Journal of Nature and Science, Vol.1, No.2, e44, 2015

Microbiology

 

Monochloramine for controlling Legionella in biofilms: how much we know?

 

Maria Anna Coniglio1, Stefano Melada2, Mohamed H Yassin3

 

1Department “G.F. Ingrassia” – Hygiene and Public Health, University of Catania, Catania, Italy. 2Sanipur srl, via S. Quasimodo, 25 I-25020, Flero (BS), Italy. 3Department of Infection Control and Infectious Diseases, University of Pittsburgh Medical Center, Pittsburgh, PA, USA

 


Prevention of Legionella in water system is a challenge especially when biofilm is present. Hospitals, in particular, deal with vulnerable population requiring additional protection against Legionella. Monochloramine (MC) has been used for small-scale hospital systems in Europe and the US only recently. This review focuses on Legionella in biofilm touching major practical challenges with water disinfection using MC. To date there are no published reviews on this topic so a critical and comprehensive update on the progress in the field was necessary. Scientific databases were reviewed for articles published between 1980 and 2013, containing the terms ‘Legionella’-‘Legionellosis’-‘Legionnaires’ Disease’ and ‘Biofilm’ and ‘Disinfection’-‘Legionella’ and ‘Monochloramine’.  In total, 36 articles were considered and divided in 5 groups to evaluate: (i) MC biofilm penetration, residual concentrations, production of disinfection by-products; (ii) influence of pipe material on biofilm formation and disinfectant penetration; (iii) effect of nitrification on MC decomposition rate; (iv) MC treatment and VBNC state of L. pneumophila in biofilms; (v) influence of protozoa on MC disinfection of biofilm. Among the antimicrobial agents, MC appears more effective for decreasing Legionella within the biofilms in vitro and in plumbing systems. Journal of Nature and Science, 1(2):e44, 2015.

 

Legionella | monochloramine | biofilm control | disinfection

 

On surfaces exposed to water a majority of microorganisms tend to form a ‘biofilm’, which is composed of extracellular polymeric substances (EPS) excreted by the microorganisms themselves. In a long distribution system, with wide variations in flow rates, biofilm would eventually be produced due to the sedimentation of organic particles. Because biofilms may contain enough bacteria to give an infective dose, they represent a potential health risk especially in hospitals, where patients constitute a vulnerable population. Furthermore, biofilms on distribution pipes contribute to bacterial regrowth and disinfectant decay in water.

Legionellae are ubiquitous and they could live as free-living planktonic forms or as intracellular parasites of protozoans (Hsu et al. 2011).  The organisms are also able to survive chlorination and thus enter water supply systems and proliferate in humid thermal habitats, including air conditioners, water systems, cooling towers, water fountains and hospital equipments. Legionellae are frequently found in biofilms on the surfaces of these systems, where they are more resistant to eradication compared to their free-living planktonic counterparts (Lin et al. 2011).

One of the key issues for controlling the growth of legionellae in biofilms is to recommend an effective disinfection method. Two main factors interfere with the activity of antimicrobial agents: (i) they may fail to penetrate through the EPS or bind to it before they reach legionellae (Simões et al. 2010); (ii) legionellae may become resistant to conventional chemical antimicrobials (Cooper  and Hanlon 2010).

At present, chlorination is the most commonly used treatment for Legionella control in water systems. Lapses in chlorination or discontinuous chlorination with chlorine or chlorine dioxide can lead to an increased resistance of biofilm bacteria to chlorine (Casini et al. 2008). Copper-silver ionization is currently used for Legionella control in water distribution systems and there is evidence that accumulation of copper and silver inside the biofilms is responsible for the prolonged bactericidal effect (Liu et al. 1998). Nevertheless, in Europe copper based products for drinking water disinfection have not been allowed since 1st February 2013 due to the Biocidal Product Directive 98/8/EC (EEA Commission Decision 1998). UK, Spain, the Netherlands and Poland, that have been using copper/silver ionization for Legionella control for a long period of time, obtained a derogation till 31st December 2017 providing that as of 1st January  2015 users should be actively informed about the immediate need to implement alternative methods.

