Opportunistic Premise Plumbing Pathogens

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2	format correct	Catherine Yang	-11 word(s)	3007	2022-04-29 05:17:23	\|

This entry is adapted from the peer-reviewed paper 10.3390/w14071129

Opportunistic premise plumbing pathogens (OPPP) are microorganisms that are native to the plumbing environment and that present an emerging infectious disease problem. They share characteristics, such as disinfectant resistance, thermal tolerance, and biofilm formation. The colonisation of domestic water systems presents an elevated health risk for immune-compromised individuals who receive healthcare at home.

opportunistic premise plumbing pathogens drinking water biofilm disinfectant resistance

1. Introduction

Opportunistic premise plumbing pathogens (OPPPs) are waterborne microorganisms that inhabit water distribution systems and premise plumbing ^[1]. OPPPs have been distinguished from other drinking water contaminants as they are adapted to growth and proliferation in drinking water systems ^[2]. This growth can be promoted and influenced by water stagnation, increased water residence times, the application of subinhibitory disinfectant concentrations, and fluctuating water temperatures ^[3]^[4]. Because of the complex design and age of residential plumbing infrastructure, the maintenance of parameters such as these is an ongoing challenge ^[5]. OPPPs share characteristics, such as disinfectant resistance, biofilm formation, amoeba digestion resistance, and growth under oligotrophic conditions. Although Legionella pneumophila, Pseudomonas aeruginosa, and Mycobacterium avium have been considered model OPPPs, the definition has expanded to include species such as Acinetobacter baumannii, Stenotrophomonas maltophila, Helicobacter pylori, Aeromonas hydrophila, and Methylobacterium spp. ^[1]. Of all the waterborne disease transmission in the US in 2014, Legionnaires’ disease, pneumonia caused by Pseudomonas spp. and nontuberculous Mycobacteria infection have been attributed with the largest number of deaths ^[6]. Legionella spp. infection almost exclusively presents as a nontransmissible respiratory infection, such as Legionnaires’ disease or Pontiac fever ^[7], whereas other OPPPs, such as P. aeruginosa, Mycobacteria spp., and A. baumannii, each cause a range of potentially transmissible and antimicrobial-resistant infections, including pneumonia, septicaemia, and dermal infection, which further complicate their management ^[1].

Legionnaires’ disease is the only OPPP-caused infection that is a nationally notifiable disease in the US. The CDC reported that, in 2018, there were approximately 10,000 cases of Legionnaires’ disease ^[6]. However, it has been suggested that the incidence of Legionnaires’ disease was underestimated, and that the true number of cases may be 1.8 to 2.7 times higher than what is reported. Additionally, the origins of these infections are rarely identified, as environmental sampling is typically only conducted in response to extended outbreaks. Outbreaks in domestic settings are less easily detected because of the inherent low numbers of exposed occupants at individual premises; although the sum total of exposed individuals is likely to exceed those in large buildings. As such, it is difficult to quantify the total public health risk that is associated with various environmental reservoirs. The elderly, newborns, and those with compromised immune systems are especially vulnerable to waterborne infections. The number of individuals with conditions that may put them at risk of OPPP infection, such as advanced age, cancer, and immunodeficiency, are increasing ^[6]. Life expectancy has increased by more than six years since 2000, and the number of cancer diagnoses worldwide is set to increase by 47% in 2040 ^[8]. At-home healthcare has emerged as an alternative to extensive inpatient hospital stays ^[9]^[10]. Services such as chemotherapy, tracheotomy care, and ventilator support, are being facilitated by government healthcare and disability support schemes in countries such as the United Kingdom, the US, and Australia ^[11]^[12]^[13]. These “at home” alternatives are receiving further attention in the wake of the COVID-19 pandemic because of the need to reduce the burden on the healthcare system and to support those with potential long-term respiratory side effects ^[14]. When in a hospital or healthcare facility, a patient’s risk of healthcare-associated infection (HAI) and exposure to environmental risks has been minimised by the implementation of infection control and prevention guidelines, with varying success ^[15]^[16]. Despite such initiatives, the US CDC reported significant increases in four of the six monitored HAIs from 2019–2020, even with decreased surveillance activities due to shortages in personnel and equipment ^[17]. Conversely, patients receiving healthcare in residential properties may have poor access to plumbing, sanitation, and ventilation, which are overlooked by these guidelines ^[10]. Major outbreaks of OPPP infection are typically associated with larger buildings, such as hospitals, which has resulted in drinking water guidelines that focus on the unique risks that are posed by this infrastructure. Without the consistent environmental surveillance of residential properties, which can vary significantly in size, age, occupancy, and infrastructure quality, it is difficult to identify and quantify the unique risks that are posed by OPPPs in these settings. If healthcare services continue to move patient care away from the hospital environment, further research is required in order to identify and quantify the potential risks, and to tailor infection surveillance and prevention guidelines to the patient and to their property.

