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Waterborne transmission of protozoan

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Waterborne transmission of protozoan parasites: Review

of worldwide outbreaks e An update 2004e2010

Selma Baldursson, Panagiotis Karanis*

University of Cologne, Faculty of Medicine, Center of Anatomy, Institute II, Medical and Molecular Parasitology, Joseph-Stelzmann-Strasse 35,
D-50937 Cologne, Germany

article info abstract

Article history: The present update gives a comprehensive review of worldwide waterborne parasitic
Received 13 July 2011 protozoan outbreaks that occurred and were published globally between January 2004 and
Received in revised form December 2010. At least one hundred and ninety-nine outbreaks of human diseases due to
11 October 2011 the waterborne transmission of parasitic protozoa occurred and were reported during the
Accepted 12 October 2011 time period from 2004 to 2010. 46.7% of the documented outbreaks occurred on the
Available online 20 October 2011 Australian continent, 30.6% in North America and 16.5% in Europe. Cryptosporidium spp.
was the etiological agent in 60.3% (120) of the outbreaks, Giardia lamblia in 35.2% (70) and
Keywords: other protozoa in 4.5% (9). Four outbreaks (2%) were caused by Toxoplasma gondii, three
Contamination (1.5%) by Cyclospora cayetanensis. In two outbreaks (1%) Acanthamoeba spp. was identified as
Diarrhea the causative agent. In one outbreak, G. lamblia (in 17.6% of stool samples) and Cryptospo-
Protozoan parasites ridium parvum (in 2.7% of stool samples) as well as Entamoeba histolytica (in 9.4% of stool
Public health surveillance systems samples) and Blastocystis hominis (in 8.1% of stool samples) were detected. In those coun-
Waterborne disease outbreak (WBDO) tries that are likely affected most a lack of surveillance systems is noticeable. However,
Worldwide review countries that established surveillance systems did not establish an international stan-
dardization of reporting systems.
2011 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6603
2. Material and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6604
3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6604
4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6610
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6612
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6612

1. Introduction (Cotruva et al., 2004). They are one of the main reasons for 4
billion cases of diarrhea that causes annually 1.6 million
Waterborne parasitic protozoan diseases have a worldwide deaths (www.who.int) and 62.5 million Disability Adjusted
distribution and are, in both developed and developing Life Years (DALYs) worldwide (Wright and Gundry, 2009).
countries, reasons for epidemic and endemic human suffering Diarrhea belongs to the five most common disease causes of

