Water Research 114 (2017) 14e22

Contents lists available at ScienceDirect

Water Research
journal homepage: www.elsevier.com/locate/watres

Review

Waterborne transmission of protozoan parasites: Review of

worldwide outbreaks - An update 2011e2016
Artemis Efstratiou a, b, Jerry E. Ongerth a, c, Panagiotis Karanis a, *
a
State Key Laboratory of Plateau Ecology and Agriculture, Center for Biomedicine and Infectious Diseases, Academy of Animal Science and Veterinary
Medicine, Qinghai University, Xining, Qinghai 810016, PR China
b
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan
c
Civil, Mining, & Environmental Engineering, University of Wollongong, Wollongong, NSW 2522, Australia

a r t i c l e i n f o a b s t r a c t

Article history: This review provides a comprehensive update of worldwide waterborne parasitic protozoan outbreaks
Received 22 November 2016 that occurred with reports published since previous reviews largely between January 2011 and
Received in revised form December 2016. At least 381 outbreaks attributed to waterborne transmission of parasitic protozoa were
18 January 2017
documented during this time period. The nearly half (49%) of reports occurred in New Zealand, 41% of the
Accepted 19 January 2017
Available online 25 January 2017
outbreaks in North America and 9% in Europe. The most common etiological agent was Cryptosporidium
spp., reported in 63% (239) of the outbreaks, while Giardia spp. was mentioned in 37% (142). No out-
breaks attributed to other parasitic protozoa were reported. The distribution of reported outbreaks does
Keywords:
Contamination
not correspond to more broadly available epidemiological data or general knowledge of water and
Cryptosporidium environmental conditions in the reporting countries. Noticeably, developing countries that are probably
Diarrhea most affected by such waterborne disease outbreaks still lack reliable surveillance systems, and an in-
Giardia ternational standardization of surveillance and reporting systems has yet to be established.
Protozoan parasites © 2017 Elsevier Ltd. All rights reserved.
Public health surveillance systems
Waterborne disease outbreak (WBDO)
Worldwide review

Contents

1. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
2. Search . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
2.1. Outbreaks reported between 2011 and 2016 and analysis of results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
2.2. Current and future challenges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
3. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

1. Background worldwide waterborne outbreaks from 1991 to 2008 11% were

caused by parasites (Baldursson and Karanis, 2011; Karanis et al.,
Waterborne infectious diseases remain a major source of 2007; Yang et al., 2012), and parasitic protozoan outbreaks are
morbidity and mortality in the world, causing more than 2.2 million one of the leading causes of 1.7 billion cases of diarrhea. They
deaths per year and far more cases of illness every day, including contribute to 842,000 deaths annually and remain the second
diarrhea and gastrointestinal diseases (www.who.int). Among the leading cause of death in children under 5 years of age (www.who.
int, Kotloff et al., 2013; Checkley et al., 2015; Platts-Mills et al.,
2015).
* Corresponding author. Cryptosporidiosis and giardiasis are among the most common
E-mail address: panagiotis.karanis@uk-koeln.de (P. Karanis).

http://dx.doi.org/10.1016/j.watres.2017.01.036
0043-1354/© 2017 Elsevier Ltd. All rights reserved.
 A. Efstratiou et al. / Water Research 114 (2017) 14e22
waterborne infectious agents causing diarrhea and the most com-
mon protozoan agents with a total of 30,000 cases reported every
year in the United States alone (Yoder et al., 2012a, 2012b). The
waterborne incidents are logically related to human Cryptospo-
ridium prevalence estimated to be 3e5%, and Giardia infecting
approximately 10% of the world's population (Huang and White,
2006). In the group of parasitic protozoa, several other species
may be transmitted to humans through the drinking water route
and cause infections: Entamoeba histolytica, Toxoplasma gondii,
Balantidium coli, Cyclospora cayetanensis, Microsporidia, Isospora,
Naegleria spp. Sarcocystis spp., Balantidium coli, Acanthamoeba spp.
and Blastocystis hominis (Plutzer and Karanis, 2016). Transmission
by the fecal-oral route renders most of these protozoa capable of
infecting humans through various means of fecal contamination of
land and rivers by feces of both human and animal origin (Plutzer
and Karanis, 2016; Lanata, 2003).
Accurate estimation of waterborne disease requires compilation
of global health statistics and the implementation of effective sur-
veillance systems covering all countries. In the US, the USEPA and
Centers for Disease Control and Prevention have collaborated to
collect information about the causes of waterborne disease out-
breaks (WBDOs) starting in 1971 e.g. USA Waterborne Disease and
Outbreak Surveillance System (WBDOSS). The CDC publishes
annual or biennial summaries of Outbreaks Associated with
Drinking Water (Beer et al., 2015a), Outbreaks Associated with
Recreational Water (Hlavsa et al., 2015), and Outbreaks Associated
with Environmental and Undetermined Water Exposures (Beer
et al., 2015b). In succeeding years, many countries established
their own independent surveillance systems; Sweden in 1980
(Stanwell-Smith et al., 2003), Japan in 1981 with the National
Epidemiological Surveillance of Infectious Diseases (NESID), En-
gland and Wales in 1983 for Cryptosporidium and in 1992 for out-
breaks of infectious intestinal disease (Wall et al., 1996), and
Australia in 1990 with the National Notifiable Diseases Surveillance
System (NNDSS). Furthermore, the United Kingdom established the
Health Protection Agency (HPA) in 2003, which later became part of
Public Health England, an executive agency of the Department of
Health, and the Public Health Agency of Canada (PHAC) was foun-
ded in 2004. The following year, the European Centre for Disease
Control and Prevention (ECDC) was created as an EU-wide insti-
tution for public health (http://ecdc.europa.eu/), according to the
example of the USA. Most of the above centers provide carefully
assembled data and detailed reports on waterborne parasitic pro-
tozoan outbreaks to the public. In developing countries, however,
there continues to be a critical absence of governmental systems for
the documentation of protozoan infections or waterborne out-
breaks (Karanis et al., 2007; Baldursson and Karanis, 2011).
Although these institutional systems gather epidemiological data
on disease incidence attributable to the protozoan agents that
clearly can be waterborne, data collection and reporting on
waterborne incidents or outbreaks are not reported routinely, e.g.
Yoder et al. (2008). While waterborne gastroenteritis outbreaks of
various etiologies are typically reported in the literature (as sum-
marized here), virtually no organized system provides for identi-
fication let alone description and analysis of such events in poor
and developing regions. As a result, information regarding water-
borne parasitic protozoan outbreaks in developing countries is
insufficient. Epidemiological information and relation to water re-
ported from the organized systems listed above may be used to
estimate the impact of waterborne protozoan transmission in areas
lacking direct information.
Previously, two reviews regarding worldwide waterborne out-
breaks caused by parasitic protozoa have been published, which
updated the number of the worldwide outbreaks until 2011; one in
2007 in the Journal of Water and Health (Karanis et al., 2007:
15
Waterborne transmission of protozoan parasites: A worldwide re-
view of outbreaks and lessons learnt) examining a time period of
close to a hundred years from the beginning of the previous cen-
tury, and the other in 2011, in the journal Water Research for the
period of 2004e2011 (Baldursson and Karanis, 2011: Waterborne
transmission of protozoan parasites: Review of worldwide out-
breaks - An update 2004e2010). Therefore, the aim of the present
work is to update worldwide waterborne parasitic outbreaks that
occurred between 2011 and 2016. Given the clearly incomplete
picture of global waterborne incidence in published reports, effort
is given to project a worldwide distribution pattern.
2. Search
Τhe collection of data was based upon available global literature
sources. Literature search used the MEDLINE/PubMed and Scopus
databases, as well as available electronic data from surveillance
systems all over the globe, including the Centre for Disease Control
and Prevention (CDC) and the European Centre of Disease Pre-
vention and Control (ECDC). The collection of data entailing this
present review of waterborne parasitic protozoan outbreaks was
also based on the use of on line information from, Euro Surveillance
(published by ECDC), Canada Communicable Disease Report (CCDR
by PHAC), Morbidity and Mortality Weekly Report (MMWR by CDC)
and Public Health England's electronic gastrointestinal outbreak
surveillance system (eFOSS).
In the above electronic databases the terms “outbreak (and)
Cryptosporidium”, “outbreak (and) cryptosporidiosis”, “outbreak
(and) Giardia”, “outbreak (and) giardiasis”, “outbreak (and) Cyclo-
spora”, “outbreak (and) Blastocystis”, “outbreak (and) Entamoeba”,
“outbreak (and) Acanthamoeba”, “outbreak (and) Amoebiasis”,
“outbreak (and) Toxoplasma”, “outbreak (and) microsporidia”,
“outbreak (and) Sarcocystis”, “outbreak (and) Naegleria”, “outbreak
(and) Balantidium coli”, “outbreak (and) Isospora” were applied and
the listed articles critically reviewed.
2.1. Outbreaks reported between 2011 and 2016 and analysis of
results
In the five year period between January 2011 and December
2016, 381 waterborne outbreaks of parasitic protozoan diseases
were reported worldwide that appeared in the online databases.
Tables 1 and 2 present a summary of the outbreaks. These tables
also include a few waterborne outbreaks that occurred before 2011
but were published at a later time and therefore were not included
in the aforementioned reviews of 2007 and 2011.
Waterborne outbreaks of Cryptosporidium spp. are documented
in Table 1, whereas Table 2 consists of worldwide waterborne
outbreaks caused by Giardia spp.. Both tables specify the parame-
ters of place (region and country), time (month and year), as well as
estimated and laboratory-confirmed cases in brackets, if denoted in
the original article. For each outbreak, the suspected cause and the
key reference is annotated.
Waterborne outbreaks reported worldwide as compiled in this
review (Tables 1 and 2), were heavily skewed to two regions, North
America and Australasia, Fig. 1. The majority of the reported out-
breaks (63%, or 239 outbreaks) had Cryptosporidium spp. as their
etiological agent, while Giardia spp. was the cause in 37% (142) of
them (Tables 1 and 2). No other protozoa were reported as the
causative agents of parasitic protozoan waterborne outbreaks be-
tween the years 2011e2016. A single outbreak due to contamina-
tion of drinking water by Cyclospora cayetanensis took place in
Puerto Rico in 2008 but was not reported until later (Brunkard et al.,
2011), and is included here as it was not reported in time for the
previous reviews.
16 A. Efstratiou et al. / Water Research 114 (2017) 14e22