2. Control of Opportunistic Premise Plumbing Pathogens

A multibarrier approach has been suggested as the most effective approach to control the growth and proliferation of OPPPs. This risk-based approach allows for the failure of one barrier to be compensated for by the effective maintenance of the additional barriers ^[18]. The barriers that are used in the production of safe drinking water include the protection of the source water, the maintenance of the infrastructure, filtration, and disinfection ^[19]. However, the biological stability of drinking water is dynamic, and it can be affected by variables such as the nutrient availability, the disinfectant selective pressure, and the temperature, which are unique to each distribution system. The identification of the barriers where interventions can be applied is a prerequisite for this approach. The singular, complex, and diverse nature of building water system environments may compromise the successful implementation of strategies that are aimed at reducing the microbial load ^[20]. Reducing the levels of biodegradable organic matter and the assimilable organic carbon in drinking water prior to distribution has been shown to reduce biofilm formation and growth in premise plumbing ^[21]. Ironically, disinfection agents such as monochloramine and chlorine, which are aimed at reducing the microbial load, may cause an increase in the assimilable organic carbon because of the oxidation of organic carbon, which results in the potential re-growth of the microorganisms in DWDSs ^[21]^[22]. It is essential to monitor the microbial, engineering, and chemical parameters of drinking water on a routine and high-frequency basis throughout the distribution system in order to validate the efficacy of the current barriers, particularly at the point of use. If these barriers are found to be inadequate, additional stages of disinfection, or a re-evaluation of the identified barriers, can be instigated by water utilities and homeowners in order to minimise the uncontrolled growth of OPPPs.

Current drinking water treatment principles are tailored to waterborne pathogens that primarily originate from human and animal faecal contamination. Disease from these organisms is generally contracted via ingestion. However, the diseases with the largest numbers of deaths attributed to waterborne transmission in the US were infections with non-tuberculous mycobacteria, Pseudomonas spp., and Legionnaires’ disease ^[6]. In the majority of these cases, ingestion is not the route of infection. OPPPs are characterised by their resistance to commonly used disinfectants, such as chlorine. When primary disinfection strategies are developed for faecal indicator bacteria, the premise plumbing environment will select for the dominance of disinfectant-resistant pathogens ^[2]. Consequently, these strategies may select for diseases that are acquired by means other than the faecal–oral route. The US EPA National Primary Drinking Water Regulations state that chloramines (4 mg/L), chlorine (4 mg/L), and chlorine dioxide (0.8 mg/L) are added to drinking water to control microorganisms. The WHO reviewed the national drinking water quality guidelines of 104 countries and found that 66 countries had set regulatory values for the chlorine in the municipal drinking water. This value ranged from 0.1 to 5 mg/L, and it was not always clear if this value referred to the free or total chlorine ^[23]. As a consequence of this variation, in addition to other environmental variables, such as climate, the persistence of OPPPs in DWDSs, and the subsequent risk of infection, will differ between counties. It is difficult to maintain disinfectant residual throughout the distribution system because of the reactions with dissolved nutrients, secreted protective exopolysaccharides, and sediments. Water utility companies are responsible for managing the water treatment throughout the distribution network, to the property meter. Once the water enters a premises, the water quality is the responsibility of the property owner. Larger commercial buildings, such as hospitals, may opt to conduct additional onsite water treatment to manage waterborne healthcare-acquired infections; however, this rarely happens in residential properties ^[19]. Often, residential homeowners are not aware of the water quality changes that may occur from the water meter to their tap, or of the infrastructure that may be contributing to these changes. When present in premise plumbing biofilms, OPPPs may become more tolerant to disinfection methods. Not all OPPPs are resistant to the same levels of residual disinfection, and the maintenance of a residual level that is high enough to control highly resistant pathogens, such as Mycobacterium spp. and Legionella spp., would be problematic. Factors such as water stagnation, temperature fluctuations, and the physical integrity of premise plumbing infrastructure can influence the efficacies of residual disinfectants. Sublethal concentrations of disinfectants such as chlorine may reduce the population diversity and select for the growth of disinfectant-resistant OPPPs ^[1].

