The purpose of this review was to highlight the most frequent biological indicators used to estimate the microbiological quality of drinking and recreational water. It was observed that the incorporation of other microbiological indicators should be considered to strengthen the decision-making process on water quality management and guarantee its safe consumption in recreational activities.
HIGHLIGHTS
- The incorporation of other microbiological indicators should be considered to strengthen the decision-making process on water quality management.
- The presence and concentration of bacterial, viral, and parasitic indicators are similar in several countries with diverse environmental conditions.
INTRODUCTION
Water is one of the most valuable natural resources, an essential element for life development and human activities [Romeu-Álvarez et al. 2012]. It is intended for different uses: human consumption, industrial processes, recreational activities of primary and secondary contact, ecological conservation, among others [Baird & Cann 2014].
Due to alterations in natural and anthropogenic processes, it is necessary to guarantee its quality so that there is no risk for humans and the environment [Samboni-Ruiz et al. 2007; Lugo & Lugo 2018]. Water is suitable for human consumption and domestic use, including personal hygiene and recreational activities, when it has low physical and chemical contaminant concentrations [WHO 2011; Lugo-Arias et al. 2020]. Although the use of water in recreational activities can bring health benefits, it can also generate adverse effects when it is contaminated [WHO 2000]. To assess the microbiological water quality, organisms are used as single indicators since their presence reveals contamination [Silva-Iñiguez et al. 2007].
Microbiological indicators of fecal contamination expose pathogenic organisms. They must be in higher concentration than pathogens and have similar survival characteristics [Noble et al. 2003; Pulido et al. 2005]. Fecal contamination indicators have proven to be an alternative to the difficulty of identifying and quantifying pathogens that cause water-origin diseases [Campos-Pinilla et al. 2008]. Microbiological quality control of water for human consumption and recreational use [ACH] requires pathogenic microorganisms' analysis [Silva-Iñiguez et al. 2007].
These analyses are hard to execute due to the great variety of cultivable pathogenic bacteria, isolation tests, the low concentration of aggressive species, the need for specialized laboratories, high economic costs, and time-consuming. To identify the presence of pathogens in a reliable way, water quality monitoring should be done by searching for fecal contamination indicators approved by international and national standards.
Microorganisms must meet the following requirements: [1] be a normal constituent of the intestinal microbiota of healthy individuals; [2] be present exclusively in the feces of homeothermic animals; [3] be present where pathogenic intestinal microorganisms are; [4] appear in high numbers; [5] facilitate isolation and identification; [6] be unable to reproduce outside the intestine of homeothermic animals. Their survival time must be equal to or greater than a pathogenic bacterium, and their resistance to environmental factors must be equal to or greater than fecal pathogens [Fernández et al. 2001]. The objective of this review is to highlight the most common microbiological indicators that are used to evaluate the microbiological quality of drinking and recreational water to identify new methods that optimize microbiological monitoring of water quality.
METHOD
The research was conducted in the Science Direct, Redalyc, Scielo, and in the Google Scholar search engine selecting peer-reviewed documents and published research articles in the last ten years, based on the following keywords: microbiological indicators, drinking water, and recreational water. Articles' selection criteria were as follows: [1] biological indicators to assess the microbiological quality of drinking and recreational water quality; [2] water bodies that were affected by outflow wastewater; [3] the impact of microbiological water quality on individuals' health; and [4] recreational water affected by bathers.
Recreational waters in artificial systems such as swimming pools were not considered as they have different environmental conditions, compared to those of interest in this work. For example, swimming pool water quality criteria are like those for the quality of drinking water, including microbiological parameters that differ from the water quality characteristics of natural bodies [Carrasquero Ferrer et al. 2020]. Also, swimming pool water is treated with different treatment methods, for example, disinfection with chlorine, UV-C radiation, ozone, membrane processes, among others [Dudziak et al. 2019; Skibinski et al. 2019]. The above is not feasible from a technical and economic point of view for natural water bodies such as seas and rivers.
Articles that did not meet the above criteria were excluded from the analysis. The guidelines were also based on microbiological quality standards for drinking and recreational water of the following organizations: the World Health Organization [WHO], the United States Environmental Protection Agency [EPA], and the standards of water quality of the European Union [EU]. These served as the basis for defining the microbiological water quality criteria in Latin America and the world.
RESULTS AND DISCUSSION
The most damaging effect of contaminated water has been the transmission of diseases by microorganisms that can inhabit humans [see Table 1] [Romero et al. 2009].