* Corresponding author. Tel.: 49 221 478 5655; fax: 49 221 478 3808.
E-mail address: panagiotis.karanis@uk-koeln.de (P. Karanis).
0043-1354/$ e see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.watres.2011.10.013
 Author's personal copy
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death (www.who.int) and is responsible for 21% of deaths of
children younger than five years of age (Kosek et al., 2003). The
most prevalent waterborne parasitic infections producing
diarrhea are cryptosporidiosis and giardiasis, already the
appearance of infections caused by Giardia lamblia account
2.8  10^8 cases yearly (Lane and Lloyd, 2002). Other parasitic
protozoa with a waterborne transmission that cause human
infections are Toxoplasma gondii, Entamoeba histolytica, Acan-
thamoeba spp., Cyclospora cayetanensis, Microsporidia, Isospora,
Blastocystis hominis, Sarcocystis spp., Naegleria spp. and Balan-
tidium coli. Since most of these protozoa use the faecal-oral
way of transmission they can infect humans through
sewage and contamination of land and rivers by animal or
human feces (Lanata, 2003). Efficient sanitation and improved
water supplies are the main safety measures against parasitic
protozoan hazards. The United States created organizations
like the Center for Disease Control and Prevention (CDC) and
the US Environmental Protection Agency (USEPA) that
enforced waterborne disease outbreak surveillance since 1971
(WBDOSS). In 1980 Sweden established a surveillance system
(Stanwell-Smith et al., 2003) and in 1981 Japan started the
National Epidemiological Surveillance of Infectious Diseases
(NESID). The National Notifiable Diseases Surveillance System
(NNDSS) in Australia was founded in 1990, the Health
Protection Agency (HPA) of the United Kingdom in 2003, and
furthermore, the Public Health Agency of Canada (PHAC) in
2004. Following the example of the USA European Countries
created the European Center for Disease Control and Preven-
tion (ECDC) in 2005. From most of these centers highly quali-
fied information and documentations of waterborne parasitic
protozoan outbreaks are approachable. In developing coun-
tries, governmental systems to register incidence and preva-
lence of protozoan infections or waterborne outbreaks are not
established. Consequently there is a lack of documentation of
waterborne parasitic protozoan outbreaks in developing
countries.
In 2007, the Journal of Water and Health published a review
of worldwide waterborne outbreaks caused by parasitic
protozoa (Karanis et al., 2007: Waterborne transmission of
protozoan parasites: A worldwide review of outbreaks and
lessons learnt) which spans a time period of almost hundred
years from the beginning of the previous century. The aim of
the present work is to update worldwide waterborne outbreaks
of pathogenic protozoa during the time period of 2004e2011
and to figure out their worldwide distribution pattern.
2. Material and methods
For the collection of data a variety of global literature sources
was used. The research included articles from the databases
MEDLINE/PubMed, MEDPILOT and Scopus as well as available
electronic data from surveillance systems all over the world,
like the Center for Disease Control and Prevention (CDC) and
the European Center of Disease Prevention and Control
(ECDC). The collection of data entailing this present review of
waterborne parasitic protozoan outbreaks is based on a search
of the medical literature databases MEDLINE/PubMed, MED-
PILOT and Scopus, as well as on the use of electronic data from
Morbidity and Mortality Weekly Report (MMWR by CDC), Euro
Surveillance (published by ECDC), Canada Communicable
Disease Report (CCDR by PHAC), Communicable Disease
Report (CDR by HPA) and CRYPTNET (www.mednetvet.org).
In the named electronic databases the terms outbreak
(and) Cryptosporidium, outbreak (and) cryptosporidiosis,
outbreak (and) Giardia, outbreak (and) giardiasis, outbreak
(and) Cyclospora, 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 exerted and the listed articles critically
reviewed.
3. Results
During a time period of almost hundred years, between the
previous century and 2004, a number of 325 waterborne
protozoan parasitic outbreaks have been reported world-
wide (Karanis et al., 2007), while in the considerable shorter
time period of seven years, between 2004 and 2010, 199
reports of waterborne protozoan parasitic outbreaks were
published. Between January 2004 and December 2010, one
hundred and ninety-nine waterborne outbreaks of parasitic
protozoan diseases occurring during this time period have
been published worldwide and could be detected in the
considered databases. The outbreaks are summarized in
Tables 1e3.
Table 1 documents worldwide waterborne outbreaks
caused by Cryptosporidium spp., Table 2 shows worldwide
waterborne outbreaks caused by G. lamblia and Table 3
summarizes the worldwide waterborne outbreaks caused by
T. gondii, E. histolytica, Acanthamoeba spp., C. cayetanensis,
Microsporidia, Isospora, Blastocystis spp., Sarcocystis spp., Nae-
gleria spp. and Balantidium coli. Additional, Tables 1e3 point
out the parameters of time (month and year), place (region
and country), estimated cases and labor-confirmed cases in
brackets if denoted in the original article. For each outbreak,
the suspected cause and the key reference is annotated.
In the reported outbreaks, Cryptosporidium spp. was the
etiological agent in 60.3% (120) of the outbreaks, G. lamblia in
35.1% (70) and other protozoa in 4.5% (9). Four outbreaks (2%)
were caused by T. gondii and three (1.5%) by C. cayetanensis. In
two outbreaks (1%) Acanthamoeba was identified as causative
agent. In one outbreak, four parasitic protozoa were impli-
cated: G. lamblia (in 17.6% of stool samples) and Cryptospo-
ridium parvum (in 2.7% of stool samples) as well as E. histolytica
(in 9.4% of stool samples) and B. hominis (in 8.1% of stool
samples) were detected. The outbreak occurred in Malaysia
during April and May 2004 among Orang Asli (Aborigine)
(Hakim et al., 2007). Summarizing the outbreaks, we count this
outbreak as a single one, while it is mentioned in all three
tables of each detected pathogen.
From the Australian continent, 46.7% (93) of worldwide
waterborne outbreaks caused by parasitic protozoa were re-
ported. In New Zealand 80 outbreaks occurred (40.2%), in
Australia 13 (6.5%).
The waterborne outbreaks on the American continent
amount to 33.1% (66) of worldwide waterborne outbreaks.
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Table 1 e List of worldwide waterborne outbreaks caused by Cryptosporidium spp.