The maintenance of the water temperature has been highlighted in global drinking water guidelines as a factor that can be manipulated to minimise pathogen growth. The WHO guidelines recommend that cold water be stored below 20 °C, and that hot water be stored above 60 °C ^[24]. However, both hot- and cold-water temperatures can be difficult to maintain during seasonal changes, and in large or old buildings. For example, the larger building sizes in Flint, Michigan, have been linked to higher levels of recoverable Legionella spp., when compared to single-story buildings, because of the zones of warm stagnant water that are favourable to bacterial growth ^[25]. Once pathogens have colonised premise plumbing, and particularly when they are present as a biofilm, hot-water flushing may be rendered ineffective. L. pneumophila was isolated from the bathroom and kitchen hot-water taps of a 1972 apartment after a case of potentially domestically acquired Legionnaires’ disease was reported in a one-week-old newborn. Epidemiological investigations found that the water leaving and returning to the heat exchanger was below the recommended hot-water temperatures of 53 and 40 °C, respectively. The hot-water temperatures were subsequently increased, and no Legionella spp. were detected from the water leaving the hot-water exchanger. However, Legionella spp. were still detected in the hot water returning to the heat exchanger, which indicates the colonisation of the plumbing infrastructure ^[26]. The heating element of an electrically heated water-storage tank is suspended in the water, and does not reach any sediment at the bottom of the tank that is likely to harbor OPPPs ^[27]. Instantaneous hot-water systems have been suggested as an appropriate alternative to continuous-flow or water-storage tanks to minimise the amount of warm water that remains stagnant in residential properties ^[28].

Point-of-use (POU) filters have been suggested as a method to reduce the exposure to OPPPs from a contaminated water source or device ^[29]. These POU filters may be used in conjunction with point-of-entry filters, which can be installed at the properties main water intake in order to address the water quality degradation from the municipal DWDS ^[30]. This intervention has been effective in healthcare settings at eradicating Legionella spp. and P. aeruginosa, and it has resulted in the elimination of infection ^[31]^[32]. A cost–benefit assessment estimated that the installation of POU devices as the final stage of water treatment could prevent 3.4 million cases of disease and mortality due to waterborne pathogens, which would result in USD 1814 of averted costs per disease case ^[33]. As with other barriers, the maintenance of POU filters is critical. Bacterial numbers may amplify in the POU filter if they are not maintained, and if it is not operated properly ^[34]. Biofilms on plumbing fixtures, such as tap faucets and shower heads, provide a source of nutrients and protection for pathogens, such as S. aureus and A. baumannii, which can disseminate AMR. Cross-contamination between the kitchen environment and water-related devices during inappropriate cleaning practices has been identified as a source of bacterial transmission ^[35]. Beta-lactam resistant genes were detected in S. maltophila and P. aeruginosa shower-drain isolates ^[36]. This colonisation may occur if an individual is a carrier of the antimicrobial-resistant infection, and it is of particular concern when considering the colonisation of shared plumbing fixtures. Significant growth of P. aeruginosa was found in a nursing home whirlpool bath after a resident with a known P. aeruginosa toe infection used the shared facility daily along with other residents, irrespective of incontinence, infection, or skin problems ^[37]. Carbapenem-resistant OPPPs, such as Acinetobacter spp. and P. aeruginosa, have been identified as antibiotic-resistant threats by the CDC, and have resulted in 41,100 infections and 3400 deaths, combined, in 2017 ^[38]. If installed and maintained properly, POU filters may be an appropriate and affordable additional protection barrier for the increasing vulnerable population receiving healthcare at home ^[39].

The growth of OPPPs in drinking water and water-related devices may be unavoidable, but their impact is manageable. Although OPPPs are identified on the basis of their shared characteristics, they are members of widely different taxonomic groups and, therefore, they react to prevention measures differently. The current drinking water guidelines must acknowledge the growing complexity of plumbing infrastructure and the limitations of disinfection procedures on dynamic bacterial communities. It is not sufficient to rely solely on the water industry to provide and maintain safe drinking water, from treatment to the point of use. Additional preventative measures should be considered on an individual basis for people who are considered to be at particular risk of developing a waterborne HAI, such as the elderly, infants, and those with weakened immune systems ^[40]^[41].