Table 1
List of worldwide waterborne outbreaks caused by Cryptosporidium spp.

Month/year Location/country Etiological agent Est. cases, Suspected cause Key reference
1
outbreaks

August 2004a Ohio, USA C. hominis IdA15G1 150 Public swimming pool Cope et al. (2015)
February 2008a Sydney, Australia C. hominis IbA10G2 [31] Public swimming pool Mayne et al. (2011)
JuneeJuly 2008a Northhamp-tonshire, C. cuniculus 422 [23] Public water supply Puleston et al. (2014)
UK
July 2008a Texas, USA C. hominis IaA28R4, [112] Lake contaminated by human diarrheal Canteyet al. (2012)
IaA15R3 fecal incidents
September 2008a Lake Michigan, USA Cryptosporidium and 41 [4] runoff containing sewage being Serdarevic et al. (2012)
Giardia released into the lake
2007e2008a USA 39 unknown spp, 14 C. 60 outbreaks, 58 outbreaks associated with treated, 2 Hlavsa et al., (2011)
hominis, 7 C. parvum 12,154 cases outbreaks associated with untreated
recreational water
January and April New South Wales, C. hominis IbA10G2 1141 public swimming pool Waldron et al. (2011)
2009a Australia
March and April Norway C. parvum 74 [11] not definitively, but water could not be Rim
seliene et al. (2011)
2009a excluded
September 2007 Shanghai, China C. hominis IaA14R4, [38] hospital outbreak, multiple pathogens Feng et al. (2012),
eOctober 2009a IdA19 present, possible waterborne Wang et al. (2013)
transmission
January 2010a Vermont, USA Cryptosporidium sp. 34 Private well contamination at vacation Centers for Disease Control and
rental house Prevention (2013)
July 2010a Pennsylvania USA Cryptosporidium sp. 10 Contamination of well at private Centers for Disease Control and
residence Prevention (2013)
September 2010a Wales, UK C. hominis 48 Public swimming pool McCann et al. (2014)
October 2010a South East England, UK C. hominis 30 [19] Community swimming pool Chalmers (2012)
November 2010a €
Ostersund, Sweden C. hominis z27,000 [186] Drinking water, insufficient municipal Widerstro€m et al. (2014)
IbA10G2 water treatment plant
December 2010a Niagara region, Canada C. hominis 12 offline ultraviolet disinfection system at Hopkins et al. (2013)
recreational water park
October 2010a Ireland Cryptosporidium sp. 1 Travel related waterborne outbreak Health Protection Surveillance
Centre, Ireland, 2011
2010a New Zealand Cryptosporidium spp. 11 outbreaks, 29 73.2% untreated drinking-water supply, Institute of Environmental
cases 16.1% inadequately treated water Science and Research Ltd (ESR),
supply, 1.8% recent or ongoing New Zealand, 2010
treatment failure, 1.8% source water
quality inferior to normal (percentages
of a total of 56 waterborne outbreaksb)
2009e2010a USA Cryptosporidium spp. 27 outbreaks, 422 24 outbreaks associated with treated Hlavsa et al. (2014)
cases and 3 outbreaks associated with
untreated recreational water.
April 2011 Skellefteå, Sweden C. hominis 20,000 Surface waterworks lacked sufficient Guzman-Herrador et al. (2015),
barriers for parasites Rehn et al. (2015)
June 2011 Indiana & Michigan, C. parvum 20 [3] Direct contact with calves or water Centers for Disease Control and
USA Prevention (2012)
2011 Ireland Cryptosporidium sp. 6 [2] waterborne transmission could not be Health Protection Surveillance
definitively out ruled as the initial Centre, Ireland, 2012
source of the infection
2011 New Zealand Cryptosporidium spp. 7 outbreaks, 19 80% untreated drinking-water supply, Institute of Environmental
cases 37.8% inadequately treated water Science and Research Ltd (ESR),
supply, 13.3% source water quality New Zealand, 2011
inferior to normal (percentages relate to
a total number of 45 waterborne
outbreaksb)
2011 UK Cryptosporidium spp. 3 outbreaks Swimming or similar pools PHE Gastrointestinal Infections
Data 2013
May 2012 Seoul, Republic of Korea C. parvum 126 [3] Tap water contaminated by a sewage Moon et al. (2013)
leak from aged pipelines
November Broome, Western C. hominis IbA10G2 [18] Public swimming pool Ng-Hublin et al. (2015)
eDecember Australia
2012
2012 Ireland Cryptosporidium sp. 12 Public water supply Health Protection Surveillance
Centre, Ireland, 2013
2012 New Zealand Cryptosporidium spp. 19 outbreaks, 64 72.5% untreated water, 29.4% Institute of Environmental
cases inadequately treated water supply Science & Research Ltd (ESR),
(percentages relate to a total number of New Zealand, 2012
56 waterborne outbreaksb)
2012 UK Cryptosporidium spp. 9 outbreaks Swimming or similar pools PHE Gastrointestinal Infections
Data 2013
2011e2012 USA Cryptosporidium spp. 37 outbreaks, 890 36 outbreaks associated with treated Hlavsa et al. (2015)
cases and 1 outbreak associated with
untreated recreational water.
July 2013 Halle (Saale), Germany C. hominis IbA9G2 [167] River Saale overflowed the floodplain, Gertler et al. (2015)
parts of the city centre and damaged
sewage system
 A. Efstratiou et al. / Water Research 114 (2017) 14e22 17