Month/year Location/country Est. cases Susp. cause Key reference
a
Aug 2001 Nurnberg/Germany 201 (15) Potentially tap water during field exercise Brockmann et al., 2008
among military recruits
Jan 2004 Ohio/USA 82 Drinking water from a well in a factory Liang et al., 2006
ApreMay 2004 Cameron Highlands/ Probably 79 G. lamblia (17.6%), Entamoeba (9.4%), Hakim et al., 2007
Malaysia Blastocystis hominis (8.1%), Cryptosporidium
(2.7%)b/source of infection probably
contaminated water or food
Mar 2004 North West England 4 (4) Swimming pool Nichols et al., 2006
MayeJun 2004 Northern and 7 (7) Swimming pool Nichols et al., 2006
Yorkshire/England
Jun 2004 Georgia/USA 14 Treated recreational water in a Dziuban et al., 2006
community pool
Jul 2004 Ohio/USA 160 Treated recreational water in a Dziuban et al., 2006
community wading pool
Jul 2004 Illinois/USA 37 Treated recreational water in a Dziuban et al., 2006
community pool, wading pool and
interactive fountain
Aug 2004 California/USA 336 Treated recreational water of a Dziuban et al., 2006
water park pool
AugeSep 2004 Nagano/Japan 41 (30)/74e288d Swimming pool in a hotel Ichinohe et al., 2005,
Yokoi et al., 2005,
Takagi et al., 2008
Aug 2004 Wisconsin/USA 6 Treated recreational water in a Dziuban et al., 2006
community pool
Aug 2004 Colorado/USA 6 Treated recreational water of a hotel pool Dziuban et al., 2006
AugeSep 2004 California/USA >250 Oocysts in backwash and sand from Wheeler et al., 2006
waterslides filter in a water park
AugeNov 2004 Bergen/Norway 133 Additive during large giardiasis outbreak Robertson et al., 2006a, b
Sep 2004 Illinois/USA 8 Treated recreational water in a hotel pool Dziuban et al., 2006
Oct 2004 Northern and 10 (9) Swimming pool Nichols et al., 2006
Yorkshire/England
2004 New Zealand 8 Untreated water supply Institute of Environmental
Science and Research
Ltd (ESR), New Zealand, 2004
2004 Queensland/Australia 5 (5) Public swimming pool Dale et al., 2010
Mar 2005 South-east-Ireland 31 Waterborne and person-to-person Health Protection
community outbreak Surveillance Center
(HPSC) 2006, Ireland
Apr 2005 West-Ireland 7 Waterborne Health Protection
Surveillance Center
(HPSC), Ireland
Jun 2005 New York/USA 2307 Interactive fountain, state park Yoder et al., 2008
Jun 2005 Kentucky/USA 53 Treated recreational water in Yoder et al., 2008
community pools
Jun 2005 Florida/USA 47 Treated recreational water in a hotel pool Yoder et al., 2008
Jun 2005 Iowa/USA 24 Treated recreational water in a Yoder et al., 2008
community pool
Jun 2005 Kentucky/USA 9 Treated recreational water in a Yoder et al., 2008
community wading pool
Jul 2005 Kansas/USA 84 Treated recreational water in a Yoder et al., 2008
water park pool
Jul 2005 Oregon/USA 20 Treated recreational water in a Yoder et al., 2008
membership club pool
JuleAug 2005 New York State/USA >3000 (425) Use of a recreational water Schaffzin et al., 2006
interactive fountain
JuleAug 2005 Madison, Missouri/USA 56 Recreational pool water Turabelidze et al., 2007
Aug 2005 Ohio/USA 523 Treated recreational water in a Yoder et al., 2008
community pool
Aug 2005 New York/USA 97 Treated recreational water in a camp pool Yoder et al., 2008
Aug 2005 Louisiana/USA 31 Interactive fountain in a water park Yoder et al., 2008
AugeSep 2005 Copenhagen/Denmark 99 (13) Carrots served in a basin with water Ethelberg et al., 2009
at a canteen salad bar
AugeDec 2005 London/England 84 Swimming pools Nichols et al., 2006

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Table 1 e (continued )
Month/year Location/country Est. cases Susp. cause Key reference

Sep 2005 Western Turkey 191 (15) Public drinking water supply contaminated Aksoy et al., 2007
by sewage or animal waste following
heavy rainfall
SepeNov 2005 South East England 140 (140) Public water supply Nichols et al., 2006
SepeDec 2005 North-west Wales 218 Drinking unboiled tap water, washing Mason et al., 2010
fruit or salad, fruit juice drinks, and
other transmission ways
Oct 2005 New York/USA 22 Treated recreational water Yoder et al., 2008
in a membership club pool
Nov 2005 Gwynedd and Anglesey, 100e232 Drinking water from several sources, incl. Carnicer-Pont et al., 2005;
northwest Wales/UK Lake Cwellyn Nichols et al., 2006
2005 Kentucky, Ohio/USA >800 Multiples modes of transmission Yoder et al., 2008
2005 New South Wales/Australia 254 (254) Public swimming pool Dale et al., 2010
2005 New Zealand 5 outbreaks, 63% untreated water supply, 22.2% Institute of Environmental
17 cases contamination of water source, 7.4% Science and Research
contamination of reservoirs, 37% Ltd (ESR), New Zealand, 2005
unknown factors (percentages relate
to a total number of 27
waterborne outbreaksc)
2005 Victoria/Australia 9 (9) Public swimming pool Dale et al., 2010
2005 Victoria/Australia 6 (5) Unknown swimming pool Dale et al., 2010
2005 Victoria/Australia 20 (18) Suspected waterborne, public Dale et al., 2010
Swimming pool
Jan 2006 England 14 (6) Swimming pool Davison, 2006
May 2006 Florida/USA 55 Treated recreational water, Yoder et al., 2008
interactive fountain
May 2006 South West England 35 Faecally contaminated surface water, Hoek et al., 2008
consumption of water from private well
Jun 2006 Missouri/USA 116 Treated recreational water, interactive Yoder et al., 2008
fountain, water park
Jun 2006 Wyoming/USA 29 Multiple community pools and Yoder et al., 2008
untreated reservoir
Jun 2006 Pennsylvania/USA 13 Treated recreational water, pool of a Yoder et al., 2008
membership club
JuneOct 2006 Wyoming/USA 34 Recreational water use at any public Alden et al., 2007
swimming pool and one local reservoir
JuneNov 2006 Charleston region, 85 Recreational water venues and 13 Alden et al., 2007
South Carolina/USA day care centers
Jul 2006 Montana/USA 82 Treated recreational water Yoder et al., 2008
of community pools
Jul 2006 Illinois/USA 65 Treated recreational water in a water Yoder et al., 2008
park of a day camp
Jul 2006 Louisiana/USA 29 Treated recreational water, interactive Yoder et al., 2008
fountain, water park pool
Jul 2006 South-Ireland 28 Waterborne Health Protection
Surveillance Center
(HPSC) 2007, Ireland
Jul 2006 California/USA 16 Treated recreational water, Yoder et al., 2008
interactive fountain
Jul 2006 South Carolina/USA 12 Treated recreational water Yoder et al., 2008
of a community pool
Jul 2006 Missouri/USA 6 Treated recreational water Yoder et al., 2008
of a community pool
Jul 2006 South-Ireland 2 Waterborne, private house Health Protection
Surveillance Center
(HPSC) 2007, Ireland
JuleAug 2006 Louisiana/USA 35 Recreational water use at Alden et al., 2007
commercial water park
Aug 2006 Wisconsin/USA 22 Treated recreational water Yoder et al., 2008
of a community pool
Aug 2006 Georgia/USA 19 Treated recreational water Yoder et al., 2008
in a community pool
Aug 2006 Illinois/USA 18 Treated recreational water Yoder et al., 2008
of a water park
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Table 1 e (continued )
Month/year Location/country Est. cases Susp. cause Key reference

