The Pall Medical-sponsored event provided plenty of ‘food for thought’ for estates and facilities personnel responsible for hospital water systems, and clearly demonstrated how difficult and persistent a foe organisms such as Pseudomonas aeruginosa and Legionella pneumophila, which, if left unchecked, pose significant patient health risks, can be.
Infection with Pseudomonas aeruginosa has long been considered an endemic hazard for vulnerable patients on intensive and augmented care units, but the problem was catapulted into the limelight earlier this year with the tragic deaths of four babies in neonatal units in Northern Ireland (HEJ – May and June 2012). As investigations firmly established the source of infection as tap water, a flurry of new guidance – from the Regulation and Quality Improvement Authority (RQIA) in Northern Ireland,1 and the Department of Health (DH) in England and Wales2 – set out definitive guidelines that acknowledge the potential role of contaminated hospital water in the transmission of Pseudomonas to patients. The latest DH advice,2 published in late March, builds on previous 2010 guidelines, issued following earlier incidents in augmented care wards, where tap water was identified as the source of persistent colonisation with pseudomonad bacteria. The new guidelines emphasise the importance of water monitoring via regular sampling, risk assessment, water safety plans, and best practice hand hygiene. If potential water contamination problems are detected, recommendations include use of an alcohol hand rub to supplement handwashing, and of sterile or filtered water, or water from a known, bacteriafree source. Point-of-use (POU) filters are also recommended, long-term in some cases.
An established link
The link between Pseudomonas infections and water is not new, however. According to Professor Matthias Trautmann, director of Infection Control at the Institut für Krankenhaushygiene (Institute of Hospital Hygiene) at the Klinikum Stuttgart, the connection was described as far back as 1993 in a children’s hospital in Freiburg in Germany.3 Speaking at a specialist waterborne diseases ‘masterclass’ held recently in Nottingham, Prof. Trautmann, well known for his investigations into Pseudomonas transmission, joined other leading experts discussing not only the control of Pseudomonas, but also other problematic waterborne pathogens such as Legionella, the cause of Legionnaires‘ disease. The meeting was chaired by Dr Tim Boswell, consultant microbiologist at the Nottingham University Hospitals NHS Trust, and sponsored by Pall Medical.
Pseudomonas epidemiology
The audience was introduced to Pseudomonas by Professor Kevin Kerr, director of Infection Control for Harrogate and District NHS Foundation Trust, assistant editor of The Journal of Hospital Infection, and chair of the European Society for Clinical Microbiology and Infectious Diseases’ Study Group on Food and Waterborne Infection. He described how pseudomonad bacteria, including Stenotrophomonas maltophilia, can be found in most moist environmental niches in hospitals, including potable water from bottles, cold water dispensers, and ice machines. The bacteria are very well adapted to live in damp conditions, due to their ability to form ‘biofilm’, a sticky extracellular matrix which allows them to attach to inanimate surfaces. They are also able to resist, and even destroy, the free-living aquatic amoebae that ‘graze’ on other organisms. Pseudomonads do not present a problem to all patients, but can be lethal for the increasing number of immunocompromised individuals. In the UK, Pseudomonas causes some 10% of nosocomial infections, being one of the most common causes of ventilatorassociated pneumonia (VAP). As well as significant morbidity, mortality associated with infection in vulnerable patients can be high for those undergoing chemotherapy for solid organ and haematological malignancy, and in those with severe burns, for example. Onset of infection in neutropenic patients can be very rapid, and, unless promptly treated, can result in severe sepsis and other complications such as ecthyma gangrenosum.
Antibiotic resistance
Rapidly rising antibiotic resistance to commonly used broad spectrum antibiotics is making Pseudomonas infections increasingly difficult to treat. Resistance to ceftazidime, for example, is now as high as 50% in some places in Europe,4 while some strains are resistant to all antibiotics except colistin, used as ‘a last resort’ due to its toxicity. Prof. Trautmann noted that Pseudomonas is an obligate aerobe, which needs both air and moisture, adding that Legionella and Pseudomonas grow in different water system locations – with Legionella thriving in central water tanks and dead end pipes, resulting from modifications in older plumbing systems, where, rather than destroying amoebae, it exploits them as a host. Pseudomonas, meanwhile, is ‘mainly an endpoint problem’, as its need for air makes it more likely to grow in taps, mixing valves, tap aerators, and rubber tubing. Outbreaks may result from contaminated humidifiers, bronchoscopes where filters have not been used for the final rinse, ventilators, or even contaminated care products. However, ‘in epidemics’, Professor Trautmann said, ‘a large proportion of infections is due to transmission between patients’. He added: “However, many studies conclude that horizontal transmission has occurred if two patients have the same clone, yet the tap in the patient’s room has not been checked, so some conclusions may be wrong. Nevertheless, the mean of all the studies indicates around a 50% involvement.”