Table 1 (continued )

Month/year Location/country Etiological agent Est. cases, Suspected cause Key reference
1
outbreaks

August 2013 Oregon, USA C. parvum IIaA15G2R1 2780 City water treatment facility DeSilva et al. (2016)
chlorinated but not filtered water.
2013 Ireland Cryptosporidium spp. 3 community Contamination of drinking and Health Protection Surveillance
outbreaks (29 swimming pool water, respectively Centre, Ireland, 2014
cases), 2
swimming pool
out-breaks (5
cases)
2013 New Zealand Cryptosporidium spp. 21 outbreaks, 66 77.4% untreated water, 40.3% Institute of Environmental
Giardia & Crypto cases inadequately treated water supply Science and Research Ltd (ESR),
implicated in 1 (percentages relate to a total number of New Zealand, 2013
outbreak (2 cases) 56 waterborne outbreaksb).
2013 UK Cryptosporidium spp. 6 outbreaks Swimming or similar pools PHE Gastrointestinal Infections
Data 2013
2014 Ireland Cryptosporidium spp. 5 Swimming pool HealthProtection Surveillance
Centre, Ireland, 2015
2014 New Zealand Cryptosporidium spp. 10 outbreaks, 26 92.9% untreated water, 21.4% ESR, New Zealand, 2014
cases inadequately treated water supply
(percentages relate to a total number of
56 waterborne outbreaksb)

Total this review 239 total outbreaks reported 65,540 total cases reported
1
Note: ND ¼ no data; Numbers in bold indicate more than a single outbreak.
[ ]: number of laboratory confirmed cases.
a
Outbreaks occurred before 2011, but were published after 2010 and are not included in the review of Baldursson and Karanis (2011).
b
For some waterborne outbreaks more than one contributing factor was recorded.

Surprisingly, nearly a half (49% or 188 outbreaks) of the reported
worldwide waterborne outbreaks caused by parasitic protozoa
were reported in Australia and New Zealand. A total of 185 (48%)
outbreaks were reported in New Zealand alone, with 3 (less than
1%) in Australia (Tables 1 and 2). The waterborne outbreaks on the
American continent amount to almost 41% (155) of the worldwide
waterborne outbreaks, all but one of which occurred in the USA
(Tables 1 and 2).
Europe contributed with 9% (35) of worldwide waterborne
outbreak reports. The distribution within the European countries
was: Ireland 2.4% (9) of worldwide waterborne outbreaks, the UK
5.5% (21) and at least 1.3% (5) in continental Europe (Norway 1,
Sweden 2, and Belgium and Germany from one each) (Tables 1 and
2). In Asia, only three (1%) waterborne parasitic protozoan disease
outbreaks were reported, two from the Republic of Korea and one
in China.
Among the documented outbreaks, 82% (314) were character-
ized by multiple modes of transmission, including untreated water
supplies, contaminated water sources, failures in treatment pro-
cessing, contamination of reservoirs or post treatment contami-
nation. In about 14% (55) of the reported outbreaks, the source of
infection was identified as recreational water, primarily due to
contamination with Cryptosporidium spp. (48 outbreaks), with the
recreational water source usually being a public/community
swimming pool. In 7 of the reported outbreaks, the source was
water intended for drinking, contaminated with a protozoan
pathogen. Finally, in 1.3% (5) of the reported outbreaks the way of
transmission was either not determined or not mentioned.
Regarding the species of the infectious agents involved, the
epidemiological investigations of only 38 Cryptosporidium out-
breaks during 2011e2016 lead to a successful isolation and iden-
tification of the causative agent (see Table 1). This is a long-standing
problem in outbreak investigations due to the perpetrating occur-
rence preceding occurrence of putatively resulting infections.
Hence sampling at a minimum of days if not weeks after the fact,
causative conditions are rarely continuing and therefore not iden-
tifiable. Analysis of patient samples may provide the common
infecting agent. Three different Cryptosporidium species were
recognized, C. hominis, C. parvum and C. cuniculus, with C. hominis
having been identified as the etiological agent in 26 outbreaks,
C. parvum in 11 and C. cuniculus in just one. On the other hand, all 19
outbreaks where the Giardia species was reported were either due
to G. intestinalis (17 outbreaks) or G. lamblia (2 outbreaks). Infor-
mation on the occurrence in water of other protozoan pathogens,
e.g. Cyclospora cayetanensis, Toxoplasma gondii, Isospora belli,
Balantidium coli, Blastocystis hominis, Entamoeba histolytica and
other free-living amoebae (FLA), has been described (Plutzer and
Karanis, 2016) although no waterborne outbreaks have been spe-
cifically attributed to these organisms.
2.2. Current and future challenges
During a period of over a hundred years, from the start of the
last century until 2004, a total of 325 waterborne protozoan para-
sitic outbreaks were reported worldwide (Karanis et al., 2007). In a
considerably shorter period of time, between 2004 and 2010, 199
reports of waterborne outbreaks of parasitic protozoa were pub-
lished (Baldursson and Karanis, 2011). This current third systematic
review of reported waterborne outbreaks of protozoan diseases
around the world adds to understanding their current distribution
pattern and evaluating the global disease burden. The present
survey compiled a total of 381 outbreak reports during the last six
years. This is an apparent increase in the number of reported out-
breaks when compared with the previous reviews of Baldursson
and Karanis (2011), where 199 outbreaks during a 7-year period
(2004e2011) were reported, and an even bigger increase from the
325 outbreaks reported by Karanis et al. (2007) throughout the
course of the previous century.
The compiled reports summarized here including those
compiled previously by Karanis et al. (2007) and by Baldursson and
18 A. Efstratiou et al. / Water Research 114 (2017) 14e22

Table 2
List of worldwide waterborne outbreaks caused by Giardia spp.