Aug 2006 Colorado/USA 15 Birthday party at indoor community Boehmer et al., 2009
swimming pool
Aug 2006 Illinois/USA 7 Day camp pool and Alden et al., 2007
community water park
Aug 2006 Wisconsin/USA 4 Treated recreational water Yoder et al., 2008
of a community pool
Aug 2006 Illinois/USA 4 Treated recreational water Yoder et al., 2008
of a water park
Aug 2006 Florida/USA 3 Treated recreational water Yoder et al., 2008
in a hotel pool
Sep 2006 Minnesota/USA 47 Treated recreational water Yoder et al., 2008
in school pools
Sep 2006 Ohio/USA 10 Drinking water from Yoder et al., 2008
a well (in a church)
Sep 2006 Florida/USA 49 (9) Interactive water fountain Eisenstein, 2008
in neighborhood
Oct 2006 West-Ireland 6 Waterborne Health Protection
Surveillance Center
(HPSC) 2008, Ireland
Oct 2006 Georgia/USA 4 Treated recreational water Yoder et al., 2008
in a community pool
Nov 2006 South-east-Ireland 8 Waterborne community outbreak Health Protection
Surveillance Center
(HPSC) 2008, Ireland
Dec 2006 USA 7 Waterborne community outbreak Departments of Public
Health 2007
2006 Victoria/Australia 134 (134) Suspected waterborne, Dale et al., 2010
unknown swimming pool
2006 Victoria/Australia 30 (11) Suspected waterborne, Dale et al., 2010
school swimming pool
2006 South Australia 19 (14) Waterborne, unspecified source Dale et al., 2010
2006 Victoria/Australia 18 (18) Suspected waterborne, Dale et al., 2010
public swimming pool
2006 New Zealand 6 outbreaks, 83.3% untreated water supply, 44.4% Institute of Environmental
15 cases contamination of water source, 5.6% Science and Research
contamination of Ltd (ESR), New Zealand, 2006
reservoirs, 5.6% unknown
factors (percentages relate to a total
number of 18 waterborne outbreaksc)
2006 Western Australia 14 (14) Suspected waterborne, Dale et al., 2010
public swimming pool
2006 Victoria/Australia 10 (7) Suspected waterborne, public Dale et al., 2010
swimming pool
Jan 2007 South-east-Ireland 7 Waterborne community outbreak Health Protection
Surveillance Center
(HPSC) 2008, Ireland
Feb 2007 City and county of 182 (98) Public water supply using Lough Corrib Pelly et al., 2007
Galway/Ireland (a large lake)
Mar 2007 West-Ireland 304 Waterborne community outbreak Health Protection Surveillance
Center (HPSC) 2008, Ireland
Mar 2007 USA 186 Waterborne community outbreak Departments of Public
Health 2007
Mar 2007 Norway 25 (10) Drinking water from hotel Hajdu et al., 2008
dispensers and
tap water, consuming ice
cubes in hotel
bar, eating broccoli soup
Jun 2007 USA 2 Waterborne, private house Departments of Public
Health 2007
JuneDec 2007 Utah/USA 1902 Treated recreational water venues Rolfs et al., 2008
Jul 2007 South-Ireland 2 Waterborne, private house Health Protection
Surveillance Center
(HPSC), Ireland

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Table 1 e (continued )
Month/year Location/country Est. cases Susp. cause Key reference

