Waterborne transmission of protozoan parasites: a review of worldwide outbreaks – an update 2017–2022

Waterborne diseases occur via ingesting contaminated drinking water and bathing water as vehicles for exposure to infectious pathogens (Leclerc et al. 2002; Plutzer & Karanis 2016). According to the World Health Organization (WHO), waterborne infections of gastro-enteric origin are among the leading causes of morbidity and mortality worldwide (Angelici & Karanis 2019).

Diarrhoeal illnesses are one of the common causes of mortality in low-income countries. They are among the top five causes of death and pose significant risks to humans and animals (www.who.int). Protozoan parasites are causal agents for 1.7 billion diarrheal diseases and 842,000 deaths annually (Arslan et al. 2022). They are the second largest cause of mortality in children under five, with more than 525,000 deaths per year (www.who.int). Waterborne diseases caused by protozoan parasites are regarded as a public health concern in both developed and developing nations and are responsible for many outbreaks worldwide (Plutzer & Karanis 2016).

Cryptosporidium and Giardia are the most common pathogens in the reported outbreaks over the last decades in comparison to other parasitic protozoa such as Entamoeba, Toxoplasma, Balantidium, Isospora, Blastocystis, Acanthamoeba, Microsporidia, Sarcocystis, Naegleria, and Cyclospora (Karanis et al. 2007; Baldursson & Karanis 2011; Efstratiou et al. 2017). Cryptosporidium oocysts and Giardia cysts have been found to contaminate surface waters and groundwater resources around the world (Omarova et al. 2018). Also, parasitic protozoa in facilities, such as pools, hot tubs, water playgrounds, or other artificially constructed water structures used for recreational purposes can lead to a waterborne outbreak (Hlavsa 2021). Since most of these protozoa spread via feces, they can also infect humans through sewage, land, or rivers contaminated with animal or human feces (Lanata 2003).

Given the high number of human infectious diseases associated with water, determining the waterborne transmission of less frequent etiological agents is complicated, and the role of different water environments in the transmission of protozoan infections, especially those connected with zoonotic protozoa, is under-recognized (Plutzer & Karanis 2016).

Reliable prediction of waterborne diseases requires global health statistics and effective surveillance systems across all countries. Many countries have developed surveillance systems that report data on national outbreaks. The United States established the Centers for Disease Control and Prevention (CDC), the US Environmental Protection Agency (USEPA), and the USA Waterborne Disease and Outbreak Surveillance System (WBDOSS), which have been monitoring waterborne diseases since 1971. Moreover, the national epidemiological surveillance of infectious illnesses (NESID) in Japan, ‘The National Notifiable Diseases Surveillance System (NNDSS)’ in Australia, ‘Public Health England (PHE)’ in the United Kingdom, ‘Public Health Agency of Canada (PHAC)’ in Canada, and the ‘European Center for Disease Control and Prevention (ECDC)’ as a European institution for public health (http://ecdc.europa.eu/). However, in developing countries, monitoring systems still need to indicate and report outbreaks of waterborne protozoan parasites.

Waterborne outbreaks highlight the ability of pathogens to penetrate various water barriers and their potential to infect humans and animals. Moreover, they indicate the incidence and severity of the disease caused by these pathogens and the difficulty of their control via water treatment procedures. Even though the outbreak data do not reveal the accurate incidence of waterborne diseases, the outbreak surveillance provides information regarding the significant waterborne pathogens, relative grades of hazard associated with water resources and water treatment procedures, and the appropriateness of relevant assessments. The outbreak reports are indicators of pathogens of public health importance and hygiene deficiencies in water systems that may also be the leading causes of endemic waterborne diseases. Therefore, the present review aims to update worldwide waterborne parasitic outbreaks reported during 2017–2022.

Data from advanced search engines of scholarly databases, including PubMed and Scopus, and data from global surveillance systems, such as the CDC and the ECDC, were searched for literature and reports on waterborne parasitic protozoan outbreaks. Moreover, online sources including Euro Surveillance (published by ECDC), The Institute of Environmental Science and Research Ltd (ESR), Canada Communicable Disease Report (CCDR by PHAC), Health Protection Surveillance Centre (HPSC), Morbidity and Mortality Weekly Report (MMWR by CDC), and outbreak surveillance for gastrointestinal disease (eFOSS by PHE) were used to collect data for the current review.

Keywords used in this study were as follows: ‘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) toxoplasmosis’, ‘outbreak (and) microsporidia’, ‘outbreak (and) microsporidiosis’, ‘outbreak (and) Sarcocystis’, ‘outbreak (and) sarcocystosis’, ‘outbreak (and) Naegleria’, ‘outbreak (and) Balantidium coli’, ‘outbreak (and) balantidiosis’, ‘outbreak (and) Dientamoeba fragilis’, and ‘outbreak (and) Isospora’.