Prospective studies and outbreaks
Prof. Trautmann and his former team at Ulm University Hospital undertook one of the first definitive prospective studies to establish whether taps might be a source of P. aeruginosa (the most common species) infections. Carried out on a 12- bedded intensive care unit over 22 weeks, extensive water sampling revealed all water outlets were harbouring distinct genotypes over prolonged periods. Over a seven-month period, five (29%) of 17 patients were infected with genotypes also detectable in tap water. Intensive cleaning and autoclaving of the tap aerators did not resolve the problem. Prof. Trautmann’s team concluded that, where the source of endemic P. aeruginosa infections is unknown, the water system should always be sampled.5 During a 144- week extension of the study on this ward, 45 patients were infected or colonised with Pseudomonas, three suffering from bloodstream infections. In 12 cases the organism had been detected previously in the water tap of the same room, while in six further cases, the infective organism had been found in the tap of an adjacent room. In total, 18 could be attributed to the organism’s presence in the tap water. “What was clear from this prospective study,” Prof. Trautmann explained, “was that taps could play a part in patients’ infections, while, in other cases, taps had become colonised with Pseudomonas from a patient already colonised on arrival on the ward.”6
Microaspiration route
Prof. Trautmann said pseudomonad bacteria were most likely to travel from tap water to the patient via microaspiration through a ventilator tube during facial washing, or via gauze dressings that had become wet during washing. His recommendations for avoiding this transmission route included staff training to ensure tap water is never used for oral care, face, or neck washing, or dissolving oral medications. Alcoholic hand rub should be used after, rather than before, handwashing at patient sites, and dumping of used wash water in patient room sinks, which may contaminate taps, should be avoided. The Professor also recommended testing of outlets in all ICU rooms. While taps consistently negative were not considered problematic, the aerators in positive taps should be cleaned and changed regularly, while central chlorination of water, although often effective for Legionella, ‘had little effect’ on Pseudomonas growth in taps. Turning to consider water filters, Prof. Trautmann described a 2002 study7 undertaken by he and his colleagues on an 11-bed Surgical ICU at Oberallgäu Klinikum Kempten in Bavaria, which had seen increasing Pseudomonas problems. Different interventions, including hiring an infection control nurse, introducing more hand hygiene training, and even testing patients’ digestive tracts, had had no effect.
Monday morning sampling
The team’s first action was to sample all patient room water outlets twice monthly early on Monday mornings to catch the first flush of water after stagnation over the weekend. Nearly all samples were positive, but elimination of water use for face washing, avoiding oral care with it, and improved hand hygiene, had no real effect. However, following the introduction of Pall’s AQ14F disposable POU filters, the taps immediately tested negative – subsequently mirrored by a 70% fall in the burden of Pseudomonas infections, which had originally affected around 50% of patients. A parallel economic study demonstrated that, while prior to fitting the taps with filters, monthly antibiotic treatment for four patients cost e4,000, following their introduction (having taken into account the filters’ cost), the reduction in antibiotic use saw monthly net cost savings of around e1,500. “Three years later, as pseudomonad levels decreased, taking into account overall treatment costs, including ICU support for Pseudomonasinfected patients (according to literature figures), we were saving around e60,000 annually,” Prof. Trautmann explained. Prof. Kerr also presented a comprehensive review of the evidence of the connection between water and pseudomonad outbreaks. In an outbreak of Stenotrophomonas maltophilia on a Dutch neonatal ICU, staff were alerted when five babies became colonised, and some subsequently developed overt infection. The unit had never seen the bacterium before, but the infectioncausing isolate was isolated from the tap water. The outbreak was controlled via sterile water for washing infants, and increased staff use of alcohol hand rub.8
Bottled water the culprit