3. Pathogen Detection from Environmental Sources

Culture-based methods for the detection of indicator bacteria have long been held as the “gold standard”, as they detect viable target organisms. However, an examination of the full spectrum of potentially pathogenic microorganisms is not a feasible part of routine monitoring protocols ^[42]. The number of pathogens that are targeted by culture-based epidemiological studies is limited by the selective media that are chosen prior to sampling, and by the time that is required to handle the samples. One of the defining characteristics of an OPPP is its ability to adapt and proliferate in nutrient-poor environments, which often results in slowed growth rates, or the conversion to a VBNC state ^[7]. For example, OPPPs such as Legionella spp., Mycobacterium spp., and Methylobacterium spp. may take up to 14 days before the first appearance of colonies on agar ^[1]. Nutrient-rich selective agars and pretreatment steps, such as heating or acidification, are typically used to combat competitive overgrowth by faster-growing organisms ^[43]. These selective media have some drawbacks, as they may inhibit or restrict the growth of the target organisms, and they may also induce the VBNC state ^[7].

Challenges may arise when trying to enumerate VBNC bacteria by using culture-based methods ^[44]^[45]^[46]^[47]. VBNC bacteria are stressed or injured cells that are characterised by their lack of proliferation on agar, which leads to an underestimation of the viable cells in a sample. Although they are difficult to enumerate on routine agar, VBNC cells are not considered dead, as they have an intact membrane, contain undamaged genetic material, and are metabolically active. Nutrient-depleted media, such as R2A agar, have been recommended to enhance the recovery of environmental waterborne pathogens ^[48]. The growth of OPPPs on selective media was used by 162 studies, which included 11 different types of media for Pseudomonas spp. International standard methods have been published for the enumeration of the OPPPs, L. pneumophila and P. aeruginosa, from environmental water samples ^[49]^[50]. Only 15 and 3% of the studies that have investigated the presence of Legionella spp. and Pseudomonas spp., respectively, have referenced the ISO protocols. The US Environmental Protection Agency recommends ISO 11731 and the CDC standard culture methods to monitor the presence of Legionella spp. in premise plumbing. It is valuable to maintain consistent sampling and testing protocols in order to understand and implement effective risk-assessment protocols. To date, such international standards have not been published for the enumeration of the OPPPs, Acinetobacter spp., Aeromonas spp., Helicobacter spp., Methylobacterium spp., Mycobacterium spp., and Stenotrophomonas spp. from environmental water samples. This lack of standardisation has resulted in significant variation between the sampling techniques and the enumeration protocols that were employed by the studies that are included.

Several nucleic acid and immunology-based protocols have been developed to address the limitations that are associated with the traditional culture-dependent methods. These include techniques such as polymerase chain reaction (PCR), microarrays, and fluorescence in situ hybridisation (FISH) ^[51]^[52]^[53]. The CDC have recommended PCR methods for routine Legionella spp. testing in conjunction with spread plate culture techniques. Similar to many OPPPs, Legionella spp. have been shown to replicate intracellularly within macrophagic hosts, which results in a thickened outer membrane, greater resistance to environmental stress, and the ability to readily enter a VBNC state. Seven of the studies that were included used both culture and PCR methods for the detection of Legionella spp. Although PCR techniques are considered to be more sensitive than culture-based techniques, the commonly used protocols do not distinguish between the DNA from viable, injured, or dead cells that persists in the environment, which may contribute to the overestimation of pathogens in a sample ^[54]. Propidium monoazide (PMA) quantitative PCR is a practical alternative that can differentiate between live, dead, and membrane-damaged cells. PMA is an intercalating molecule that selectively binds to the DNA of viable and membrane-damaged cells. This bond inhibits the PCR amplification of dead bacterial DNA, thereby reducing the likelihood of false positive results and the overestimation of the pathogen concentration ^[55]. Alternative techniques, such as FISH, have been proposed to bridge the gap between the underestimation of contamination by culture, and the potential overestimation by PCR ^[56]. Buchbinder et al. (2002) compared the specificity and sensitivity of culture, PCR, and FISH for the detection of Legionella spp. in residential drinking water ^[57]. It was found that, although PCR was significantly more sensitive than FISH, FISH was more specific (72%, compared to 47% for PCR). It was suggested that, because the FISH assay was able to detect VBNC cells, it is potentially a better alternative than PCR for future routine testing protocols. However, this approach is limited by the high costs that are associated with the user training, the protocol optimization, and the need for high pathogen densities that may not be present in many environmental samples ^[58].

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Claire Hayward

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Confirm

1. Introduction

2. Control of Opportunistic Premise Plumbing Pathogens

3. Pathogen Detection from Environmental Sources

References