Abstract
OBJECTIVE
To review the evidence for the efficacy of products used for environmental or hand cleaning on the rates of Clostridium difficile–associated diarrhea (CDAD).
QUALITY OF EVIDENCE
MEDLINE, EMBASE, and the Cochrane Database of Systematic Reviews were searched for articles pertinent to the efficacy of cleaning products against C difficile or studies with outcomes related to rates of CDAD. Evidence was level II.
MAIN MESSAGE
Minimizing the incidence of CDAD in geriatric rehabilitation units is essential to achieving the goals of increasing patient function and independence for discharge into the community. Attention to environmental control of C difficile and its spores by health care workers and patient visitors is an important secondary prevention strategy.
CONCLUSION
Chlorine-releasing agents are more effective than detergents for killing spores produced by C difficile. No level I evidence is available to determine if the use of chlorine-releasing agents has an effect on rates of CDAD. Hand-washing is currently the recommended strategy for reducing transmission of C difficile. Alcohol gels do not inactivate C difficile spores; however, increased use of alcohol hand gel has not been associated with higher rates of CDAD.
Résumé
OBJECTIF
Examiner les preuves indiquant que les produits utilisés pour nettoyer l’environnement et les mains sont efficaces pour réduire le taux de diarrhée due au Clostridium difficile (DDCD).
QUALITÉ DES PREUVES
On a consulté MEDLINE, EMBASE et la Cochrane Database of Systematic Reviews en retenant les articles portant sur l’efficacité des agents de nettoyage contre le C difficile ou les études traitant de questions liées aux taux de DDCD. Les preuves étaient de niveau II.
PRINCIPAL MESSAGE
La réduction de l’incidence de la DDCD dans les unités de réadaptation gériatrique est une condition essentielle pour accroître l’état fonctionnel et l’indépendance des patients qui retournent dans la communauté. Pour les intervenants et pour les visiteurs des patients, le contrôle du C difficile et de ses spores dans l’environnement est primordial comme stratégie de prévention secondaire.
CONCLUSION
Les agents qui libèrent du chlore sont plus efficaces que les détergents pour tuer les spores du C difficile. Il n’existe pas de preuves de niveau I indiquant que l’utilisation d’agents libérant du chlore influence les taux de DDCD. Le lavage des mains est la stratégie présentement recommandée pour réduire la transmission du C difficile. Les gels d’alcool n’inactivent pas les spores du C difficile; toutefois, une utilisation accrue de gels d’alcool n’a pas entraîné d’augmentation du taux de DDCD.
Clostridium difficile infection (CDI) is the most frequent cause of nosocomial infectious diarrhea.1–3 The Canadian Nosocomial Infection Surveillance Program reported an incidence of 4.74 cases of C difficile–associated diarrhea (CDAD) per 1000 patients admitted to hospital in Canada between January 1, 2007, and April 30, 2007.4 In the United States, the proportion of hospital discharges in which the patient record showed a discharge diagnosis code for CDI more than doubled between 2000 and 2003; the overall rate during this period was several-fold higher (P = .001) in persons older than 65 years of age (228/100 000) than in the 45- to 64-year-old age group (40/100 000).5 Incidence of CDI has also increased in Canada and Europe. While these increases have been seen in both pediatric and adult populations, elderly individuals have been disproportionately affected.5
Clostridium difficile–associated diarrhea is associated with increased lengths of hospital stay, costs, morbidity, and mortality among adult patients.5,6 Patients experiencing CDAD while in hospital were almost twice as likely to be discharged to long-term care facilities.2,7 Isolation precautions, implemented to control the spread of CDAD, can result in prolonged bed rest. Negative effects of prolonged bed rest specific to the elderly can include disorientation, delirium, psychosocial dysfunction, disruption in social support, functional decline, and physical deconditioning.8 The loss of muscle strength during bed rest has been estimated to be as high as 5% daily, with lower limbs most affected.9 Preventing occurrence and recurrence of CDAD is an essential aspect of geriatric practice in an institutional setting and is linked to several core values of excellence in clinical care determined by the Task Force on the Future of Geriatric Medicine (Box 1).10 The challenge of managing CDAD in the elderly has been described in a recent review article.11
Box 1. Selected attributes and competencies for excellence in geriatric care.