Water other than tap water can also be the culprit, Prof. Kerr said. In another P. aeruginosa outbreak, at Berlin’s Charité University Hospital, 19 patients on six ITUs were colonised with a single strain – eventually tracked down to bottled water used for a variety of purposes. Removing this water ended the outbreak.9 However, Prof Kerr said these published reports were likely to represent only ‘the tip of an iceberg’, since many outbreak reports may never be published. Most hospitals rarely saw ‘outbreaks’ as such, although many studies had been carried out to examine endemic situations. A French study of a 16-bed ICU, where tap water was sampled weekly, clearly demonstrated two-way colonisation traffic between patients and taps. This could have been caused either by healthcare workers’ hands, or body fluids being tipped down handwash basins, but disinfecting taps had no effect.10 In a large three-year study on a Spanish 16-bed ITU, a very wide range of patient samples were taken on admission, and subsequently three times weekly. Tap water and taps were also sampled, and tested for P. aeruginosa every 72 hours. As taps can become colonised with more than one strain, DNA analysis was undertaken on at least four colonies per culture plate. Over that time, ICU-acquired colonisation was found in 31 patients, four developing VAP. Pseudomonas was isolated from over two-thirds of water samples, and, of 47 strains isolated from patients, 39 (83%) were acquired from the water supply.11
Swiss ICU intervention
Considering how patients might be supplied with safe water, Prof. Kerr described an intervention in a Swiss ICU. Here, colonised patients belonged to one of three groups: those with a unique strain, not shared with any other patient or tap water isolate; patients colonised or infected with a strain shared with other patients, and patients colonised with an isolate indistinguishable from a tap water isolate. Thermal disinfection, copper/silver ionisation, and tap replacement, had no effect in patients colonised by a unique strain, as these had probably been acquired before admission. There was, however, a decrease in patients with shared strains, and a big reduction in patients with the same strains as tap outlets, although these interventions did not eliminate this category of colonisation.12 In another approach, on a neurosurgery ICU in France, repair of taps and sinks and pipework maintenance were undertaken following a rapidly worsening outbreak of multi-resistant Pseudomonas serogroup O11, traced to the water outlets. However, the outbreak was only terminated by closing the wards, and total replacement of the taps and sinks.13 Discussing the potential of 0.2 m POU filters to reduce Pseudomonas infections on the ICU, Prof. Kerr cited a report on an outbreak of P. aeruginosa bloodstream infections on a haematology unit in Ancona, Italy, which in 2001 had 20 infections in one of its two wards. By the first half of 2002, these had doubled, and P. aeruginosa had been detected in the unit’s water. After introduction of POU filters, infections had returned to baseline levels by the second half of 2002, dropping further by 2003.14
Sub-acute care unit
In another study, in a US sub-acute care unit for patients requiring long-term ventilation, rather than full intensive care, POU filters were fitted on all taps, shower heads, and ice machines, resulting in both a reduction in Pseudomonas-originated VAP, and savings of over $200,000.15 However, Prof. Kerr emphasised that there was ‘no one magic bullet’ when dealing with bacteria such as Pseudomonas and Stenotrophomonas. This was demonstrated in a 24-bedded neonatal ICU in Naples with 350 admissions per year. In late 2005, 12-13% of neonates were becoming colonised with P. aeruginosa, and active surveillance of the babies was introduced to identify additional cases. Infection control methods were also reinforced. However, by the next quarter, colonised baby numbers had increased by over 20%. Environmental sampling, including of water and healthcare workers’ hands, was introduced, but had no effect. A third intervention – feedback of typing data results to staff – also failed. By the last quarter of 2006, nearly 50% of the babies were colonised, infections started to develop, and there were four deaths. The situation only improved after further environmental sampling and 30-minute weekly hand hygiene updates for all staff. By the third quarter of 2007, colonisation levels had dropped back to baseline levels. However, at 12% these were still high, and additional hand hygiene was introduced. Prior to the educational programme, healthcare workers demonstrated a 23% compliance before handling patients, and 11% afterwards, while, following it, the figures rose to 63% and 57% respectively.16
An ‘integrated approach’ advocated
Prof. Kerr concluded: “I have become convinced that there is a link between water and patient infections. I would suggest an integrated approach combining good standard infection control practices with POU filtration as a potential solution to the increasing problem of pseudomonad infection in vulnerable patients.”