Among the antimicrobial agents of relatively most recent application in the disinfection of water, monochloramine (MC) seems to be more effective for decreasing Legionella within the biofilms in vitro (Lee et al. 2010) and in hospital plumbing systems in the US (Kandiah et al. 2012) as well as in Italy (Marchesi et al. 2012; Casini et al. 2014). The aim of this review is to assess the available literature that supports the effectiveness of MC for controlling Legionella growth in biofilms.

 

METHODS

 

Search for literature was carried out using terms: ‘Legionella’ OR ‘Legionellosis’ OR ‘Legionnaires’ Disease’ AND ‘Biofilm’ AND ‘Disinfection NEAR Legionella’ AND ‘Monochloramine’. The search, including published papers between 1980 and 2013, was conducted in relevant chemical and biomedical databases: ACS Publications, Elsevier, JSTOR, Nature Publishing Group, PubMed, SDOS and Wiley Online Library. Considering the relatively new application of MC, non published research, letters and conference communications were also included. Inclusion criteria were: studies about the effectiveness of MC under in vitro conditions, and studies with more than three months of follow up in real conditions. The literature review has been divided in five main parts to evaluate the following aspects of the action of MC: (i) biofilm penetration, residual concentrations and production of disinfection by-products; (ii) influence of pipe material on biofilm formation and disinfectant penetration; (iii) effect of nitrification on decomposition rate; (iv) MC treatment and viable but nonculturable (VBNC) L. pneumophila in biofilms; (v) effect of protozoa on MC disinfection of biofilm.

After this initial search, 125 articles were identified for further review. Each article was evaluated with respect to the use of MC, if the technology was adequately tested for validity and/or accuracy against biofilm, and if the management of the water distribution system was associated with the control of Legionella. After this initial process, 32 articles were considered. Of those, 1 was a review article (Simões et al. 2010) and the others were surveys.

 

Table 1 shows a summary of the main studies on the effectiveness of MC against the biofilm.


 

Table 1. Description of noteworthy studies on effectiveness obtained through the application of MC

Authors

Study design

Results

Wolfe et al., 1990            

Experimental

Maintaining a chloramine residual of at least 1-2 mg/L could be sufficient to limit nitrifier growth in drinking water

Chen et al, 2000

Experimental

Reduction of biofilm viable cells counts better than free chlorine at neutral pH

Pintar et al., 2003               

Experimental

Effectiveness in controlling ammonia-oxidizing bacteria activity in the biofilm 

Thomas et al., 2004        

Experimental

Important increase in dead biomass proportion at a concentration of 0.5 mg l-1

van der Kooij et al., 2005  

Experimental

A model system of copper can temporarily reduce Legionella colonization but, after 2 years, biofilm colonization on copper, stainless steel and cross-linked polyethylene (PEX) pipes is very similar

Park et al, 2008              

Experimental

High-level MC residual in a low-nutrient water system linked with a reduction in biofilm density on pipe surfaces and to depressed potential functional/metabolic ability of the biofilm community                                                                                                        

Türetgen, 2008                

Experimental

Decrease of cell cultivability significantly begins at 1 ppm.  At 1.5-2 ppm environmental L. pneumophila enters VBNC state

van Schalkwyk et al., 2010  

Experimental

Even at concentrations as low as 1 ppm MC is able to penetrate complex biofilm matrixes like that in cooling towers

Dupuy et al, 2011 

Experimental

Similar effectiveness towards free or co-cultured L. pneumophila while chlorine and chlorine dioxide were less efficient on co-cultured L. pneumophila

Ramseier et al., 2011      

Experimental

Minimal reaction with organic matter but specific reaction with bacterial membrane at high oxidant exposures

Chien et al, 2012 

Experimental

More effectiveness in controlling biofouling (accumulation of micro-organisms, plants or algae) in cooling systems employing secondary-treated municipal wastewater compared to free chlorine    