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Adapted from Besdine et al.10
Multidisciplinary team strategies are necessary to help prevent this devastating problem. Guidelines for infection prevention and control in hospitals are well documented (Box 2).5 Recent literature supports the importance of antimicrobial stewardship.5
Box 2. General strategies to prevent Clostridium difficile infection.
To reduce the risk of Clostridium difficile–associated diarrhea (CDAD) in colonized patients ...
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To prevent patient colonization ...
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Adapted from Dubberke et al.5
While C difficile shares many transmission risk factors with other organisms in terms of infection prevention, its ability to form spores has unique implications for hand hygiene and environmental disinfection strategies. The C difficile spores are resistant to the bactericidal effects of alcohol and most hospital disinfectants.5 The importance of addressing the incidence of spores in the environment is essential to controlling the spread of CDAD, as colonization of C difficile from an exogenous source is an essential prerequisite for CDAD (Box 3).6,12–16
Box 3. Prerequisites and risk factors for Clostridium difficile–associated diarrhea.
Prerequisites
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Risk factors for occurrence
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Risk factors for recurrence (occurs in 15% to 55% of cases)
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The aim of this article is to describe the available evidence for the role of cleaning products in preventing the spread of CDAD in hospitals and its relevance in the elderly population receiving inpatient rehabilitation care. Additionally, evidence on the controversial issue of increased use of alcohol-based hand rubs is explored. Within the inpatient geriatric rehabilitation setting, care is provided primarily by family physicians. As such, they play an important role in providing leadership related to hospital-specific infection control guideline development and on-unit compliance with environmental infection control measures.
Quality of evidence
We searched MEDLINE (January 1996 to November 2008), EMBASE (1998 to 2009), and the Cochrane Database of Systematic Reviews using the key words Clostridium difficile, CDAD, Clostridium infection, cleaning agents, detergents, and disinfectants to find English-language reports on cleaning products effective against C difficile spores. A manual search of references in articles found was also completed. Ten reports describing efficacy of cleaning agents on C difficile spores and 5 studies describing the use of hand cleaning agents were found in total. Evidence was level II.
Levels of evidence
Level I: At least one properly conducted randomized controlled trial, systematic review, or meta-analysis
Level II: Other comparison trials, non-randomized, cohort, case-control, or epidemiologic studies, and preferably more than one study
Level III: Expert opinion or consensus statements
Cleaning products for environmental control
Clostridium difficile bacteria are not part of the normal gastrointestinal flora. One of the prerequisites for CDAD is colonization with C difficile from an exogenous source. Surfaces that become contaminated with feces can serve as reservoirs for C difficile. Although the vegetative form of C difficile is fragile, it is capable of sporulating when environmental conditions do not support growth. Spores produced by C difficile can persist in the environment for extended periods of time.3 Clostridium difficile spores have been isolated from numerous surfaces in patient rooms including commodes, bed railings, nursing call devices, and clothing.17 Additionally, C difficile spores have been shown to persist as a skin contaminant on patients even after their diarrhea resolves, which can serve as a reservoir for health care provider transmission to other patients.18
Reducing environmental sources of C difficile spores is likely to reduce C difficile colonization in hospitalized patients, which might in turn reduce rates of CDAD. To reduce the number of spores in the environment, the Centers for Disease Control and Prevention recommend using chlorine-releasing products after meticulous cleaning to remove organic material.3 Health Canada guidelines simply state that during an outbreak thorough environmental cleaning with a disinfectant of demonstrated effectiveness might be required.19
Evidence to support decision making about the use of environmental cleaners is weak. Of concern is the limited data linking choice of cleaning agent to rates of CDAD. Furthermore, there is no level I evidence to support the efficacy of any one chemical germicide for reducing the presence of spores in the environment. Our search yielded 9 studies and 1 research letter describing research into the efficacy of cleaning products against C difficile spores. Four studies compared cleaning agents in the laboratory setting to determine efficacy against C difficile spores (Table 1),20–23 the research letter reported the effects of different cleaning agents on the rate of sporulation in the laboratory setting,24 and 2 studies reported the effects of cleaning agents on C difficile spore levels in the hospital environment.25,26 Only 3 studies described the effects of cleaning agents on rates of CDAD in the hospital setting (Table 2).27–29
Table 1.