Table 1
Main microorganisms that transmit diseases in the water
Type of microorganismName of the microorganismDiseaseBacterias Escherichia coli Diarrhea and stomach pain Shigella spp. Shigellosis Vibrio cholerae Cholera Salmonella typhi Typhoid fever Salmonella spp. Salmonellosis Yersinia enterocolitica Yersiniosis Campylobacter jejuni Enteritis Viruses Enterovirus Various diseases: intestinal, respiratory, among others Rotavirus Various diseases: intestinal, fever, among others Adenovirus Various diseases: colds, conjunctivitis, among others Protozoa Giardia lamblia Giardiasis Cryptosporidium parvum Cryptosporidiosis Entamoeba histolytica Dysentery Helminths Ascaris lumbricoides Ascariasis
Type of microorganismName of the microorganismDiseaseBacterias Escherichia coli Diarrhea and stomach pain Shigella spp. Shigellosis Vibrio cholerae Cholera Salmonella typhi Typhoid fever Salmonella spp. Salmonellosis Yersinia enterocolitica Yersiniosis Campylobacter jejuni Enteritis Viruses Enterovirus Various diseases: intestinal, respiratory, among others Rotavirus Various diseases: intestinal, fever, among others Adenovirus Various diseases: colds, conjunctivitis, among others Protozoa Giardia lamblia Giardiasis Cryptosporidium parvum Cryptosporidiosis Entamoeba histolytica Dysentery Helminths Ascaris lumbricoides Ascariasis
Bioindicators serve as a complementary tool to evaluate water microbiological quality. Their application requires organism identification based on diversity indices, adjusting intervals that quantify water quality. For example, in Japan, the authorities in charge of water monitoring have illustrated guides of the organisms [bacteria, fungi, insects, amphibians, and fish] that can be found in water sources, including information on the tolerance of pollutants [heavy metals, dioxins, among others] to chemical compounds. This outlines information on the state of the water in real-time [Koschelow & Briedis 2013]. An organism is considered a bioindicator when its degree of tolerance is known, since not all of them offer information due to their eating habits, life cycle, and frequency with which they are found [Miravet Sánchez et al. 2016].
It is found that the presence and concentration of bacterial, viral, and parasitic indicators are similar in several countries with diverse environmental conditions [Liberatore et al. 2015], proving their use in different types of water [Campos-Pinilla et al. 2008]. Domestic contamination generates high health risks due to high concentrations of fecal microorganisms [Wade et al. 2015]. Therefore, it is important to have laboratory tests, exposing bacteria, viruses, and parasite concentrations in a precise moment with low economic costs. The most common bacteria used for drinking water control, wastewater, and recreational uses are total coliforms, fecal coliforms, Escherichia coli, and Enterococcus faecalis.
Clostridium perfringens has also been proposed as an indicator of distant fecal contamination in groundwater and as an indicator of the presence of protozoan cysts [Campos-Pinilla et al. 2008]. The presence of coliform bacteria is considered the best indicator of fecal contamination, and in the long term, it serves to monitor the effectiveness of control programs. Its use is advantageous because it gives a quick response to environmental changes such as pollution based on domestic discharges [Koschelow & Briedis 2013]. Numerous epidemiological studies in different aquatic environments have shown a relationship between coliform counts and the appearance of infectious diseases in humans.
However, various studies reveal that there is no significant relationship between these indicators and diseases related to seawater bathing [Vergaray et al. 2007]. Total coliforms and Escherichia coli [E. coli] have been suggested as reliable indicators of wastewater contamination. Recreational waters such as seawater are susceptible to fecal contamination, which can increase the health risk associated with swimming in contaminated beach water [Praveena et al. 2013]. In water analysis, the presence of E. coli indicates fecal contamination, with a positive correlation between the concentration of organisms and the amount of contamination [Romero et al. 2009].
Also, there is a trend towards linearity between the concentrations of thermotolerant coliforms and E. coli, which shows that such indicators could be used as a tool for river water microbiological quality [Romeu-Álvarez et al. 2012].