Month/year Location/country Etiological agent Est. cases, Suspected cause Key reference
1
outbreaks

August 2007a Colorado, USA G. intestinalis 13 Outbreak associated with water not Brunkard et al. (2011)
intended for drinking from park
September 2008a Illinois, USA Shigella sonnei, 41 Community water system Brunkard et al. (2011)
Cryptosporidium,
Giardia
2007e2008a USA G. intestinalis, 1 4 outbreaks, 38 all outbreaks associated with treated Hlavsa et al., (2011)
outbreak with both cases recreational water
C. hominis,
G. intestinalis
May 2009a Idaho, USA G. intestinalis 7 contamination of community well at Private Centers for Disease Control and
residence Prevention (2013)
a
August 2009 Utah, USA G. intestinalis 8 cross-connection between potable and non- Centers for Disease Control and
potable water sources resulting in backflow Prevention (2013)
August 2009a New York, USA G. intestinalis 26 Contaminated natural water- Source at Centers for Disease Control and
spring public outdoor area Prevention (2013)
September 2009a New York, USA Giardia spp. [36] fecal contamination of private roadside Bedard et al. (2016)
spring/not approved for drinking water
a
April 2010 Jeollabuk province, G. lamblia 25 [7] provisional water supply tube destroyed Cheun et al. (2013)
Republic of Korea under a building construction and
contaminated
June 2010a Nevada, USA G. intestinalis 20 contaminated irrigation puddle/canal/ Centers for Disease Control and
swamp at public outdoor area Prevention (2013)
June 2010a Minnesota, USA G. intestinalis 6 transient non-community Centers for Disease Control and
well state park Prevention (2013)
a
December 2010 Hemiksem, G. lamblia, 222 [3] point-source contamination of tap water Braeye et al. (2015)
Belgium Campylobacter, with river water
Norovirus,
Rotavirus
2010a New Zealand Giardia spp. 29 outbreaks, 113 Untreated drinking-water supply (73.2%), Institute of Environmental Science
cases inadequately treated water supply (16.1%), and Research Ltd (ESR), New
recent or ongoing treatment failure (1.8%) Zealand, 2010
and source water quality inferior to normal
(1.8%). Percentages relate to a total number
of 56 waterborne outbreaksb
2009e2010a USA G. intestinalis 7 treated recreational water Hlavsa et al. (2014)
May 2011 Colorado, USA G. intestinalis 2 contaminated river/stream water at camp/ Beer et al. (2015a,b)
cabin
November 2011 Utah, USA G. intestinalis 20 contaminated river/stream at public Beer et al. (2015a,b)
outdoor area
2011 New Zealand Giardia spp. 20 outbreaks, 62 80% untreated drinking-water supply, 37.8% Institute of Environmental Science
cases inadequately treated water supply, 13.3% and Research Ltd (ESR), New
source water quality inferior to normal Zealand, 2011
(percentages relate to a total number of 45
waterborne outbreaksb)
February 2012 Idaho, USA G. intestinalis 4 contaminated river/stream water at Beer et al. (2015a,b)
national forest
May 2012 Idaho, USA G. intestinalis, 7 contaminated river, stream, well water at Beer et al. (2015a,b)
Campylobacter community
June 2012 Alaska, USA G. intestinalis 21 [4] contaminated spring, well or river water, at Beer et al. (2015a,b)
camp.
August 2012 Utah, USA G. intestinalis 28 [5] Change in pressure in the neighborhood Beer et al. (2015a,b)
distribution allowed contaminated well
water to flow into the drinking water
2012 New Zealand Giardia spp. 19 outbreaks, 65 72.5% untreated water, 29.4% inadequately Institute of Environmental Science
cases treated water supply and Research Ltd (ESR), New
(percentages relate to a total number of 56 Zealand, 2012
waterborne outbreaksb)
2011e2012 USA G. intestinalis 3 outbreaks, 34 1 outbreak associated with treated and 2 Hlavsa et al. (2015)
cases with untreated recreational water
G. intestinalis, 125 cases Untreated recreational water
Norovirus
2013 New Zealand Giardia spp. Both 26 outbreaks, 100 77.4% untreated water, 40.3% inadequately ESR, New Zealand, 2013
Giardia & Crypto cases treated water supply (percentages relate to
were implicated in a total number of 56 waterborne
1 outbreak (2 cases) outbreaksb).
2014 New Zealand Giardia spp. 23 outbreaks, 77 92.9% untreated water, 21.4% inadequately ESR, New Zealand, 2014
cases treated water supply (percentages relate to
a total number of 56 waterborne
outbreaksb)

Total this review 142 total outbreaks reported 1110 total cases reported
1
Note: ND ¼ no data; Numbers in bold indicate more than a single outbreak.
[ ]: number of laboratory confirmed cases.
a
Outbreaks occurred before 2011, but were published after 2010 and are not included in the review of Baldursson and Karanis (2011).
b
For some waterborne outbreaks more than one contributing factor was recorded.
 A. Efstratiou et al. / Water Research 114 (2017) 14e22 19

Fig. 1. Global distribution of reported waterborne cryptosporidiosis and giardiasis outbreaks summarized from the literature in this review.

Fig. 2. Waterborne Giardia and Cryptosporidium outbreaks and cases reported in the literature, 1954e2016.