Kandiah et al, 2012           

Observational

Better biofilm penetration than copper-silver ionization

Pressman et al, 2012     

Experimental

Limiting the free ammonia concentration during MC application slows the onset of nitrification episodes by maintaining the biofilm biomass at a state of lower activity. MC is able to penetrate biofilms 170 times faster than free chlorine

Dupuy et al, 2014             

Experimental

Less effectiveness than chlorine dioxide against Acanthamoeba cysts

 

 

Table 2. Description of noteworthy studies comparing the effects of MC vs. other oxidative disinfectants

Authors

Study design

Results

Kandiah et al., 2012

Observational

Appropriate flushing procedures and cleaning of the faucets with a bleach-based solution were unsuccessful in eradication of Legionella species despite adequate copper and silver levels. After monochloramine introduction into the hot water system faucets, all sensor faucets converted negative after only three weeks of monochloramine installation.

Marchesi et al., 2012

Observational

Legionella pneumophila contamination was followed in comparison with 2 other water networks in the same building using chlorine dioxide. MC significantly reduced the number of contaminated sites compared with baseline (from 97.0% to 13.3%, respectively), chlorine dioxide device I (from 100% to 56.7%, respectively), and device II (from 100% to 60.8%, respectively). MC could represent a good alternative to chlorine dioxide in controlling legionellae contamination in public and private buildings.

Pressman et al., 2012

Experimental

The initial MC mass delivery inside a nitrifying biofilm was 170 times greater compared to free chlorine for equivalent chlorine concentrations.

Chen et al., 2000

Experimental

Compared to free chlorine, MC had a longer residual effect in biofilm cells also at neutral pH. While the amount of biofilm removed by chlorine and MC was not statistically significantly different (p = 0.45), MC killed bacteria in the biofilm better than did free chlorine at neutral pH (p = 0.001).

Ercken et al., 2003

Experimental

The biocidal activity of MC against Naegleria lovaniensis was 8x weaker than that of hypochlorite but 2x stronger than that of peracetic acid.

Dupuy et al., 2011

Experimental

Comparison of the efficacy of chlorine, MC and chlorine dioxide against trophozoites of three different Acanthamoeba strains showed that MC was more efficient than chlorine and chlorine dioxide at the same level towards free or co-cultured L. pneumophila.

 

 


Biofilm penetration, residual concentrations and production of disinfection by-products

Despite its relatively low oxidative activity, MC is more effective than the other oxidative disinfectants (e.g. chlorine and chlorine dioxide). The ability of MC to better penetrate biofilms follows a dose-dependent effect. Table 2 compares MC to other disinfectants in controlling Legionella.It has been recently demonstrated that MC is able to penetrate biofilms 170 times faster than free chlorine (Pressman et al. 2012) and that even at concentrations as low as 1 ppm it is able to penetrate complex biofilm matrixes like that in cooling towers (van Schalkwyk et al. 2010).

Compared to the other oxidative disinfectants, MC has a longer residual effect in biofilm also at neutral pH (Chen and Stewart 2000). Maintenance of MC residual above 3 mg/L is needed to effectively control biofilm in cooling systems employing secondary-treated municipal wastewater as the only source of makeup water (Chien et al. 2012). Moreover, MC minimally reacts with organic matter but react specifically with bacterial membrane at high oxidant exposures (Ramseier et al. 2011).

The application of chloramines, as well as chlorine, may cause increased formation of highly carcinogenic nitrosamines and other disinfection by-products (DBPs) (Chang et al. 2011). Table 3  summarizes studies describing the effect of MC on DBPs. A recent study investigating the effects of corrosion products of copper in plumbing systems on N-nitrosodimethylamine (NDMA) formation from DMA found that the transformation of MC to dichloramine and complexation of copper with DMA were involved in elevating the formation of NDMA by copper at pH 7.0 (Zhang and Andrews 2013). Anyway, MC generally results in lower concentrations of DBPs compared to the other oxidative disinfectants. It has been recently demonstrated that DBPs levels in filtered river waters, as well as in coagulated surface waters collected from water treatment plants are generally higher after chlorination than after chloramination (Farré et al. 2013).