Legionella
Prof. Trautmann also described Legionella infections as originating in the community, ‘often being acquired from hotels and cruise ships’, rather than in hospitals, due to the hospital measures taken to protect the vulnerable, including water filtration. He said: “In my experience it is rare that Legionella infections originate within hospitals; I have only seen two cases in many years.” Legionella is a Gram-negative, rodshaped bacterium which cannot grow at temperatures over 60°C. There are 51 distinct species, and 73 serogroups, with L. pneumophila the most frequent human pathogen, and the most aggressive serotype being L. pneumophila serogroup 1 mab type knoxville. Infections are generally caused by inhaling the organism in aerosols during showering, with cooling towers also frequent culprits. Most susceptible are immunocompromised individuals and smokers, alcoholics, and the over-50s, particularly men. Children are rarely affected. Legionnaires’ disease can cause confusion, lobal pneumonia, bilateral chest infiltrates, and liver involvement in some patients. However, some individuals will develop Pontiac fever, a milder form of legionellosis – a short ‘flu-like illness’ not requiring treatment. Some individuals remain symptomless.
Cruise ship the source
Prof. Trautmann gave an example of a major collaboration between a number of local health organisations to track down the source of Legionella infections in patients living hundreds of miles apart. The infection was found to originate in one cruise ship, but only manifested once the travellers had reached home. He explained that cruise ships are often susceptible because they spend long periods waiting in harbour between sailings, allowing water systems to stagnate, and thus Legionella to grow. Prof. Trautmann said Legionella was rarely acquired on ICUs, as patients are too sick to shower, although hydrotherapy can be an infection route. However, suspicion should, he said, always arise when there is a cluster of pneumonia in elderly males and smokers. However, he cited a chemotherapy patient who had developed Legionnaire’s disease while on the haematology oncology unit at Bonn University Hospital. All water on the unit was filtered, with the origin found to be steam from a nearby cooling tower on the hospital’s roof, which the patient had breathed in while on a balcony.
Compulsory testing in Germany
In Germany, Prof. Trautmann explained, at least annual preventative testing of water outlets using a nationally standardised test is compulsory. Positive tests (>100 cfu/100 ml) must be reported immediately to the local health authority. “In Stuttgart,” Prof. Trautmann said, “we test outlets frequently, record water temperatures, and keep hot water above 60°C. Rarely used taps and showers are flushed daily, and in critical units – such as haematology, neonatal wards, and burns units – POU filters are used routinely on all taps and showers. All endoscopes are also rinsed with filtered water.” Dr Tom Makin, who has a 30-year background in researching the environmental aspects of Legionnaires’ disease, is a co-author of the UK’s Legionella guidelines HSE ACOP (L8) and HTM 04-01, and the former directorate manager of the Department of Medical Microbiology at the Royal Liverpool University Hospitals Trust, also discussed Legionella in healthcare settings. Now a leading international consultant, Dr Makin explained that, in the UK, travel-associated cases account for around 48% of the total, with an 11% mortality rate, with community-acquired cases at 46%, with a 12% mortality rate. While nosocomial cases only account for 6%, the mortality rate here is high, at 32%. “Does this mean we are doing well at preventing Legionella infection in hospitals,” Dr Makin asked, “or is it that we are failing to diagnose many nosocomial cases?”
Diagnosing Legionnaire’s disease
He explained how the most widely used test for diagnosing Legionnaire’s disease – a simple rapid dip stick used on urine samples – although highly sensitive for travel-related cases, only has a 46% sensitivity for hospital-acquired infections. This may, he argued, account for many of these cases remaining undetected. With only eight cases reported per million capita, Legionella is a rare infection in the UK, yet prospective studies have shown that infections should account for around 2% of the 200,000-300,000 communityacquired pneumonias (CAPS) seen in the UK each year. “We should therefore be seeing around 6,000-9,000 cases annually, yet only 400-500 are reported,” Dr Makin emphasised. In addition to showers and cooling towers, infection sources include humidifiers, flushing toilets, hydrotherapy pools, and even dental units. Legionella needs warm, stagnant water to grow, multiplying most rapidly between 25°C and 45°C. Levels remain low below 20°C, but the organism is rapidly killed above 50°C. Hot water in calorifiers should thus be kept hot, and cold water systems cold, Dr Makin stressed. There was also ‘significant potential’ for stratification in calorifiers, with Legionella growing at the bottom if the water is not kept sufficiently hot. Avoidance of stagnation was also crucial to prevent build-up of biofilm in which Legionella thrives. Underused showers and toilets can also see biofilm accumulate and be released by occasional use.
