collected were included. Households could have had multiple bathroom sinks, kitchen sinks, or showers sampled

Discussion

A recent outbreak of Acanthamoeba keratitis in the USA has raised an interest in knowing possible opportunities for exposure to Acanthamoeba and other free-living amoebae from household water sources. This systematic collection of household water samples is the largest that we are aware of and provided an opportunity to assess the prevalence of FLA in Franklin and Summit counties in Ohio in the 1990s. Household prevalence of FLA and specifically Acanthamoeba detection, at 79% and 51%, respectively, exceed amounts published in a of survey of domestic water in South Florida (Shoff et al. 2008b) and suggests that household exposure in the USA may not be substantially different from that reported in homes in the UK (48–89%) (Seal et al. 1992; Kilvington et al. 2004).

The finding of Acanthamoeba species, A. castellanii, A. polyphaga, and A. hatchetti at bathroom sink faucet sites and showers underscores the exposure opportunity for contact lens wearers since these species are pathogenic and frequently identified as causing AK. The use of established guidelines to limit the introduction of tap water into the eyes of lens wearers such as removing contact lenses before any activity involving contact with water, including showering, using a hot tub or swimming (CDC 2007) remains important, as does the use of effective contact lens disinfection solution (CDC 2007). Numerous studies have found multipurpose solutions to be ineffective against Acanthamoeba isolates and suggest that those containing hydrogen peroxide must be used to reduce the risk of AK in contact lens wearers (Silvany et al. 1990; Hiti et al. 2002; Shoff et al. 2008a; Johnston et al. 2009).

The genera found in this study are consistent with those typically found in aquatic environments (Kyle and Noblet 1986). While we do not have data on the temperature of the water from which amoebae were isolated, a seasonal distribution of detections in household sources is apparent. Thermotolerant FLA were found more often in households where samples were collected during warmer months and this is consistent with ecologic studies from natural ponds and streams (John and Howard 1995). A correlation between the level of amoebae in environmental surface water and amoeba-like corneal infections has been observed in earlier studies (Mathers et al. 1998; Meier et al. 1998). An increase in Acanthamoeba, Vannella, and Naegleria during the summer has been found in studies of FLA distribution in Oklahoma, Virginia and South Carolina waters (Kyle and Noblet 1986; John and Howard 1995; Ettinger et al. 2003). We did not find a summer increase in Naegleria detections, which may be due to the small numbers of Naegleria detected in the household samples or differences in domestic distribution of amoebae compared to outdoor water ecology.

Swab samples of biofilms were more often positive for amoebae than were water samples, and importantly, some swabs were positive in instances where water samples were negative. This suggests that the scraping action of swabbing is more effective at sampling biofilm residents than collecting water samples that have only flowed past the biofilm. As a result, using swabs for detection may lead to a more accurate measure of presence within household sites despite the increased risk of contamination by fungi. While swab samples will collect fungi along with amoebae, especially in biofilms, PCR (not available for FLA identification during the early 1990’s when amoebae were identified in this study) would now be able to identify some amoebae such as Acanthamoeba, Naegleria, Hartmannella, and Vahlkampfia. However, existing PCR methods lack available primers to identify other amoebae and, in the case of Acanthamoeba, may lack the ability to differentiate species.

This study has important differences from other published studies of FLA presence in household water. While this study found amoebae within 79% of households, other studies within the USA and the UK found amoebae in 19% and 48% of households of healthy subjects, respectively (Seal et al. 1992; Shoff et al. 2008b). These other studies contain fewer samples per house than were examined in our study. Looking in an average of five sites from each house both increased the probability of finding amoebae occurrence and created a more representative measure of amoebae within a household. The standardized collection of both water and biofilm swab samples by plumbing technicians in this study, rather than collection by the home resident as done in the previous US study (Shoff et al. 2008b), may have resulted in more consistent sample quality and, as a result, increased detection. There are factors known to affect the presence of FLA, such as water source, water treatment method and geographic location, and differences in these across the USA limits the confidence with which these results can be applied to other regions.

This study has shown FLA to be widespread in the early 1990s among households largely serviced by municipal water utilities. Although data on household water source, chlorine concentration level, and temperature are no longer available and we were unable to match this information to household amoeba detections, from public records, we know that the municipal water that served the majority of Summit and Franklin counties at the time samples were collected was from a variety of sources including well, reservoir, river, or lake water. All municipal water from these sources was treated by conventional filtration with the addition of gaseous chlorine. From available data, we also know that 15% of households in this sample were on non-municipal water (e.g., private wells) in which chlorine concentration levels were likely to be lower than those with water provided by the county (Straus et al. 1996). As many utilities have switched from chlorine to monochloramine for chemical treatment or might consider switching in the near future, the occurrence of FLA in household sources may change from that which is reported here, since monochloramine has been shown to better penetrate biofilms capable of supporting amoeba colonization (Kool et al. 1999; Flannery et al. 2006). Nevertheless, this description of FLA from a large, community-based sample of household water is likely the largest sample and the first of its kind in the USA and would still be expected to be representative of households served by chlorinated municipal water sources.

Important to convey is that high rates of amoeba occurrence do not necessarily represent a higher risk of illness. FLA are commonplace inhabitants of water and soil throughout the world. It is expected that human exposure to amoebae occurs regularly without causing illness. Evidence for this is the relatively high level of antibodies against FLA, found in 100% of sera from some populations (Cursons et al. 1980; Marciano-Cabral et al. 1987; Ferrante 1991; Chappell et al. 2001;) compared to the estimated low disease incidence of 1.65–2.01 per million contact lens wearers per year (Schaumberg et al. 1998). Case–control studies designed to assess the role of FLA in central nervous system infections, corneal infections, and pneumonia, along with host susceptibilities and environmental conditions will be needed to associate specific amoeba species with risk of disease. Household prevalence surveys of water and biofilm sampled systematically from multiple sites within the home will be useful to measure effectiveness of changes in water treatment programs.

Notes

Acknowledgements

The authors acknowledge Dr. Thomas K. Sawyer for his expertise and commitment to identifying the amoebae for this study and Dr. Lauri Hicks for her contribution to the manuscript.

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Copyright information

© Springer-Verlag (outside the USA) 2010

Authors and Affiliations

  • Lauren J. Stockman
    • 1
  • Carolyn J. Wright
    • 2
  • Govinda S. Visvesvara
    • 3
  • Barry S. Fields
    • 2
  • Michael J. Beach
    • 4
  1. 1.Centers for Disease Control and PreventionAtlantaUSA
  2. 2.Centers for Disease Control and PreventionAtlantaUSA
  3. 3.Centers for Disease Control and PreventionAtlantaUSA
  4. 4.Centers for Disease Control and PreventionAtlantaUSA

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