Table 3. Description of noteworthy studies on the production of DBPs through the application of MC*

Authors

Study design

Results

Chang et al., 2011

Experimental

NDMA was the dominant species of nitrosamines and the levels of other nitrosamines were too low to show specific formation characteristics following treatments. The presence of bromide shifted the DBPs species into brominated DBPs, and treatment with MC generated a higher proportion of brominated DBPs than those obtained with sodium hypochlorite.

Zhang et al., 2013

Experimental

The investigation on the effects of corrosion products of copper on NDMA formation from DMA showed that the transformation of MC to dichloramine and complexation of copper with DMA were involved in elevating the formation of NDMA by copper at pH 7.0.

Lu et al., 2009

Experimental

Chloramination of the dissolved natural organic matter (DOM) fractions yields much less THMs and HAAs than chlorination with the increase of disinfectant dosage, contact time and dissolved organic carbon content.

Farré et al., 2013

Experimental

Chlorination formed higher concentrations of DBPs or more potent DBPs in waters collected from three different drinking water treatment plants, along with reverse osmosis permeate from a desalination plant.

* DBP:Disinfection byproducts, NDMA: N-nitrosodimethylamine, DMA:Dimethylamine, THM: Trihalomethanes , HAA: halogenated acetic acid

 


Influence of pipe material on biofilm formation and monochloramine effectiveness

Another factor on formation and persistence within the biofilms of Legionella is the influence of pipe material. Copper piping has been in use in water systems to minimize the risk of Legionellosis because copper may prevent colonization of the pipe and could inhibit the biofilm growth. Anyway, a model system of copper can temporarily reduce Legionella colonization but, after 2 years, biofilm colonization on copper, stainless steel and cross-linked polyethylene (PEX) pipes was very similar (van der Kooij et al. 2005).

The decomposition rate of MC may be enhanced by copper due to the formation of a Cu(II)-humic acid complex (Fu et al. 2009). A laboratory experiment has confirmed that MC could decay rapidly only in the presence of new copper pipes, providing a possible explanation for the rapid disinfectant loss in the new buildings (Nguyen et al. 2012).  Nevertheless accumulation of Cu(II) ions could occur also after years of use of copper/silver ionization. Figure 1 shows a longitudinal section of a water pipe after more than 10 years of use of copper/silver ionization. Note the severe corrosion within the pipe wall. Copper corrosion products can thus affect the MC disinfection by affecting its decomposition rate. An adequate chloramination system should be put in place to reduce MC decomposition rate and to avoid accumulation of DBPs.

 

 

Figure 1. Longitudinal section of a water pipe after more than 10 years of use of copper/silver ionization. (Picture from Boffardi BP, Hannigan JM. A limited evaluation of pitting corrosion of copper piping in a hospital domestic hot water system using copper-silver ionization for Legionella control. AWT, Mohegan, 2013.)

 

Effect of nitrification on decomposition rate of monochloramine into biofilm

Chloramination provides a source of ammonia promoting the growth of nitrifying bacteria within the biofilms. Nitrifying bacteria can grow in the presence of MC due to their ammonia and nitrite oxidizing characteristics. Biofilm grown on pipe surfaces can harbor nitrifiers, belonging primarily to Nitrosomonas, Nitrobacter and Nitrosospira (Lipponen et al. 2004). Nitrification in drinking water distribution systems may result in water quality degradation and subsequent noncompliance with existing regulations. Accelerated chloramine decay is related to high levels of nitrification and when nitrification is absent chloramine is expected to better penetrate iron biofilms (Lee et al. 2011). A possible explanation for these evidences is that the presence of high free ammonia concentration due to MC decomposition allows the microorganisms deeper within the biofilm to remain active during MC application. Moreover, once initiated, nitrification is very hard to stop because CT value (product of disinfectant concentration and contact time) is too low in biofilm where the right residual MC cannot be maintained. In fact, limiting the free ammonia concentration during MC application could slow the onset of nitrification episodes by maintaining the biofilm biomass at a state of lower activity (Pressman et al. 2012).