STUDY | AGENTS INCLUDED | METHODS | OUTCOMES |
---|---|---|---|
Fawley et al,20 2007 | Anionic surfactant and NaDCC (1000 mg/L free chlorine)* Detergent and hypochlorite* NaDCC alone (1000 mg/L free chlorine)* Nonionic surfactant and phosphate Hydrogen peroxide (concentration not provided) |
Solution of mature spores were exposed to cleaning agents for 0, 10, 20, and 30 min, cleaned then incubated anaerobically for 48 h; results interpreted in comparison to nonexposed control preparations | All 3 chlorine-containing agents inactivated vegetative cells and spores within 10 min of exposure; exposure to detergent (nonionic surfactant and phosphate) or hydrogen peroxide resulted in no difference in the number of viable spores compared with controls at 30 min |
Perez et al,21 2005 | Chlorine dioxide equal to 600 mg/L free chlorine* Acidified bleach equal to 5000 mg/L free chlorine* Domestic bleach in 3 dilutions (5000 mg/L free chlorine, 3000 mg/L free chlorine, and 1000 mg/L free chlorine)* 7% hydrogen peroxide |
Spores were grown anaerobically and heated to kill vegetative cells; stainless steel disks were contaminated with spore suspension and exposed to cleaning agents for 10, 15, or 30 min; after neutralizing the cleaning agent, agar plates were inoculated with the contents of each disk and incubated for 2 and 5 d | Acidified bleach, regular bleach (5000 mg/L free chlorine), and 7% hydrogen peroxide inactivated spores within 10 min of exposure; chlorine dioxide and domestic bleach at 3000 mg/L and 1000 mg/L free chlorine were all able to inactivate spores; however, exposure times were longer (up to 30 min) |
Block,22 2004 | 0.26% peracetic acid—a biocide with manufacturer claims of sporicidal activity NaDCC tablets (1000 mg/L free chlorine)* |
Spores were grown anaerobically on blood agar plates and harvested by suspending the cultures in methanol; equal aliquots of spore suspensions were dried on stainless steel disks and PVC floor covering material; each material was exposed to the test solutions for 3, 5, or 10 min, after which time remaining viable spores were counted | Neither agent was effective in eradicating the spores, although both agents reduced spore counts; on stainless steel, at 10 min, peracetic acid exposure resulted in a 6 log10 reduction in viable spores compared with a 0.7 log10 reduction in viable spores with NaDCC (P = .011); on PVC, the log10 reduction in viable spores for peracetic acid (2.7) and NaDCC (0.9) were not statistically different |
Wullt et al,23 2003 | 70% isopropanol 2% glutaraldehyde 0.26% peracetic acid Acidified nitrite |
C difficile bacteria and spores were grown anaerobically on blood agar for 48 h; vegetative cells were killed using ethanol, and spores were suspended in water to which disinfecting agents were added for 5, 15, and 30 min before being inactivated | Glutaraldehyde, peracetic acid, and acidified nitrite reduced spore counts by 99% after 15-min exposure; glutaraldehyde has been associated with dermatitis and symptoms of asthma secondary to exposure; isopropanol showed no effect on spore viability even after 30-min exposure |
NaDCC—sodium dichloroisocyanurate, PVC—polyvinyl chloride.