Karanis (2011), include 293 of giardiasis comprising 86,938 cases,
Fig. 2. One outbreak alone accounted for an estimated 50,000 cases
(Portland, Oregon, 1954, Veasie, 1969 and Meyer, 1973). Except for
the 1954 outbreak, not published until 1969, sporadic reports of
waterborne Giardia outbreaks began to appear the mid-1960s,
continuing at the rate of 1e2 per year until about 2005. After that
period an increase in the frequency of outbreak reports was
apparent predominantly in non-community water systems or from
recreational water contact. The compiled reports include 432 of
waterborne cryptosporidiosis, comprising 577,242 cases, Fig. 2. One
outbreak alone accounted for an estimated 403,000 cases (Mil-
waukee, Wisconsin, 1993, MacKenzie et al., 1994). The earliest
waterborne Cryptosporidium outbreak was reported in 1983
(Galbraith et al., 1987). Current knowledge of human cryptospo-
ridiosis epidemiology and of the ecology and distribution of Cryp-
tosporidium in the environment indicates that waterborne
cryptosporidiosis has a history as long as mankind. Documentation
and reporting of such outbreaks closely follows the development in
the mid-1980's of analytical methods and water sample analysis
technology e.g. Stibbs and Ongerth (1986) and Ongerth and Stibbs
(1987). An increase in the number of waterborne cryptosporidi-
osis outbreaks has been apparent since the early 2000's. This par-
allels the increased surveillance and investigation of cases
associated with small (non-community) water systems and
20 A. Efstratiou et al. / Water Research 114 (2017) 14e22
recreational water contact similar to that observed for waterborne
giardiasis, Fig. 2.
This rising trend of waterborne parasitic protozoan outbreak
reports agrees with previous findings regarding the increasing
number of reports of water-associated infectious disease outbreaks
(Yang et al., 2012), and has been attributed to the significant ad-
vances in data reporting and surveillance systems being set up in
many developed countries (Baldursson and Karanis, 2011). The
increase in reports does not necessarily indicate either a funda-
mental increase that might suggest worsening conditions in the
regions from which the vast majority of reports originate. The high
proportion of outbreak reports from New Zealand underscores the
influence of reporting efficiency.
This study supports previous observations that such improved
reporting from regions of high economic and sanitation status
contributes to a distorted picture of the global conditions. Devel-
oped regions have a higher rate of reported parasitic waterborne
outbreaks despite higher infection prevalence and likely higher
outbreak incidence in developing countries (Baldursson and
Karanis, 2011). It should be clear that those countries probably
most affected by both of the parasites are not able to identify or
provide any reports of outbreak events due to the lack of surveil-
lance systems.
Public health and disease outbreak monitoring requires reliable
surveillance and notification systems. However, most surveillance
and notification systems are affected by a degree of underestima-
tion, an observation which is especially true of infectious diseases
because of common characteristics such as an absence of symptoms
and self-limiting courses of disease (Gibbons et al., 2014). A study of
underreporting of gastrointestinal disease in Ontario, Canada esti-
mated that there were approximately 285 community cases for
each case reported to the province (Majowicz et al., 2005). It is
important to mention that reporting efforts and efficiency vary
from country to country and pathogen to pathogen, depending on
many factors, but most notably, the availability of research and
surveillance resources and the epidemiological characteristics of
causative agents (Yang et al., 2012). In developing countries, where
gastrointestinal infections are suspected to be grossly under-
reported, it is at least partly due to their endemic characteristics
(Ashbolt, 2004). Many developed countries put major focus on
bacterial and viral infections, and therefore only a few or no para-
sitic protozoa are included in operational surveillance systems
(Fletcher et al., 2012). Even in the US, which has arguably the most
developed national system of waterborne disease surveillance in
the world (Leclerc et al., 2002), and where reporting of crypto-
sporidiosis has been on the rise (Painter et al., 2016), completeness
of notifiable infectious disease reporting was found to vary greatly,
and depended on the disease (Doyle et al., 2002). Europe is no
exception, as in the most recently published Annual Epidemiolog-
ical Report on Communicable Diseases for 2014, ECDC found it
likely that many infectious diseases continue to be underreported
in most of the EU/EEA countries, despite their surveillance being
mandatory, e.g. three countries do not have complete surveillance
systems for Giardia and nine out of the 26 countries failed to report
data on cryptosporidiosis (www.ecdc.europa.eu, Caccio  and
Chalmers, 2016). Even though underreporting constitutes a uni-
versal problem having its basis on each country's socioeconomic
status and investment of research resources (Yang et al., 2012),
there has been an encouraging increase in the number of reports of
water-associated infectious disease outbreaks all over the world
since the early 1990s (Yang et al., 2012), as well as a rise in reported
outbreaks of cryptosporidiosis and giardiasis in particular (Craun
et al., 2005).
For the last 35 years, enteric protozoa have been the leading
cause of reported waterborne disease outbreaks of a known
etiologic agent (Moe et al., 2007). Both Giardia cysts and Crypto-
sporidium oocysts are transmitted through water, and have been
shown to be universally present although widely undetected in raw
water samples throughout the USA (Ongerth, 2013a, 2016). Giardia
infection has been recognized as the number one intestinal para-
sitic disease affecting humans in the USA (Kappus et al., 1994). Like
Cryptosporidium, Giardia has been shown to be universally
distributed but underdetected due to poorly planned and imple-
mented monitoring (Ongerth, 2013b). Outbreaks due to both or-
ganisms have been heavily associated with consumption of surface
water or groundwater that has been contaminated (Adam et al.,
2016; Hlavsa et al., 2011, 2015). Cryptosporidiosis is the most
frequently reported gastrointestinal illness in outbreaks associated
with treated recreational water in the US (Yoder and Beach, 2007;
Hlavsa et al., 2015). This can be partly attributed to an unusually low