TMV concerns
Dr Makin also expressed concern about thermostatic mixing valves, where he explained that the blended water ‘provides the ideal temperature for growth of Legionella’. He said: “As the cold side is rarely used, it becomes stagnant, allowing biofilm build-up. Systems fitted with intelligent devices can overcome this with automatic flushing. “ Dr Makin also noted that ‘some sophisticated non-touch taps’ contain water chambers that may become contaminated, or utilise materials conducive to bacterial growth. Some models had, he said, now been modified so that they no longer have a chamber, and incorporate a bacteria-resistant silicon diaphragm. Turning to consider heat gain in cold water systems, which can lead to water temperatures conducive to Legionella growth, Dr Makin stressed the dangers of hot and cold pipes running too close together in service ducts, and radiant heat ceiling panels placed too close to cold pipes.
Venturi system for keeping water cold
The audience also heard about a German system for keeping cold water moving to prevent biofilm formation. Manufactured by Kemper, it uses the Venturi principle (see Fig. 1), which exploits a constriction in the cold water pipe. When two pipes run off either side of that constriction in a ‘secondary circuit’, a positive and negative effect creates a pushing and suction movement that keeps water flowing in areas such as side wards, where taps may be underused. Other options for controlling, but not eradicating, Legionella, include maintaining high and low temperatures, chlorine dioxide – ‘five times more effective than chlorine’; copper and silver ions – although efficacy can be affected by the chemistry of the water; silver and hydrogen peroxide; regular flushing of outlets; self-purging showers, and UV irradiation. “None of these control measures will, however, be effective if the system contains significant amounts of scale and corrosion deposits,” Dr Makin warned. Moving to discuss POU filters, he warned that, ‘while these do not eradicate Legionella from circulating water within hot and cold water systems, a 0.2 m POU filter is the only measure that will provide a virtually 100% guarantee of Legionellafree water at the final outlet’, adding: “The national L8 guidelines state that levels of Legionella bacteria in water are satisfactory at less than 100 cfu/L, while WHO guidelines require non-detectable levels for water coming into contact with high risk patients. POU filters are the only method that can assure this.”
Point-of-use filters and burns
A subsequent presentation from burn injuries specialist, Rudi Deleus, head nurse of the burns unit at Belgium’s Leuven University Hospital, and a member of the European Burns Association, the Belgium Association for Burn Injuries, and the Belgium Scar Academy, explained how a programme of POU filtration, disinfection, and extensive hand hygiene, had facilitated beneficial hydrotherapy for burns and wound trauma patients at the hospital. He stressed that hydrotherapy only became hazardous if pathogens were transmitted between patients due to contaminated equipment, or between patients and healthcare workers, mostly via hands, or contaminated tap water. To combat these problems, the team at Leuven routinely samples tap water, equipment, and personnel, and disinfects all equipment immediately post-use. Rudi Deleus said: “Large wounds are very difficult to treat in a hospital bed, because of the high volumes of fluid needed, and the unit deploys shower stretchers rather than covered tanks, allowing fast decontamination times between each use.” With the bacterial load of the water supply at Leuven found to vary from 30 to 2,000 bacteria per 100 mL, wounds are cleansed with water filtered through sterile grade water filters, such as Pall Aquasafe disposable showerheads. (These incorporate a 0.2 m pore filter, protecting patients from bacteria, protozoa, and fungi, and are resistant to chemicals used for disinfection). However, the water supply is also pre-filtered to remove any debris, such as rust, using a 0.5 m filter (although old iron plumbing has largely been replaced with PVC or polyethylene). Transmission between patients and healthcare workers’ hands is prevented by using sterile gloves to clean, scrub, and renew the bandages, and by disinfection of hands with hand alcohol.