Aug 2007 Idaho/USA 50 Recreational water at splash parks Jue and Schmalz, 2009
Aug 2007 Stockholm/Sweden 23 (9) Drinking water from a Persson et al., 2007
well at a camping site
close to a field with sheep
OcteDec 2007 Staffordshire/England 57 (39) Swimming pool associated Coetzee et al., 2008
2007 Galway/Ireland 182 Heavy precipitation of historic Pelly et al., 2007
proportions and the water source
reaching the highest
level on record
2007 New Zealand 5 outbreaks, 80% untreated water supply, 20% Institute of Environmental
16 cases contamination of water source, 6.7% Science and Research Ltd
treatment process failure, 6.7% (ESR), New Zealand, 2007
contamination of reservoirs, 6.7%
post treatment contamination,
13.3% unknown factors
(percentages relate to a total number of
15 waterborne outbreaksc)
2007 Northern Territory/ 4 (2) Suspected waterborne, public Dale et al., 2010
Australia swimming pool
Jan 2008 West-Ireland 3 Waterborne, private house Health Protection
Surveillance Center
(HPSC) 2009, Ireland
Mar 2008 South-Ireland 2 Waterborne and person-to-person Health Protection
in a private house Surveillance Center
(HPSC) 2009, Ireland
JuneJul 2008 Northamptonshire/UK 33 (23) Drinking water supplied from the Smith et al., 2010
Pitsford Reservoir
Jul 2008 South-east-Ireland 2 Waterborne and animal transmission Health Protection
in a private house Surveillance Center
(HPSC), Ireland
2008 New Zealand 4 outbreaks, 61.5% contamination of water source, Institute of Environmental
17 cases 50% untreated Science and Research Ltd
water supply, 11.5% contamination (ESR), New Zealand, 2008
of reservoirs, 15.4%
unknown factors (percentages relate
to a total number of 26
waterborne outbreaksc)
2009 New Zealand 5 outbreaks, 66.7% untreated drinking water supply, Institute of Environmental
13 cases 20.8% contamination of reservoirs, Science and Research
16.7% contamination of water Ltd (ESR), New Zealand, 2009
sources, 20.8% unknown factors
(percentages relate to a total
number of 24 waterborne
outbreaksc)
Nov 2010 Ostersund/Sweden 10,000 Contaminated water supply Sveriges Radio 2010

( ): laboratory confirmed cases.

a outbreak occurred before 2004, but was published at 2010 and is not included in the review of Karanis et al. (2007).
b infectious rate of tested stool samples.
c for some waterborne outbreaks more than one contributing factor was recorded.
d variation between authors.

From the 61 outbreaks in North America (30.6%) 60 appeared
in the United States (30.1%) and 1 in Canada (0.5%). The
documented five outbreaks in South America (2.5%) occurred
in Peru (two outbreaks, 1%), in Brazil (two outbreaks, 1%) and
in French Guiana (one outbreak, 0.5%).
Europe contributes 16.5% (33) of worldwide waterborne
outbreaks. The distribution within the European countries is
as follows: Ireland 6.5% (13) of worldwide waterborne
outbreaks, the United Kingdom 5.5% (11), Norway 2% (4),
Sweden 1% (2) and at least 0.5% (1) in Finland, Denmark and
Germany, respectively.
In Asia 7 (3.5%) waterborne outbreaks of parasitic protozoan
diseases were reported, 3 (1.5%) in Turkey and 1 (0.5%) in each
of the following countries: Japan, China, India and Malaysia.
The worldwide distribution of waterborne outbreaks
caused by parasitic protozoa on the individual continents is
presented in Fig. 1, while Fig. 2 shows the distribution across
countries.
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Table 2 e List of worldwide waterborne outbreaks caused by Giardia lamblia.