infectious dose; ingestion of as few as 10 Giardia cysts or a single
Cryptosporidium oocyst might be enough to cause illness (www.cdc.
gov, Haas and Rose, 1994; Karanis and Schoenen, 2001), a factor
contributing to the US Environmental Protection Agency (EPA)
drinking water maximum contaminant level goal of 0 for both
Giardia and Cryptosporidium (www.epa.gov, Pandit and Kumar,
2015).
In developed countries worldwide, nearly 2% of adults and 6e8%
of children are infected with Giardia, while one third of the people
in the developing world have had giardiasis (www.cdc.gov).
Furthermore, Cryptosporidium is the second most common water-
borne pathogen worldwide, with an estimated 30,000 cases of
cryptosporidiosis occurring annually in the USA (Yoder et al.,
2012b), and is identified in 2% of all diarrhea cases in developed
countries compared to a 7% rate in children and 14% in AIDS pa-
tients (Chen et al., 2002; Kotloff et al., 2013). The high morbidity
caused by Giardia and Cryptosporidium in developing countries has
been attributed to factors including the multiple exposure routes
reflecting living and sanitation conditions, sources of organisms
and cycling through domestic animals, contamination of the
aquatic ecosystem by the high environmental burden, and resis-
tance of the (oo)cysts against common water disinfectants, infec-
tion (Slifko et al., 2000). Furthermore, severe weather events,
including heavy rainfall and river flooding, are on the rise world-
wide, and are likely to cause epidemics of waterborne gastroen-
teritis (Gertler et al., 2015).
3. Conclusions
The continued presence of Cryptosporidium and Giardia in water
systems represents an alarming significant health risk. While
literature reports suggest an increase in the number of waterborne
parasitic outbreaks due to improved surveillance and reporting
systems in developed countries, the true magnitude of waterborne
protozoan illness in regions most affected are still neglected and
poorly described. This review provides an overview of published
waterborne parasitic protozoan outbreaks in worldwide databases
and those reported in single studies. This serves to highlight the
deficiency in our knowledge regarding the frequency and extent of
the undiagnosed outbreaks worldwide. The establishment of sur-
veillance systems in developing countries would be a decisive first
step in combating parasitic protozoa and improving the health of
the population. To this end, development of reliable and affordable
diagnostic tools for the detection as well as molecular character-
ization of the causative organisms should be a priority. Ideally, in-
ternational collaboration against waterborne pathogenic protozoa
in the form of standardized reporting system and the establishment
of ‘National Working Nets for Waterborne Parasites ¼ NWNWP’
should materialize in the near future, especially in the face of
adverse climatic events driven by climate change, which are
 A. Efstratiou et al. / Water Research 114 (2017) 14e22
currently on the rise globally and pose a threat of massive water-
borne infectious disease outbreaks.
Acknowledgements
We acknowledge the funding support from the One Thousand
Talents Plan of the Chinese Government (NO. WQ2013630172).
References
Adam, E.A., Yoder, J.S., Gould, L.H., Hlavsa, M.C., Gargano, J.W., 2016. Giardiasis
outbreaks in the United States, 1971e2011. Epidemiol. Infect. 1e12.
Ashbolt, N.J., 2004. Microbial contamination of drinking water and disease out-
comes in developing regions. Toxicology 198 (1), 229e238.
Baldursson, S., Karanis, P., 2011. Waterborne transmission of protozoan parasites:
review of worldwide outbreaksean update 2004e2010. Water Res. 45 (20),
6603e6614.
Bedard, B.A., Elder, R., Phillips, L., Wachunas, M.F., 2016. Giardia outbreak associated
with a roadside spring in Rensselaer County, New York. Epidemiol. Infect. 144,
3013e3016.
Beer, K.D., Gargano, J.W., Roberts, H.E., Hill, V.R., Garrison, L.E., Kutty, P.K.,
Hilborn, E.D., Wade, T.J., Fullerton, K.E., Yoder, J.S., 2015a. Outbreaks associated
with drinkingdUnited States, 2011e2012. MMWR Morb. Mortal. Wkly. Rep. 64
(31), 842e848.
Beer, K.D., Gargano, J.W., Roberts, V.A., Reses, H.E., Hill, V.R., Garrison, L.E.,
Kutty, P.K., Hilborn, E.D., Wade, T.J., Fullerton, K.E., Yoder, J.S., 2015b. Outbreaks
associated with environmental and undetermined water exposuresdUnited
States, 2011e2012. MMWR Morb. Mortal. Wkly. Rep. 64 (31), 849e851.
Braeye, T., De Schrijver, K., Wollants, E., Van Ranst, M., Verhaegen, J., 2015. A large
community outbreak of gastroenteritis associated with consumption of drink-
ing water contaminated by river water, Belgium, 2010. Epidemiol. Infect. 143
(04), 711e719.
Brunkard, J.M., Ailes, E., Roberts, V.A., Hill, V., Hilborn, E.D., Craun, G.F.,
Rajasingham, A., Kahler, A., Garrison, L., Hicks, L., Carpenter, J., 2011. Surveillance
for waterborne disease outbreaks associated with drinking waterdUnited
States, 2007e2008. MMWR Surveill. Summ. 60 (12), 38e68.
Caccio , S.M., Chalmers, R.M., 2016. Human cryptosporidiosis in Europe. Clin.
Microbiol. Infect. 22 (6), 471e480.
Cantey, P.T., Kurian, A.K., Jefferson, D., Moerbe, M.M., Marshall, K.,
Blankenship, W.R., Rothbarth, G.R., Hwang, J., Hall, R., Yoder, J., Brunkard, J.,
Johnston, S., Xiao, L., Hill, V.R., Sarisky, J., Zarate-Bermudez, M.A., Otto, C.,
Hlavsa, M.C., 2012. Outbreak of cryptosporidiosis associated with a man-made
chlorinated lake-Tarrant County, Texas, 2008. J. Environ. Health 75 (4), 14.
Centers for Disease Control and Prevention (CDC), 2012. Outbreak of cryptospo-
ridiosis associated with a firefighting response-Indiana and Michigan, June
2011. MMWR Morb. Mortal. Wkly. Rep. 61 (9), 153.
Centers for Disease Control and Prevention (CDC), 2013. Surveillance for water-
borne disease outbreaks associated with drinking water and other nonrecrea-
tional water-United States, 2009e2010. MMWR Morb. Mortal. Wkly. Rep. 62
(35), 714.
Chalmers, R.M., 2012. Waterborne outbreaks of cryptosporidiosis. Ann. Ist. Super.
Sanit a 48 (4), 429e446.
Checkley, W., White, A.C., Jaganath, D., Arrowood, M.J., Chalmers, R.M., Chen, X.M.,
Fayer, R., Griffiths, J.K., Guerrant, R.L., Hedstrom, L., Huston, C.D., 2015. A review
of the global burden, novel diagnostics, therapeutics, and vaccine targets for
Cryptosporidium. Lancet Infect. Dis. 15 (1), 85e94.
Chen, X.M., Keithly, J.S., Paya, C.V., LaRusso, N.F., 2002. Cryptosporidiosis. N. Engl. J.
Med. 346 (22), 1723e1731.
Cheun, H.I., Kim, C.H., Cho, S.H., Ma, D.W., Goo, B.L., Na, M.S., Youn, S.K., Lee, W.J.,
2013. The first outbreak of giardiasis with drinking water in Korea. Osong Public