The titles and abstracts of the listed papers were critically evaluated and reviewed by two independent authors as part of the screening process. After the screening, duplicates and irrelevant papers were removed. The full texts of the remaining papers were obtained and assessed. Selected articles were checked for relevant references that needed to be identified through the database search. The following criteria were used to determine eligibility:

• 1.

  Articles published from January 2017 to December 2022

• 2.

  Availability of full-text and abstract in English.

• 3.

  All published studies reported waterborne parasitic protozoan outbreaks.

• 4.

  Availability of data regarding the source of the waterborne infection and the type of protozoan parasite that caused the outbreak.

The current study identified 1,426 articles. After excluding duplicates, screening titles and abstracts, and completing text evaluation, 45 articles from scholarly databases and 153 reports from online surveillance systems were included in the study (Figure 1).

In the 5 years between 2017 and 2022, 416 waterborne outbreaks of parasitic protozoan diseases were reported worldwide. Tables 1–3 present a summary of the documented outbreaks and also represent a few waterborne outbreaks prior to 2017 that were not included in the 2007, 2011, and 2017 reviews (Karanis et al. 2007; Baldursson & Karanis 2011; Efstratiou et al. 2017) since these outbreaks have been reported and published later.

Regarding the type of protozoan parasite, Cryptosporidium spp. was the etiological agent in most reported outbreaks (77.4% or 322). There were two Cryptosporidium species identified, with C. hominis and C. parvum being etiological agents in 123 (30%) and 100 (24.03%) outbreaks, respectively (Table 1).

Giardia spp. was detected in 71 outbreaks (17.1%), of which 27 (6.5%) were caused by G. duodenalis (Table 2).

Moreover, other protozoa were reported as the causative agents in 5.5% (23) of the outbreaks. In this regard, the type of the protozoan parasite, as well as the number and percentage of outbreaks were as follows: T. gondii (6 outbreaks, 1.4%), N. fowleri (4 outbreaks, 1%), B. hominis (3 outbreaks, 0.72%), C. cayetanensis (3 outbreaks, 0.72%), D. fragilis (3 outbreaks, 0.72%), Acanthamoeba spp. (1 outbreak, 0.24%), E. histolytica (1 outbreak, 0.24%), V. corneae (1 outbreak, 0.24%), and E. bieneusi (1 outbreak, 0.24%) (Table 3).

In terms of the continent, the reports revealed that the majority (47% or 195 outbreaks) of the reported worldwide waterborne outbreaks were reported in North America, following Oceania (103 outbreaks), and Europe (100 outbreaks). Furthermore, 10 outbreaks were documented in Asia, and 8 in South America (Tables 1–3).

European countries contributed 24% (100) of the total outbreaks. The distribution within the European countries was as follows: United Kingdom (18.3% or 76 outbreaks), unspecified European countries (3% or 13 outbreaks), France (1.2% or five outbreaks), and Italy (0.5% or two outbreaks). Moreover, Hungary, Poland, Finland, and Sweden independently accounted for one outbreak (0.24%).

South American countries contributed to eight outbreaks, including five (1.2%) outbreaks in Brazil and three (0.72%) in French Guiana (Figure 2).

Concerning the Asian countries, four (1.0%) outbreaks were reported in Turkey and two (0.5%) in Israel. Additionally, Taiwan, South Korea, Jordan, and Pakistan were independently accounted for one (0.24%) outbreak (Figure 2).

Concerning the suspected source of infection, recreational waters/swimming pools were the most suspected source of infection, contributing to 75.2% (313) of the total waterborne outbreaks. These outbreaks were primarily due to contamination with Cryptosporidium (92%). Giardia was responsible for 25.3% of the outbreaks related to recreational water and/or swimming pools. In 22% of the outbreaks with swimming pools as sources of infection, other protozoan parasites were the etiological agents. Among the documented outbreaks, swimming pools were the source of infection in 278 (67%) outbreaks. Finally, 154 (37%) and 52 (12.5%) outbreaks were connected to treated and untreated waters, respectively. In comparison, 71 (17.06%) outbreaks were found to be connected to contaminated water supplies, tap water, and drinking water (Tables 1–3).