Endoscope rinse water
The importance of microbiologically clean water for rinsing endoscopes following decontamination was discussed by Christina Bradley, laboratory manager for the Hospital Infection Research Laboratory at Birmingham’s Queen Elizabeth Hospital. She focused on flexible endoscopes, stressing that, being unsuitable for autoclaving, these must be cleaned meticulously. Describing washer-disinfector cleaning routines, she explained that an effective disinfectant to kill microorganisms was needed, that disinfection must reach all instrument surfaces, and that very thorough rinsing was essential to remove potentially toxic residues. Detergents and disinfectors are prepared with water – also used for final rinsing. Christina Bradley stressed that endoscopes may become re-contaminated if not thoroughly rinsed, if the water supplied to the cleaner is contaminated, or if the machine itself becomes the source of contamination due to biofilm growth, all necessitating regular maintenance, in line with national guidance.
Importance of water ‘purity’
The water source itself may also, she explained, pose potential problems, containing chemical residues, particulates that may block filters, microorganisms, and bacterial endotoxins. Although guidelines allow low bacterial levels in water used for preparation of the detergent and disinfectant, the final rinse water must be microbiologically ‘clean’. Washers use direct mains water, ‘of drinking quality’, but not necessarily sterile. Patient infections caused by Mycobacteria, and fungi resulting from contaminated scopes rinsed in tap water, have been reported. In one case, Pseudomonas aeruginosa was found to have colonised 16 ERCP (endoscopic retrograde cholangiopancreatography) patients out of 240 (6.7%). ERCP is a higher risk procedure in which the scope enters the bile duct. Around 9% of gastrointestinal patients were also found to be colonised or infected with P. aeruginosa. All the endoscopes underwent automatic endoscope reprocessing (AER), but a thick biofilm was found in the detergent holding tank, inlet water hose, and the unit’s air vents.17 The contamination source could also be the water treatment system itself, or contamination built up as low counts of incoming bacteria able to multiply within the washer. This could occur in the filters, which Christina Bradley said should be treated, or changed, frequently. Water treatment systems should also be located within, or close to, the machine, to reduce the potential for contaminated pipework, while avoidance of static water – leading to biofilm build-up – was also essential.
Surface disinfection cycle
Christina Bradley emphasised that the surface disinfection cycle should be undertaken at the beginning of the day to destroy any overnight proliferation of microorganisms. Weekly water sampling is recommended, with results plotted, to highlight any emerging trends that might suggest a build-up of biofilm. The most widely used water treatment methods are filtration, using 0.2 m rated filters, and reverse osmosis (RO). Christina Bradley told the audience: “My main concern is the removal of bacteria, and 0.2 m filters will certainly prevent bacteria from getting into the system.” Bacterial filters may become blocked, she explained, necessitating pre-filtering to prevent this. Silt density testing would establish what types of initial filters were required for the local water type. Biocides could also be very effective, but the speaker advised additional use of a filter, and cautioned against using ultraviolet (UV) light alone for decontamination, due to the high water volumes involved. The HTM 2030 guidelines recommend RO, and RO combined with 0.2 m filters, heat, UV, or sterile water, for critical internal applications.
HTM due for replacement
However, Christina Bradley said the use of sterile water would not be practical on a regular basis, again because of the volumes involved. Weekly water testing should find no organisms detected per 100 mL, while testing for Mycobacteria should be annual, and again, should not detect any organisms. Endotoxins in final rinse water should also be tested for when scopes are to be used for invasive procedures. The HTM 2030 guidelines are soon, however, to be replaced by CfPP 01-06. The current draft on water quality recommends trend analysis and species identification where bacterial counts are found to be greater than 10 cfu per 100 mL. If Legionella appears to be a problem, the advice is to include AER in with both Legionella risk assessment, and the routine Legionella management regime. Christina Bradley also outlined the European EN ISO 15883 standards for washer-disinfectors, which give final rinse water levels as less than 10 cfu of bacteria per 100 mL from weekly tests. Quarterly tests should find final rinse water free of Legionella, Pseudomonas, and Mycobacteria, while, where a higher bacterial count is found, the species should be identified to determine any necessary action. Endotoxin levels should be controlled within a limit of 0.25 EU/mL. A 2006 recommendation from Epidemiology & Infection suggests that super chlorination is needed at levels of over 10-100 cfu/100, and that washers be taken out of service if levels over 100 cfu/100 are detected.18 Christina Bradley emphasised the importance of well-defined staff procedures for water testing, and involvement of clinicians in risk assessment, since the risks of infection with endoscopy that penetrates sterile areas of the body, such as the gall bladder or lungs, were ‘much greater than in the gastrointestinal tract’. :
References
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