This includes fecal enterococci [FE] as a bacteriological indicator in marine waters for recreational use due to its resistance to seawater conditions, temperature, and relationship with gastrointestinal, respiratory, and dermatological diseases [Silva-Iñiguez et al. 2007]. Although no indicator can accurately determine water quality, enterococci have a predictive bent in marine environments, while somatic bacteriophages are useful bioindicators in seawater ecosystems [Janelidze et al. 2011]. In contrast, a study by Atoyan et al. [2011] suggests that FE and fecal coliforms [FC] are not reliable indicators of human fecal contamination in the Pettaquamscutt River due to inconsistencies found in high rates of false-positive and negative tests. Furthermore, there was a considerable amount of spatial and temporal variability in the reliability of the tests.
The inclusion of chemical nucleic acid-based methods for evaluating the microbiological quality of water can improve the identification of sources of human fecal contamination in water sources [Ahmed et al. 2015]. The United States Environmental Protection Agency requires the use of FE as an indicator of the risk of contracting a gastrointestinal illness from swimming activities in waters contaminated by FC. However, none of these indicators are definite for human fecal contamination because there is a wide variety of warm-blooded animals [Atoyan et al. 2011]. That is why several techniques have recently emerged for monitoring human fecal contamination sources based on indicators related to human beings.
Adolescentis bifidobacterium has been suggested as a specific bacterium of the human intestinal tract that can accurately identify human fecal contamination in freshwater. It is an anaerobic Gram-negative bacillus that grows exclusively in human intestines and has been suggested as an alternative fecal contamination indicator, since it does not survive in seawater, so it cannot reproduce itself in the environment. Its evaluation is carried out using a nested polymerase chain reaction [PCR] method for the exclusive detection of A. bifidobacterium in human feces.
It has been used in water and sediment samples [Atoyan et al. 2011]. On the other hand, the presence of pathogenic viruses has gained importance in recent decades due to epidemiological studies and improvements in environmental detection techniques.
However, these techniques require molecular procedures that are not within the reach of most water analysis laboratories [Moresco et al. 2012]. As an alternative, bacteriophages such as the ones that infect Bacteroides fragilis have been proposed. It was observed that its behavior is like some viruses that cause diseases of hydric origin, and its detection can be done in a few hours. Depending on the type of water and environmental conditions, the use of phages is recommended [Campos-Pinilla et al. 2008]. Monitoring coastal waters with total coliforms, FC, and E. faecalis phage indicators are recommended to prevent potential waterborne diseases [Janelidze et al. 2011].
Also, water sample testing is essential to verify the presence of indigenous microflora, such as pathogenic Vibrio species. It can be useful to predict and prevent waterborne diseases, such as cholera and Vibrio-related gastroenteritis [Janelidze et al. 2011]. The risk of infection by enteric viruses and other pathogens in the use of recreational waters has been described in some studies. For example, the coastal water quality in Brazil was evaluated through base fecal indicators, such as coliforms or Enterococcus spp. [Prasad et al. 2015]. However, bacterial contamination did not correlate with the presence of human enteric viruses [Wong et al. 2009].
Human viruses, such as adenoviruses [HAdV], hepatitis A [HAV], polyomaviruses [JCPyV], and human noroviruses [HuNoV], are associated with waterborne diseases. HAdV, HAV, and HuNoV can replicate inside the gastrointestinal tract and are excreted in high concentrations in feces of infected individuals [Moresco et al. 2012]. JCPyV is found in the urine of approximately 80% of adults, and the infection is spread during childhood. These viruses are usually spread into the water by industrial or agricultural activities [Lyons et al. 2015; Rusiñol et al. 2015]. Once in the water, these viruses are very stable and resistant to chemical agents such as UV radiation and chlorine.
The presence of viruses in various water environments has been revealed, highlighting the need to include them in the analysis of water quality. In a study carried out by Moresco et al. [2012], no correlation was observed between virus detection and FC presence. It can be assumed that these common bioindicators [FC] are not accurate in associating the risk of disease contraction with water environments [Rusiñol et al. 2015]. In the case of parasites, the presence of helminth eggs and protozoan cysts is the main risk to human health. The parasites most studied are giardia cysts and Cryptosporidium oocysts. The detection and counting of these parasites are an alternative health indicator since analysis is easy to carry out in laboratories with basic equipment [Campos-Pinilla et al. 2008].
Recreational water quality criteria
Water quality standards have been used through microbiological parameters that measure the degree of contamination [Bonamano et al. 2015]. Table 2 shows the microbiological quality criteria for primary contact with recreational water. Table 3 shows studies of microbiological indicators for recreational waters.
Table 2
Criteria for evaluating the microbiological quality of recreational water
Fecal indicatorAllowable limitNormativeTotal coliforms [TC]