In the last three decades, many reports of waterborne outbreaks were linked to protozoan parasites. WHO has classified Cryptosporidium as one of the leading causal agents in both food and waterborne diseases (Gururajan et al. 2021). During the past few years, scientific articles have provided accurate and ongoing records of global outbreaks. The first global review (Karanis et al. 2007) in this regard showed a large number of outbreaks (325), with the subsequent ones (Baldursson & Karanis 2011; Efstratiou et al. 2017; Ma et al. 2022) recording 199, 381, and 251 outbreaks in 2011, 2017, and 2022, respectively.

The present review identified 416 outbreaks reported during the past 5 years globally and continues the previous studies of 2007, 2011, and 2017. We found that the highest number of parasitic waterborne outbreaks were reported in developed countries. The review of 2007 indicated that most of the outbreaks were reported in the USA (52.6%) with nearly two-thirds of them having occurred in North America. The review of 2011 showed that the highest number of reports appeared in New Zealand (40.2% or 80 outbreaks), and 30.1% of the total outbreaks were recorded in the United States (60 outbreaks). Based on the review of 2017, 48% were observed in New Zealand, following 41% of the total numbers in North America.

Similarly, in the present review, the highest number of outbreaks (195, 46.8%) were reported on the North American continent, most of which occurred in the United States. The increased trend in reports of waterborne protozoan parasite outbreaks in developed countries is in accordance with prior studies (Yang et al. 2012). The significant improvements in reporting and surveillance systems, improved public health policies, precise detection approaches, and advanced socioeconomic status established in developed countries contributed to the rise in reported parasitic protozoan outbreaks. In the United States, the local, territorial, and state public health departments are predominantly responsible for the detection and investigation of waterborne disease outbreaks, and they voluntarily report the cases to the CDC via the National Outbreak Reporting System (NORS), which is a web-based platform (Hlavsa et al. 2011). There are also improved notification and reporting systems in the United Kingdom (PHE) and Australia (NNDSS), which have the highest number of waterborne outbreak reports after the United States.

Although the United States has achieved considerable progress in preventing of waterborne infections over the last century, the CDC's estimates showed that approximately 7.2 million Americans are infected (Gharpure et al. 2019). Cryptosporidium oocysts and Giardia cysts have been broadly detected in water samples throughout the United States (Ongerth 2013, 2017). Moreover, Cryptosporidium is the most frequently reported cause of waterborne outbreaks and the third leading cause of intestinal infections attributed to animal contact in the United States (Gharpure et al. 2019).

In addition to the advanced surveillance system, which can serve as a contributing factor, there are other factors, such as a large number of livestock living and grazing around surface water resources, mass farming, and manure distribution in fields, leading to the high prevalence of waterborne giardiasis and cryptosporidiosis in developed countries. The environmental distribution of Cryptosporidium and Giardia depends on human, wildlife, and agricultural sources, which have a potential role in the contamination of surface waters. The anthropogenic disturbance also leads to increasing numbers of zoonotic diseases and spillovers of zoonotic pathogens.

This review found that most waterborne outbreaks are caused by Cryptosporidium, with C. hominis being more frequent than C. parvum. It is demonstrated that many of the microbial pathogens of public health concern in recreational waters are derived from fecal contamination sources, including surface runoff, sewage, wildlife, and domestic animals (Fewtrell & Kay 2015). Waterborne cryptosporidiosis outbreaks that involve C. hominis as the primary cause attract attention toward sewage contamination rather than runoff from agricultural sources (Robertson et al. 2020). Previous experimental research proved that increased human recreation in water bodies is a risk factor strongly associated with the increased Cryptosporidium contamination levels at these sources, as only C. hominis was identified. It implies that recreational access to drinking water catchments poses a potential public health risk and that government policies restricting activities to the outskirts of the catchments should be facilitated (Loganthan et al. 2012).

The global data on waterborne disease outbreaks may underestimate the true incidence of these diseases, as not all of them are recognized, investigated, and reported in developing countries which are probably most affected by waterborne infections due to poor hygiene and inadequate water treatment standards (Baldursson & Karanis 2011). For instance, many households in these countries utilize raw water for other purposes, such as cooking, bathing, and recreational activities (Young et al. 2012; Siwila et al. 2020). Hence, to prevent misrepresenting the worldwide status of waterborne outbreaks, public health organizations in these regions require strategies for establishing an accurate diagnosis and reliable surveillance and notification system.

Waterborne pathogens infect people not only via drinking water but also when they breathe in contaminated water or get water in their ears or nose. The recent estimates by the CDC revealed a shift in the types of waterborne infections and routes of exposure in the United States during the past decades. Once the world's population grew, the need for using water on a broader scale and in new and creative ways arose. To accommodate these demands, high-rise structures, water parks, and other facilities have been built, which all need complex water systems. Water circulates further in these complicated structures, including many pipes, drains, and other plumbing equipment. Therefore it is more difficult to control water quality and apply enough disinfectant in the system (https://www.cdc.gov).