Month/year Location/country Est. cases Susp. cause/parasite Key reference

Nov 2003eJul 2004 Trondheim/Norway 12 Waterborne, child day care center Wahl and Bevanger, 2007
Mar 2004 Missouri/USA 9 Untreated recreational water, lake Dziuban et al., 2006
AprileMay 2004 Cameron Highlands (Probably 79) G. lamblia (17.6%), Entamoeba (9.4%), Hakim et al., 2007
/Malaysia Blastocystis hominis (8.1%), Cryptosporidium
(2.7%)a/source of infection probably
contaminated water or food
MayeSep 2004 Ohio/USA 3e1450 Sewage contaminated groundwater OReilly et al., 2007
Jun 2004 Vermont/USA 11 Drinking water from a well in a camp Liang et al., 2006
AugeOct 2004 Bergen/Norway 2500 (1300) Leaking sewage pipes and insufficient Nygard et al., 2006,
water treatment Robertson et al., 2006a, b;
Strand et al., 2008
2004 New Zealand 11 outbreaks, 8 outbreaks caused untreated water supplies, Institute of Environmental
34 cases 1 by inadequate water source, 2 by Science and Research Ltd
multiple sources (ESR), New Zealand, 2004
Jul 2005 California/USA 3 Water not intended to drink Yoder et al., 2008
in a private residence
Aug 2005 California/USA 41 Drinking water Yoder et al., 2008
Oct 2005 Izmir/Turkey 196 (7) Faecal contamination in public water supply Tuncay et al., 2008
2005 New South Wales 12 (3) Suspected rainwater tank or bore water Dale et al., 2010
/Australia in a health spa resort
2005 New Zealand 9 outbreaks, 63% untreated water supply, 22.2% contamination Institute of Environmental
34 cases of water source, 7.4% contamination of reservoirs, Science and Research Ltd
37% unknown factors (percentages relate to a (ESR), New Zealand, 2005
total number of 27 waterborne outbreaksb)
May 2006 Colorado/USA 6 River water in wilderness Yoder et al., 2008
Sep 2006 Florida/USA 49 (38) Interactive water fountain in neighborhood Eisenstein, 2008
2006 New Zealand 7 outbreaks, 83.3% untreated water supply, 44.4% contamination Institute of Environmental
22 cases of water source, 5.6% contamination of reservoirs, Science and Research Ltd
5.6% unknown factors (percentages relate to a (ESR), New Zealand, 2006
total number of 18 waterborne outbreaksb)
JuleAug 2007 California/USA 50 (26) Unsterilized sand in slow sand water filtration Karon et al., 2010
system in a private recreational camp
Sep 2007 New Hamshire/USA 31 Community drinking water associated (tap water) Daly et al., 2009
Nov 2007e Nokia/Finland ND Sewage contamination of drinking water Rimhanen-Finne et al., 2010
Feb 2008 distribution network
2007 Northern Ontario ND Water source in a tree-planting camp C-EnterNet Annual Report
/Canada 2007, Public Health Agency
of Canada
2007 New Zealand 7 outbreaks, 80% untreated water supply, 20% contamination Institute of Environmental
32 cases of water source, 6.7% treatment process failure, Science and Research Ltd
6.7% contamination of reservoirs, 6.7% post (ESR), New Zealand, 2007
treatment contamination, 13.3% unknown
factors (percentages relate to a total number
of 15 waterborne outbreaksb)
2008 New Zealand 14 outbreaks, 61.5% contamination of water sources, 50% Institute of Environmental
63 cases untreated water supply, 11.5% contamination Science and Research Ltd
of reservoirs, 15.4% unknown factors (ESR), New Zealand, 2008
(percentages relate to a total number
of 26 waterborne outbreaksb)
2009 New Zealand 13 outbreaks, 66.7% untreated drinking water supply, 20.8% Institute of Environmental
44 cases contamination of reservoirs, 16.7% contamination Science and Research Ltd
of water sources, 20.8% unknown factors (ESR), New Zealand, 2009
(percentages relate to a total number of
24 waterborne outbreaksb)

ND: no data.
( ): laboratory confirmed cases.
a infectious rate of tested stool samples.
b for some waterborne outbreaks more than one contributing factor was recorded.

In this review, 36.2% (72) of the documented worldwide reservoirs and post treatment contamination. In 33.7% (67
outbreaks caused by protozoan pathogens had multiple ways outbreaks), the transfer through recreational water was
of transmission, e.g. untreated water supplies, contamination detected as the source of infection, mainly due to the
of water sources, treatment process failures, contamination of contamination with Cryptosporidium spp. in 32.7% (65) of
 Author's personal copy

6610 w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 6 6 0 3 e6 6 1 4

Torres-Slimming et al., 2006

Balasundaram et al., 2010
Palanisamy et al., 2006,
Key reference

Mundaca et al., 2008

Vaudaux et al., 2010

Demar et al., 2007

Hakim et al., 2007

Aksoy et al., 2007

Joslin et al., 2006

Khan et al., 2006

Mao et al., 2009
MMWR 2007
Fig. 1 e Distribution of worldwide waterborne outbreaks
caused by parasitic protozoan between 2004 and 2010 by
continent.
Cyclospora, co-infection with outbreak of cryptosporidiosis/
T. gondii (ocular)/probably contaminated supplying water
T. gondii/contaminated cistern, municipal water supply

T. gondii/non-treated water in common neighborhood

G. lamblia (17.6%), Entamoeba (9.4%), B. hominis (8.1%),
Cryptosporidium (2.7%)b/source of infection probably

described outbreaks. In 20.6% (41) of the listed outbreaks,

drinking water systems were contaminated with a protozoan
Acanthamoeba (Keratitis)/probably waterborne

Acanthamoeba (Keratitis)/probably waterborne

C. cayetanensis/unknown way of transmission

pathogen. In 9.5% (19 outbreaks) of the reported outbreaks the

C. cayetanensis/way of transmission unclear

contaminated public drinking water supply

way of transmission was not mentioned.

Parasite/susp. cause

4. Discussion
contaminated water or food
T. gondii/unknown source

The gathering of worldwide waterborne parasitic protozoan

outbreaks illustrates their global distribution pattern. The
after heavy rainfall

present survey shows a large number of outbreaks in a short

a outbreak occurred before 2004, but was published at 2010 and is not included in the review of Karanis et al. (2007).

time period, 199 worldwide outbreaks in 7 years, while the

E. histolytica

previous overview of Karanis et al. (2007) presented 325 re-

ported outbreaks in 100 years. This significant difference in
the number of reported outbreaks is caused by the substantial
improvements of data reporting and the establishment of
Table 3 e List of worldwide waterborne outbreaks caused by other parasitic protozoa.

surveillance systems in developed countries. Both achieve-

ments of the developed countries are also the reasons for the
Probably 79
Est. cases

distortion in the reflection of the global distribution pattern.