Nonetheless, although there is evidence that maintaining a chloramine residual of at least 1-2 mg/L could be sufficient to limit nitrifier growth in drinking water  (Wolfe et al. 1990), it has been shown that greater MC residuals may be required to inactivate bacteria inside the biofilms (Park and Kim 2008).

The degradation of the hypochlorite used to produce MC can lead to an increased level of free ammonia and this can affect the disinfection effectiveness of the in situ produced MC. Increased levels of Legionella occurred for a severe degradation of the hypochlorite reagent despite MC levels were in the desired range and, only after draining and cleaning of the reagent tank, free ammonia and Legionella were reduced to negligible levels. A major US University-based medical system experienced similar issue as high temperature in the storage room caused degradation of hypochlorite (personal data).

 

Monochloramine treatment and viable but nonculturable (VBNC) Legionella pneumophila in biofilms

After disinfections with chlorine compounds, L. pneumophila can completely lose its cultivability but do not lose viability entering the viable but nonculturable (VBNC) state. Decrease of cell cultivability significantly begins at 1 ppm dosage of MC, while at 1.5-2 ppm environmental L. pneumophila enters VBNC state (Türetgen 2008).    

It has also been shown that up to 20 ppm MC concentration, Legionellae enter VBNC state and are still able to synthesize virulence factors. Nonetheless, at this concentration, attempts to resuscitate VBNC cells with amoebas failed (Alleron et al. 2013).  This suggests that the accumulation of virulence factors by VBNC cells may not be sufficient to maintain their virulence.

Anyway, disinfectants’ in vitro activity is less effective in field applications and at the moment there is a lack of studies evaluating the effect of long exposures to MC in real water systems.

 

Effect of protozoa on monochloramine disinfection of biofilm

Within biofilms, free-living amoebae (FLA) may favor the multiplication, dissemination and virulence of Legionella. Intracellular parasitism of FLA is probably at the origin of the rapid re-colonization of water distribution systems by Legionella generally observed immediately after stopping a disinfection program (Thomas et al. 2004). A recent experience in an Italian hospital (personal data) showed a rapid and massive re-colonization of the water distribution system only two weeks after stopping a 2-months disinfection program with MC caused by a temporary failure of the device. The possible presence of FLA throughout the entire water system could explain the above results, thus indicating the necessity of a continuous disinfection with MC.

Up to date, only a few studies have been focused on the effectiveness of MC against pathogenic FLA. Under laboratory conditions the biocidal activity of MC against Naegleria lovaniensis was 8x weaker than that of hypochlorite but 2x stronger than that of peracetic acid (Ercken et al. 2003). This evidence makes MC a good candidate for inactivation of pathogenic Neaegleria species and an ecologically less harmful alternative to hypochlorite.

Moreover, comparison of the efficacy of chlorine, MC and chlorine dioxide against trophozoites of three different Acanthamoeba strains showed that MC was more efficient than chlorine and chlorine dioxide at the same level towards free or co-cultured L. pneumophila (Dupuy et al. 2011). Nonetheless, despite its better effectiveness against amoeba trophozoites, MC appears less effective than chlorine dioxide against Acanthamoeba cysts (Dupuy et al. 2014).

 

CONCLUSIONS

The presence of Legionella within a biofilm makes eradication from water system very difficult. Among the antimicrobial agents, MC seems to be more effective for decreasing Legionella within the biofilms in vitro as well as in model plumbing systems. As of to date there are no published reviews on this topic, a critical and comprehensive update on the progress in the field is necessary.


 

 

 


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__________

Conflict of interest: No conflicts declared.

Correspondence author: Dr. Maria Anna Coniglio

Department “G.F. Ingrassia” – Hygiene and Public Health

University of Catania, via Santa Sofia 87, 95123 Catania, Italy.

Tel.: +39 095 3782087; Fax: +39 095 3782175.

E-mail address: ma.coniglio@unict.it

© 2015 by the Journal of Nature and Science (JNSCI).