The substantial role of recreational water as a source of waterborne infections has been frequently discussed in recent decades. In parallel, we found that parasitic protozoan outbreaks are more associated with recreational water and/or swimming pools than other sources (e.g., drinking water and community water). Global cryptosporidiosis outbreaks via recreational water sources are reported more frequently than drinking water-associated outbreaks (Chalmers 2012). A review of 2011 (Baldursson & Karanis 2011) indicated that in 7 years (between 2004 and 2010), of 120 waterborne Cryptosporidium outbreaks, 54% were related to recreational waters and 46% were linked to drinking water sources. Untreated recreational waters (e.g., lakes and dams) may be contaminated via animal, sewage, and agricultural sources. Swimming in these environments is a public health hazard (Karanis et al. 2007).

The current review found that recreational water and/or swimming pools were the infection sources in 313 (75.2%) waterborne parasitic outbreaks, 92% related to cryptosporidiosis outbreaks. These findings are consistent with the advanced monitoring systems and research on cases linked to water supply systems and recreational waters. In recent years, parasitic infection outbreaks connected to swimming pools have escalated in the United States (Hlavsa et al. 2017). Cryptosporidium is the primary cause of outbreaks in recreational water sources and swimming pools, given its chlorine resistance and the challenges of eliminating it through filtration (Gururajan et al. 2021). Thus, bathers and swimmers may be at risk of infection with participation in recreational activities in pools infected with chlorine-resistant protozoa (Pineda et al. 2020). A preliminary record published by the CDC's MMWR stated that in the United States, the number of Cryptosporidium outbreaks (at least 32) associated with swimming pools and water playgrounds was higher in 2016 compared to 2014, with 16 outbreaks (https://www.cdc.gov).

In the United States and the United Kingdom, swimming pools are the most common sources of infection for cryptosporidiosis outbreaks (Chalmers & Johnston 2018). Based on a previous study, 444 cryptosporidiosis outbreaks were reported to the CDC between 2009 and 2017. According to these reports, 156 (35.1%) outbreaks were connected with treated recreational water, with pools (100 outbreaks), kiddie/wading pools (11 outbreaks), and water playgrounds (10 outbreaks) being the most frequently involved recreational water facilities (Gharpure et al. 2019). Recent advancements in our knowledge of the potential risks of recreational waters and swimming pools and our ability to investigate waterborne infections have played a part in the apparent increase in outbreaks at these locations (Chalmers 2012).

The efficacy of the treatment strategies in removing microbial pathogens from water is undetermined, and the frequency of reported outbreaks of gastrointestinal infections caused by chlorine-resistant protozoan parasites has been a rising concern (Wood et al. 2019). Cryptosporidium oocysts which are infectious after excretion and are excreted in numbers significantly larger than the human infectious dosage (10 oocysts) possess high resistance to chlorine disinfection. All of these features should be taken into account while developing successful cryptosporidiosis prevention methods, including improved guidelines for water treatment procedures in pools and efficient filtration systems in recreational centers. Implementing extensive decontamination measures, such as hyperchlorination of public-treated recreational waters in a cryptosporidiosis outbreak is imperative (Gharpure et al. 2019).

The concentration of the disinfectant, contact time, temperature, and pH (depending on the disinfectant) are the primary elements that determine disinfection efficiency. In many industrialized and developing countries, chlorine is the most commonly used disinfectant for water purification (Omarova et al. 2018). In the United States and Europe, pressure-activated membrane processes (microfiltration, ultrafiltration, nanofiltration, and reverse osmosis) play an essential role in the production of drinking water (Deborde & von Gunten 2008; Lundqvist et al. 2019; Mozia et al. 2020; Sousi et al. 2020). Other water treatment processes are based on alternative disinfectants, such as chlorine dioxide, ozone, and UV radiation, which have yet to prove solely effective. The efficacy of drinking water treatment can be improved by using a combination of disinfectants and filtration technologies, which eliminate and inactivate various microbial pathogens (Omarova et al. 2018).

In contrast to drinking water, most treated recreational water sites lack proper regulations (Chalmers 2012). Additionally, surveillance of recreational waters to evaluate the safety of swimmers is only partially possible (Boehm & Soller 2012). The most prevalent cause of swimming pool outbreaks is a failure in policies and procedures, poorly designed sanitation systems, and inadequate maintenance, which are significant barriers to preventing and controlling waterborne outbreaks (Lewis et al. 2015).