249 (178)

112 (27)

191 (9)

31 (23)

The highest prevalence of parasitic protozoan infections is

37 (7)
138

known to occur in developing countries due to their low

20
40
11

hygiene standards. Thus, the highest rate of waterborne

parasitic protozoan outbreaks should be estimated in these
Chicago-Gary-Kanosha area, Illinois/USA

countries. Though, we found a higher rate of reported water-

borne protozoan outbreaks in developed nations. These find-
ings are due to the better technological and logistical
possibilities of the developed countries.
Location/country

Cameron Highlands/Malaysia

As the collection of data depends on the detection, inves-

Santa Isabel do Ivai/Brazil

35 states and Puerto Rico

tigation and reporting system of the outbreaks (Leclerc et al.,

Coimbatore City/India
Patam/French Guiana

Jiangshan City/China

2002) many waterborne parasitic protozoan outbreaks stay

Agronomica/Brazil

unrecognized or unreported. In 1990, Craun estimated that

Izmir/Turkey
Lima/Peru

Lima/Peru

b infectious rate of tested stool samples.

ND/between 2003 and 2005

( ): labor-confirmed cases.
Jan 2005eMay 2007
Jun 2003eNov 2005
Dec 2003eJan 2004

Aug 2004eJul 2005

AprileMay 2004
a

MayeJun 2006
OcteDec 2001
Month/year

ND : no data.
Nov 2004

Mar 2005
Sep 2005

Fig. 2 e Distribution of worldwide waterborne outbreaks

caused by parasitic protozoa between 2004 and 2010 by
country.
 Author's personal copy
w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 6 6 0 3 e6 6 1 4
only a low fractional amount of waterborne outbreaks
affecting the United States are detected and reported, possibly
as low as one-tenth (Craun, 1990). In 1995, Morris and Levin
suggested that the annual incidence of waterborne infectious
diseases in the United States could even be as high as 8 million
cases of illness and around 1200 cases of death (Morris and
Levin, 1995). Likewise, in the Annual Epidemiological Report
on Communicable Diseases in Europe 2009, ECDC infectious
diseases due to protozoan are described to be underreported,
e.g. the data of cryptosporidiosis from several EU countries are
lacking and several countries have not established a surveil-
lance system for toxoplasmosis (www.ecdc.europa.eu). The
National Institute of Hygiene in Poland (PZH) does not report
human cases of cryptosporidiosis although they are registered
and the annual number of human giardiasis is probably
underestimated (Bajer, 2008).
As water is the transmission route of the referred protozoa
Giardia cysts and Cryptosporidium oocysts are widely distrib-
uted in aquatic ecosystems and could be detected in 81% and
87% of raw water samples of 66 surface water treatment plants
in the United States 1991 (LeChevallier et al., 1991). Worldwide,
G. lamblia is one of the most prevalently identified causative
pathogen in waterborne disease outbreaks (WBDOs). Water-
borne outbreaks of giardiasis are usually associated with
ingestion of contaminated surface water or groundwater
while the contamination of recreational water has also been
noticed (Marshall et al., 1997). In developed countries G. lamblia
and Cryptosporidium spp. are the most common waterborne
pathogens. Slifko et al. (2000) described three reasons for this:
domestic animals are often infected with cryptosporidiosis or
giardiasis, the aquatic ecosystem is contaminated by the high
frequency of environmental burden and lastly, Giardia cysts
and Cryptosporidium oocysts are resistant against commonly
used water disinfectants (Slifko et al., 2000).
In the early 1900s waterborne diseases were accountable
for 25% of deaths due to infectious diseases. Chlorination, the
first used disinfection for public water supplies, lead to
a dramatic decrease of waterborne diseases in the United
States (Cutler and Miller, 2005). The WHO introduced treat-
ment guidelines for the quality of drinking water which
includes the treatment of water intended to drink with plain
sedimentation, pre-filtration, slow sand filtration, coagula-
tion, flocculation and sedimentation, rapid sand filtration,
aeration and disinfection via boiling, UV radiation, chlorine
and ozone. For water treatment plants multi-barrier systems
are recommended (www.who.int). After the introduction of
membrane filtration in North West England, the incidence of
cryptosporidiosis decreased around 79% (Goh et al., 2005). The
CDC in collaboration with the Pan American Health Organi-
zation (PAHO) generated a Safe Water System (SWS) which
includes three elements: water treatment with sodium
hypochlorite at the point-of-use (reduction of diarrheal
disease incidence: 26e84%), storage of water in safe
containers, as well as advanced hygiene and water handling
practices. Since 1998 national, regional and local SWS projects
have been implemented with NGO and government partners
in over 30 countries. A systematic review of interventions to
improve water quality for preventing diarrhea published 2007
by Clasen pointed out that interventions generally are effec-
tive (Clasen et al., 2007).
6611
USEPA and CDC established protection and prevention
guidelines as well as national statistics of waterborne
outbreaks caused by different agents in the United States. In
1994, USEPA published the Cryptosporidium Criteria Document
(www.epa.gov) and thus declared Cryptosporidium as a primary
drinking water contaminant. The attention on this protozoon
raised and led to more investigation. Beside traditional
microscopy and staining methods, enzyme immunoassays
(EIAs), direct fluorescent-antibody (DFA) and the polymerase
chain reaction (PCR) have become established as sensitive and
specific detection methods (Morgan et al., 1996). As a result of
the enhanced surveillance the USEPA announced the Interim