Health Res. Perspect. 4 (2), 89e92.
Cope, J.R., Prosser, A., Nowicki, S., Roberts, M.W., Roberts, J.M., Scheer, D.,
Anderson, C., Longsworth, A., Parsons, C., Goldschmidt, D., Johnston, S., 2015.
Preventing community-wide transmission of Cryptosporidium: a proactive
public health response to a swimming pool-associated outbreakeAuglaize
County, Ohio, USA. Epidemiol. Infect. 143 (16), 3459e3467.
Craun, G.F., Calderon, R.L., Craun, M.F., 2005. Outbreaks associated with recreational
water in the United States. Int. J. Environ. Health Res. 15 (4), 243e262.
DeSilva, M.B., Schafer, S., Scott, M.K., Robinson, B., Hills, A., Buser, G.L., Salis, K.,
Gargano, J., Yoder, J., Hill, V., Xiao, L., 2016. Community wide cryptosporidiosis
outbreak associated with a surface water-supplied municipal water system-
eBaker City, Oregon, 2013. Epidemiol. Infect. 144 (02), 274e284.
Doyle, T.J., Glynn, M.K., Groseclose, S.L., 2002. Completeness of notifiable infectious
disease reporting in the United States: an analytical literature review. Am. J.
Epidemiol. 155 (9), 866e874.
Feng, Y., Wang, L., Duan, L., Gomez-Puerta, L.A., Zhang, L., Zhao, X., Hu, J., Zhang, N.,
Xiao, L., 2012. Extended outbreak of Cryptosporidiosis in a pediatric hospital,
China. Emerg. Infect. Dis. 18 (2), 312e314.
Fletcher, S.M., Stark, D., Harkness, J., Ellis, J., 2012. Enteric protozoa in the developed
world: a public health perspective. Clin. Microbiol. Rev. 25 (3), 420e449.
Galbraith, N.S., Barrett, N.J., Stanwell-Smith, R., 1987. Water and disease after
Croydon: a review of water-borne and water-associated disease in the UK 1937-
21
86. J. Inst. Water Environ. Manag. 1, 7e21.
Gertler, M., Dürr, M., Renner, P., Poppert, S., Askar, M., Breidenbach, J., Frank, C.,
Preußel, K., Schielke, A., Werber, D., Chalmers, R., 2015. Outbreak of Crypto-
sporidium hominis following river flooding in the city of Halle (Saale), Germany,
August 2013. BMC Infect. Dis. 15 (1), 1.
Gibbons, C.L., Mangen, M.J.J., Plass, D., Havelaar, A.H., Brooke, R.J., Kramarz, P.,
Peterson, K.L., Stuurman, A.L., Cassini, A., Fe vre, E.M., Kretzschmar, M.E., 2014.
Measuring underreporting and under-ascertainment in infectious disease
datasets: a comparison of methods. BMC Public Health 14 (1), 1.
Guzman-Herrador, B., Carlander, A., Ethelberg, S., de Blasio, B.F., Kuusi, M., Lund, V.,
Lo€ fdahl, M., MacDonald, E., Nichols, G., Scho €nning, C., Sudre, B., 2015. Water-
borne outbreaks in the Nordic countries, 1998 to 2012. Euro Surveill. 20, 1e10.
Haas, C.N., Rose, J.B., 1994. Reconciliation of microbial risk models and outbreak
epidemiology: the case of the Milwaukee outbreak. Proc. Water Works Assoc.
517e523 (Denver: Am. Water Works Assoc.).
Health Protection Surveillance Center (HPSC), 2011. Epidemiology of Cryptospo-
ridiosis in Ireland 2010.
Health Protection Surveillance Center (HPSC), 2012. Epidemiology of Cryptospo-
ridiosis in Ireland 2011.
Health Protection Surveillance Center (HPSC), 2013. Epidemiology of Cryptospo-
ridiosis in Ireland 2012.
Health Protection Surveillance Center (HPSC), 2014. Epidemiology of Cryptospo-
ridiosis in Ireland 2013.
Health Protection Surveillance Center (HPSC), 2015. Epidemiology of Cryptospo-
ridiosis in Ireland 2014.
Hlavsa, M.C., Roberts, V.A., Anderson, A.R., Hill, V.R., Kahler, A.M., Orr, M.,
Garrison, L.E., Hicks, L.A., Newton, A., Hilborn, E.D., Wade, T.J., 2011. Surveillance
for waterborne disease outbreaks and other health events associated with
recreational waterdUnited States, 2007e2008. MMWR Surveill. Summ. 60 (12),
1e32.
Hlavsa, M.C., Roberts, V.A., Kahler, A.M., Hilborn, E.D., Mecher, T.R., Beach, M.J.,
Wade, T.J., Yoder, J.S., 2015. Outbreaks of illness associated with recreational
waterdUnited States, 2011e2012. MMWR Morb. Mortal. Wkly. Rep. 64 (24),
668e672.
Hlavsa, M.C., Roberts, V.A., Kahler, A.M., Hilborn, E.D., Wade, T.J., Backer, L.C.,
Yoder, J.S., 2014. Recreational water-associated disease outbreaksdUnited
States, 2009e2010. MMWR Morb. Mortal. Wkly. Rep. 63 (1), 6e10.
Hopkins, J., Hague, H., Hudgin, G., Ross, L., Moore, D., 2013. An outbreak of Cryp-
tosporidium at a recreational water park in Niagara Region, Canada. J. Environ.
Health 75 (9), 28e33.
Huang, D.B., White, A.C., 2006. An updated review on Cryptosporidium and Giardia.
Gastroenterol. Clin. North Am. 35 (2), 291e314.
Institute of Environmental Science and Research Ltd (ESR), 2011a. Annual Summary
of Outbreaks in New Zealand 2010.
Institute of Environmental Science and Research Ltd (ESR), 2011b. Annual Summary
of Outbreaks in New Zealand 2011.
Institute of Environmental Science and Research Ltd (ESR), 2011c. Annual Summary
of Outbreaks in New Zealand 2012.
Institute of Environmental Science and Research Ltd (ESR), 2011d. Annual Summary
of Outbreaks in New Zealand 2013.
Institute of Environmental Science and Research Ltd (ESR), 2011e. Annual Summary
of Outbreaks in New Zealand 2014.
Kappus, K.D., Lundgren Jr., R.G., Juranek, D.D., Roberts, J.M., Spencer, H.C., 1994.
Intestinal parasitism in the United States: update on a continuing problem. Am.
J. Trop. Med. Hyg. 50 (6), 705e713.
Karanis, P., Schoenen, D., 2001. Biological test for the detection of low concentra-
tions of infectious Cryptosporidium parvum oocysts in water. Acta Hydroch.
Hydrob 29 (4), 242e245.
Karanis, P., Kourenti, C., Smith, H., 2007. Waterborne transmission of protozoan
parasites: a worldwide review of outbreaks and lessons learnt. J. Water Health 5
(1), 1e38.
Kotloff, K.L., Nataro, J.P., Blackwelder, W.C., Nasrin, D., Farag, T.H., Panchalingam, S.,
Wu, Y., Sow, S.O., Sur, D., Breiman, R.F., Faruque, A.S., 2013. Burden and aetiology
of diarrhoeal disease in infants and young children in developing countries (the
Global Enteric Multicenter Study, GEMS): a prospective, case-control study.
Lancet 382 (9888), 209e222.
Lanata, C.F., 2003. Studies of food hygiene and diarrhoeal disease. Int. J. Environ.
Health Res. 13 (Suppl. 1), S175eS183.
Leclerc, H., Schwartzbrod, L., Dei-Cas, E., 2002. Microbial agents associated with
waterborne diseases. Crit. Rev. Microbiol. 28 (4), 371e409.
MacKenzie, W.R., Hoxie, N.J., Proctor, M.E., Gradus, M.S., Blair, K.A., Peterson, D.E.,
Kazmierczak, J.J., Addiss, D.G., Fox, K.R., Rose, J.B., Davis, J.P., 1994. A massive
outbreak in Milwaukee of Cryptosporidium infection transmitted through the
public water supply. N. Engl. J. Med. 331, 161e167.
Majowicz, S.E., Edge, V.L., Fazil, A., McNab, W.B., Dore , K.A., Sockett, P.N., Flint, J.A.,
Middleton, D., McEwen, S.A., Wilson, J.B., 2005. Estimating the under-reporting
rate for infectious gastrointestinal illness in Ontario. Can. J. Public Health
178e181.