Climate change and global warming can enhance human exposure to waterborne pathogens, especially parasitic protozoa, by directly impacting the ecosystem and human lifestyles (Lal et al. 2019). Ongoing climate change may be closely related to extreme weather events (such as floods and storms with soil runoff) that accelerate the release of fecal-contaminated surface water into groundwater, affecting drinking water resources (Angelici & Karanis 2019). Since the amount and frequency of runoff, rainfall patterns, and temperature can potentially alter the state of microbial contaminations in recreational waters, it is crucial to predict how climate change will affect the burden of recreational water diseases globally (Boehm & Soller 2012).

Seasonality also affects the transmission of waterborne infections due to the higher frequency of fecal contamination of surface waters in rainy seasons. Furthermore, high temperatures lead people to consume more water and bathe more to refresh themselves. It is demonstrated that the incidence of cryptosporidiosis and giardiasis is increased in late summer and autumn, emphasizing the significant association between weather and the transmission of waterborne pathogens (Angelici & Karanis 2019).

Concerning drinking water sources, the WHO published new treatment standards for drinking water quality in 2017, and the second addendum was published in 2022 (www.who.int). The CDC teaches people to adopt safe swimming habits in the United States and preserve their private well water from parasitic contamination. CDC aims to deliver clean and healthy water to people worldwide through various initiatives, projects, and sanitation protocols (www.cdc.gov). Moreover, the CDC launched CryptoNet (https://www.cdc.gov/parasites/crypto/cryptonet.html) in 2010, the first molecularly-based surveillance system for parasitic disease in the United States. The data provided by CryptoNet can further reveal the epidemiology of Cryptosporidium and its chains of transmission and help improve evidence-based prevention programs (Hlavsa et al. 2017).

Most monitoring and notification systems suffer from underestimating due to similar features of the diseases, absence of manifestations, and self-limiting infections (Efstratiou et al. 2017). It is notwithstanding that the efficiency of reporting is different for each country and each pathogen and highly depends on the availability of research and relevant surveillance organizations and the epidemiological feature of the causal agent (Yang et al. 2012). Many developed countries prioritize viral and bacterial infectious diseases; consequently, their monitoring systems only include a small number of parasitic protozoa (Fletcher et al. 2012). However, Cryptosporidium is considered a contaminant of surface water supplies by regulations for public water systems in the United States (Stokdyk et al. 2019).

Learning more about the epidemiology of parasitic infections, especially in developing countries, is crucial. This necessitates proper reporting and documentation systems and approaches, including accurate pathogen isolation, speciation, and subtyping. Finally, each country must provide its own surveillance system for monitoring waterborne outbreaks (Baldursson & Karanis 2011; Efstratiou et al. 2017), but even in countries with such systems, outbreak investigation activities have repeatedly failed to detect sources of infection and etiologic agents precisely.

The current review focuses on waterborne parasite outbreaks reported between 2017 and 2022, and it is the fifth overview of its kind globally as a continuation of a series of reviews since 2007. It provides compact information and demonstrates that recorded outbreaks are still high. Not only Cryptosporidium and Giardia but also other neglected protozoan parasites have been reported in recent years, a fact that foretells a breakthrough in recording systems and scientific research on these subjects. There are undoubtedly unprecedented outbreaks, particularly in developing nations, the documentation of which may shed light on public health surveillance systems regarding parasitic diseases.

The national public health surveillance systems should consider appropriate outbreak reporting systems in each country, which is a fundamental approach to rapidly diagnosing and controlling outbreaks precisely. Safe water for bathing and drinking is critical for the health of a population, especially children.

The status of outbreaks caused by waterborne pathogens indicates the quality of bathing and drinking water. It is recommended that the water purification guidelines and monitoring of waters in each country take into account all parasitic infections of public health importance. Moreover, the recent efforts to improve water and sanitation facilities should be continued, as they are highly linked to outbreaks of diseases. Participants in large-scale sporting events including open-water swimming should be aware of the increased risk of gastrointestinal infection.

The current review underlines the importance of more large-scale and effective surveillance systems, especially in light of climatic events caused by climate change, which are currently on the rise globally and pose the threat of massive waterborne disease outbreaks. Finally, the data provided by our review can help policymakers, public health communities, and related industries (e.g., owners of swimming pools and recreational water facilities) give priority to the next steps for waterborne disease prevention.

This work did not receive any specific funding.

Pavlina Bourli received a scholarship from the Master Program ‘Coastal Zone Management’ of the Marine Sciences Department of the University of the Aegean, Greece.

All relevant data are included in the paper or its Supplementary Information.

The authors declare there is no conflict.