Enhanced Surface Water Treatment Rule to minimize the
level of Cryptosporidium spp. in finished water and estimated
that the incidence of endemic illness caused by Cryptospo-
ridium spp. will decrease by 463,000 cases each year (www.epa.
gov). Due to the advertence and the surveillance system, the
data reported for the United States are the most complete of
waterborne diseases worldwide (Leclerc et al., 2002). The
increasing quality of documentation led to a rise in reported
outbreaks during recent years, especially in cryptosporidiosis
and giardiasis (Craun et al., 2005).
Nevertheless, the supreme incidence of waterborne para-
sitic protozoan infection is suggested to occur in developing
countries. In Latin America, Asia and Africa around 600
million people live in unhealthy homes (Cotruva et al., 2004),
1.1 billion people lack access to improved water supplies and
2.6 billion people lack adequate sanitation (www.who.int).
Hence high prevalence rates of waterborne infectious diseases
can be expected in developing countries where water supply
and waste disposal are deficient. Lanata (2003) stated that the
majority of giardiasis outbreaks occur in Latin America, Africa
and Asia, with about 5  105 new cases each year. However,
gastrointestinal infections are under-diagnosed in developing
countries and the prevalence is underestimated (Lanata,
2003). Current and Garcia (1991) recorded prevalence rates of
Cryptosporidium in stool samples of patients with gastroen-
teritis of 1e4% in Europe and North America, while the prev-
alence rates in Africa, Asia, Australia and South America
amount to between 3 and 20%. They also detected high rates
of asymptomatic carriage of Cryptosporidium (10e30%) in
developing countries compared to low rates of <1% in devel-
oped countries. Higher prevalence rates in developing coun-
tries can also be estimated for the other waterborne parasitic
protozoan infections. However, most studies about preva-
lence of parasitic protozoan infections have been made in
developed countries where health infrastructure and labora-
tory testing are more accessible than in developing countries
(Mak, 2004). Yotthanooi and Choonpradub (2010) consider that
data of diarrheal diseases incidence in Thailand are known to
be underreported and the causal agents of diarrheal diseases
are undiscovered.
But although surveillance systems are established in
developed countries, an international agreement of reporting
structure is still missing. As Hormann et al. (2004) criticizes,
the systems of surveillance and reporting are fundamentally
different between various countries and a comparison of data
is not always possible (Hormann et al., 2004). While the CDC
registers each waterborne outbreak by agent, location and
number of affected persons, European surveillance systems
 Author's personal copy
6612 w a t e r r e s e a r c h 4 5 ( 2 0 1 1 ) 6 6 0 3 e6 6 1 4
are used to figure out national infection rates and incidences
meanwhile neglecting the itemization of waterborne
outbreaks. The index of human cryptosporidiosis and giardi-
asis is listed annually by Euro Surveillance but the sources of
infection remain undiscovered. The number of human cases
of giardiasis in the Ukraine was 30751 in 2007, 31638 in 2008
and even 32928 in 2009. However, these data doesnt allow
precise conclusions about their origin and no further infor-
mation about their consistence is given. It remains unclear
whether these data reflect incidence or prevalence or both and
whether they also include outbreaks (www.eurosurveillance.
org). In Japan, Taniguchi described the incidence rate of
amebiasis with an annual average of 3.18 per 1,000,000 people
in 1999e2008 as second highest nationwide (Taniguchi et al.,
2008) but outbreaks and cases were not described.
Furthermore, Craun et al. (2005) declared that even in
countries with surveillance systems, outbreak investigation
activities have frequently been unable to identify sources of
infection and etiologic agents. This statement raises the
question of the quality of surveillance. Even countries that
already support a surveillance system should improve their
methods of detection and disease diagnosis. The incorporation
of molecular investigative tools including detection/diagnosis
and genotyping and the introduction of new tools (Ortega-
Pierres et al., 2009; Karanis and Ongerth, 2009) will contribute
to a better surveillance of waterborne parasitic outbreaks.
5. Conclusions
The number of waterborne parasitic outbreaks is still
increasing due to the better surveillance and reporting
systems in several countries and continents. Since this review
leans on documented waterborne parasitic protozoan
outbreaks listed in worldwide databases and reported in
single studies it can only give an overview of the detected and
reported outbreaks. Quantity and intensity of the undiag-
nosed outbreaks stay uncovered. Data about those countries
that are probably concerned most are lacking. The introduc-
tion of surveillance systems in these countries would be
helpful to detect, and as a result to combat, parasitic protozoa
with the final aim to improve the health of the population.
Therefore it is necessary to develop reliable and accessible
diagnostic tools for the detection of the causative organisms
especially in these countries. Further investigation of
emerging methods is required to provide more results con-
cerning human infections caused by parasitic organisms.
Additionally, an international standardized reporting system
should be established in all affected countries. Standardized
databases could lead to a closer and more successful collab-
oration in the battle against waterborne pathogenic protozoa.
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