Chlorine-releasing product.
Table 2.
STUDY | AGENTS INCLUDED | METHODS | OUTCOMES |
---|---|---|---|
Mayfield et al,27 2000 | Unbuffered 1:10 hypochlorite solution* Quaternary ammonium solution |
9-month before-and-after design comparing cleaning with hypochlorite or detergent on rates of CDAD; 3 units were included (bone marrow transplant, neurosurgical ICU, and general medicine) | Before use of hypochlorite, rates of CDAD were 8.6, 3.0, and 1.3 cases per 1000 patient-days for bone marrow transplant, neurosurgical ICU, and general medicine, respectively; after implementing the hypochlorite cleaning protocol, CDAD rates fell to 3.3 (HR 0.37, 95% CI 0.19–0.74) for bone marrow transplant, but did not change significantly on the other units; on return to the original disinfectant protocol in the bone marrow transplant unit, rates of CDAD returned to prestudy levels of 8.1 cases per 1000 patient-days |
Wilcox et al,28 2003 | Hypochlorite disinfectant* Neutral detergent |
2-year ward-based crossover study comparing effects of environmental cleaning with either hypochlorite or detergent on CDI | One ward experienced a drop in CDI incidence from 8.9 to 5.3 cases per 100 admissions (P < .05); the other ward showed an increase in CDI incidence to 4.7 from 3.5 per 100 admissions (P < .05) |
McMullen et al,29 2007 | Quaternary ammonium detergent Household bleach (diluted to 5000 mg/L free chlorine) and hypochlorite containing towels to clean equipment such as computers and monitoring equipment in patient rooms* |
5-month before-and-after study comparing effects of changing to a chlorine-releasing cleaning agent from a detergent cleaner in a medical ICU and surgical ICU following an outbreak of CDAD | The outbreak resulted in an increase in the monthly rates of CDAD to 16.6 and 10.4 cases per 1000 patient-days from 5.3 and 2.5 cases per 1000 patient-days, respectively; postintervention, rates in the medical ICU and surgical ICU were 3.7 and 2.2 cases per 1000 patient-days, respectively |
CDAD—Clostridium difficile–associated diarrhea, CDI—Clostridium difficile infection, CI—confidence interval, HR—hazard ratio, ICU—intensive care unit.
Chlorine-releasing product.
Effects of cleaning agent choice on sporulation rates in the laboratory setting
All studies tested commercially available products. Of the agents tested, those containing high levels of chlorine (5000 mg/L free chlorine) showed consistent efficacy against C difficile spores.21 Lower dilutions of chlorine (1000 and 3000 mg/L free chlorine) showed inconsistent capacity to eradicate spores; 1 author reported efficacy20 and 2 reported benefit only with extended exposure.21,22 Hydrogen peroxide had mixed results, with 1 report describing no benefit20; however, no concentration was provided. Hydrogen peroxide at a concentration of 7% showed efficacy similar to high levels of chlorine.21 Peracetic acid also showed mixed results,22,23 with benefit shown only when a spore suspension was exposed to a peracetic acid solution at a ratio of 1:4,23 which is not reflective of hospital cleaning practices. Detergent alone or 70% isopropyl alcohol showed no benefit.20,23
Of interest is the effect of subinhibitory levels of cleaning agents on the sporulation capacity of C difficile. One study showed that exposure to low levels of cleaning agents resulted in higher sporulation capacity compared with no exposure to cleaning agents, suggesting that sporulation capacity might increase in response to environmental stresses such as cleaning.24
Effects of cleaning agent choice on sporulation rates in the hospital environment
A recent study explored the adequacy of cleaning procedures and disinfection practices on sporulation rates in a hospital environment.25 During the 6-week study, commonly touched surfaces in rooms of patients with CDAD were cultured before and after housekeeping cleaned and again after researchers performed a second cleaning. Housekeeping cleaning protocols included using a clean cloth or mop soaked in 10% bleach, and researchers applied a 10% bleach solution using a spray bottle. All of the 9 rooms tested had cultures positive for C difficile before cleaning, 7 (78%) had cultures positive for C difficile after being cleaned by housekeeping, and 1 (11%) had cultures positive for C difficile after being cleaned by research staff. The authors reported that after the study was complete, cleaning staff were given additional time for cleaning (30 minutes per room), were trained to disinfect frequently touched surfaces (eg, bed rails, bedside tables, call buttons, telephones), and were trained to complete their cleaning with a 10% bleach solution spray.25