Mayne, D.J., Ressler, K.A., Smith, D., Hockey, G., Botham, S.J., Ferson, M.J., 2011.
A community outbreak of cryptosporidiosis in Sydney associated with a public
swimming facility: a case-control study. Interdiscip. Perspect. Infect. Dis.
341065.
McCann, R., Jones, R., Snow, J., Cleary, P., Burgess, S., Bothra, V., Chalmers, R.M., 2014.
An outbreak of cryptosporidiosis at a swimming clubecan rapid field epide-
miology limit the spread of illness? Epidemiol. Infect. 142 (01), 51e55.
22 A. Efstratiou et al. / Water Research 114 (2017) 14e22
Meyer, W.T., 1973. Epidemic giardiasis. A continued elusive entity. Rocky Mt. Med. J.
70, 48e49.
Moe, C.L., Hurst, C.J., Crawford, R.L., Garland, J.L., Lipson, D.A., Mills, A.L.,
Stetzenbach, L.D., 2007. Waterborne transmission of infectious agents. Man.
Environ. Microbiol. 222e248 (Ed. 3).
Moon, S., Kwak, W., Lee, S., Kim, W., Oh, J., Youn, S.K., 2013. Epidemiological char-
acteristics of the first water-borne outbreak of cryptosporidiosis in Seoul, Korea.
J. Korean Med. Sci. 28 (7), 983e989.
Ng-Hublin, J.S.Y., Hargrave, D., Combs, B., Ryan, U., 2015. Investigation of a swim-
ming pool-associated cryptosporidiosis outbreak in the Kimberley region of
Western Australia. Epidemiol. Infect. 143 (05), 1037e1041.
Ongerth, J.E., Stibbs, H.H., 1987. Identification of Cryptosporidium oocysts in river
water. Appl. Environ. Microbiol. 53 (4), 672e676.
Ongerth, J.E., 2013a. The LT2 Cryptosporidium data- what do they tell us about
Cryptosporidium in surface water in the USA? Environ. Sci. Technol. 47 (9),
4029e4038.
Ongerth, J.E., 2013b. ICR SS protozoan data site-by-siteda picture of Cryptospo-
ridium and Giardia in USA surface water. Environ. Sci. Technol. 47 (18),
10145e10154.
Ongerth, J.E., 2016. Cryptosporidium and Giardia in water: reassessment of occur-
rence and significance. J. Environ. Eng. 04016084. http://dx.doi.org/10.1061/
(ASCE)EE.1943-7870.0001161.
Painter, J.E., Gargano, J.W., Yoder, J.S., Collier, S.A., Hlavsa, M.C., 2016. Evolving
epidemiology of reported cryptosporidiosis cases in the United States,
1995e2012. Epidemiol. Infect. 144 (08), 1792e1802.
Pandit, A.B., Kumar, J.K., 2015. Clean water for developing countries. Annu. Rev.
Chem. Biomol. Eng. 6, 217e246.
Platts-Mills, J.A., Babji, S., Bodhidatta, L., Gratz, J., Haque, R., Havt, A.,
McCormick, B.J., McGrath, M., Olortegui, M.P., Samie, A., Shakoor, S., 2015.
Pathogen-specific burdens of community diarrhoea in developing countries: a
multisite birth cohort study (MAL-ED). Lancet Glob. Health 3 (9), e564ee575.
Plutzer, J., Karanis, P., 2016. Neglected waterborne parasitic protozoa and their
detection in water. Water Res. 101, 318e332.
Public Health England (PHE), 2015. Gastrointestinal Infections Data, Summary of
EFOSS Data, 2013.
Puleston, R.L., Mallaghan, C.M., Modha, D.E., Hunter, P.R., Nguyen-Van-Tam, J.S.,
Regan, C.M., Nichols, G.L., Chalmers, R.M., 2014. First recorded outbreak of
cryptosporidiosis due to Cryptosporidium cuniculus (formerly rabbit genotype)
following a water quality incident. J. Water Health 12 (1), 41e50.
Rehn, M., Wallensten, A., Widerstro € m, M., Lilja, M., Grunewald, M., Stenmark, S.,
Kark, M., Lindh, J., 2015. Post-infection symptoms following two large water-
borne outbreaks of Cryptosporidium hominis in Northern Sweden, 2010e2011.
BMC Public Health 15 (1), 1.
Rim
seliene, G., Vold, L., Robertson, L., Nelke, C., Søli, K., Johansen, Ø.H., Thrana, F.S.,
Nygård, K., 2011. An outbreak of gastroenteritis among schoolchildren staying
in a wildlife reserve: thorough investigation reveals Norway's largest crypto-
sporidiosis outbreak. Scand. J. Public Health 39 (3), 287e295.
Serdarevic, F., Jones, R.C., Weaver, K.N., Black, S.R., Ritger, K.A., Guichard, F.,
Dombroski, P., Emanuel, B.P., Miller, L., Gerber, S.I., 2012. Multi-pathogen
waterborne disease outbreak associated with a dinner cruise on Lake Michigan.
Epidemiol. Infect. 140 (04), 621e625.
Slifko, T.R., Smith, H.V., Rose, J.B., 2000. Emerging parasite zoonoses associated with
water and food. Int. J. Parasitol. 30 (12), 1379e1393.
Stanwell-Smith, R., Andersson, Y., Levy, D.A., 2003. National surveillance systems.
In: Hunter, P., Waite, M., Ronchi, E. (Eds.), Drinking Water and Infectious Dis-
eases: Establishing the Links. CRC Press and IWA Publishing, London.
Stibbs, H., Ongerth, J.E., 1986. Immunofluorescence detection of Cryptosporidium
oocysts in fecal smears. J. Clin. Microbiol. 24, 517e521.
Veasie, L., 1969. Epidemic giardiasis. N. Engl. J. Med. 281, 853.
Waldron, L.S., Ferrari, B.C., Cheung-Kwok-Sang, C., Beggs, P.J., Stephens, N.,
Power, M.L., 2011. Molecular epidemiology and spatial distribution of a water-
borne cryptosporidiosis outbreak in Australia. Appl. Environ. Microbiol. 77 (21),
7766e7771.
Wall, P.G., De Louvois, J., Gilbert, R.J., Rowe, B., 1996. Food poisoning: notifications,
laboratory reports, and outbreaks- where do the statistics come from and what
do they mean? Commun. Dis. Rep. CDR Rev. 6 (7), R93eR100.
Wang, L., Xiao, L., Duan, L., Ye, J., Guo, Y., Guo, M., Liu, L., Feng, Y., 2013. Concurrent
infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile
in children during a cryptosporidiosis outbreak in a pediatric hospital in China.
PLOS Negl. Trop. Dis. 7 (9), e2437.
Widerstro €m, M., Scho€nning, C., Lilja, M., Lebbad, M., Ljung, T., Allestam, G., Ferm, M.,
€rkholm, B., Hansen, A., Hiltula, J.I., Långmark, J., 2014. Large outbreak of
Bjo
Cryptosporidium hominis infection transmitted through the public water supply.
Swed. Emerg. Infect. Dis. 20 (4), 581e589.
Yang, K., LeJeune, J., Alsdorf, D., Lu, B., Shum, C.K., Liang, S., 2012. Global distribution
of outbreaks of water-associated infectious diseases. PLOS Negl. Trop. Dis. 6 (2),
e1483.
Yoder, J.S., Beach, M.J., Centers for Disease Control and Prevention (CDC), 2007.
Cryptosporidiosis surveillancedUnited States, 2003e2005. MMWR Surveill.
Summ. 56 (7), 1e10.
Yoder, J.S., Gargano, J.W., Wallace, R.M., Beach, M.J., 2012a. Giardiasis surveillan-
ceeUnited States, 2009e2010. MMWR Surveill. Summ. 61 (5), 13e23.
Yoder, J.S., Hlavsa, M.C., Craun, G.F., Hill, V., Roberts, V., Yu, P.A., Hicks, L.A.,
Alexander, N.T., Calderon, R.L., Roy, S.L., Beach, M.J., 2008. Surveillance for
waterborne disease and outbreaks associated with recreational water use and
other aquatic facility-associated health eventsdUnited States, 2005e2006.
MMWR Surveill. Summ. 57 (9), 1e29.
Yoder, J.S., Wallace, R.M., Collier, S.A., Beach, M.J., Hlavsa, M.C., Centers for Disease
Control and Prevention (CDC), 2012b. Cryptosporidiosis surveillancedUnited
States, 2009e2010. MMWR Surveill. Summ. 61 (5), 1e12.