A second study assessed the level of environmental C difficile in a variety of clinical areas, including geriatric care wards, after dry-mist hydrogen peroxide decontamination.26 The clinical areas included were selected to represent high-, moderate-, and low-risk areas, based on the existing C difficile infection rates at the facilities enrolled in the study. Three geriatric wards (10 rooms) represented high-risk areas; 2 isolation rooms on a hematology unit represented moderate-risk areas; and 2 isolation rooms (1 in an obstetric ward and 1 in an elective orthopedic ward) represented low-risk areas. After cleaning but before decontamination, 100% of geriatric care rooms had at least 1 culture positive for C difficile. After decontamination, 5 rooms had 1 or more positive cultures for C difficile (P = .033). Of 203 cultures taken in the 10 rooms, 48 (24%) were positive for C difficile before decontamination and 7 (3%) were positive for C difficile after decontamination (P < .0001). Although these benefits were not achieved in the moderate- and low-risk rooms,26 this suggests that additional cleaning strategies in high-risk areas might provide protection from exposure to C difficile spores.
Effects of cleaning agent choice on rates of CDAD
Our search yielded 3 studies describing the effects of cleaners on rates of CDAD.27–29 Changes in the rates of CDAD in geriatric medicine units cleaned with hypochlorite disinfectant were inconsistent.28 In medical and surgical intensive care unit settings, rates of CDAD were reduced following a change in cleaning protocols that included adding chlorine-releasing cleaners and chlorine-containing towels for computers and monitors.29 Use of chlorine-containing cleaners was shown to be beneficial for reducing rates of CDAD in a bone marrow transplant unit; the CDAD rate increased to pre-intervention rates once the cleaning protocol was discontinued. Rates of CDAD in the neurosurgical intensive care unit and general medicine ward were lowered, but results were not statistically significant.27
Although chlorine-releasing agents are more effective for killing spores than detergents are in the laboratory setting, efficacy related to reducing levels of spores in the environment or rates of CDAD in the hospital has not been consistently shown. The advantages and disadvantages of chlorine cleaners are considerations for their use in hospitals and are described in Box 4.19
Box 4. Advantages and disadvantages of chlorine-releasing cleaners.
Advantages
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Disadvantages
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Data from the Steering Committee on Infection Control Guidelines.19
Hand washing versus the use of alcohol-based hand rubs
Clostridium difficile spores colonize patients mainly via the hands (fecal-oral route) of health care personnel or visitors who have touched a contaminated surface or item.3,30 Concern over the increased use of alcohol-based hand gels (ABHGs) and rates of CDAD have been explored in 4 published reports.31–34 One 3-year retrospective study in a 500-bed teaching hospital where ABHGs were promoted showed that hygiene compliance rose from 38% to 63% with promotion; 85% of hand hygiene was achieved with ABHGs and 15% with hand-washing. Rates of CDAD per 1000 patient-days rose from 1.74 to 2.33 in the first year, then decreased to 1.14 and 1.18 in the subsequent 2 years, respectively. Statistical significance for the change in CDAD rates between years was not reported.31 Another report from a 600-bed teaching hospital showed that in the 3 months following an intensive marketing campaign to promote the use of ABHGs, there was a non-significant decrease in CDAD cases of 17.4% (P = .2).34 Similar results have been reported in studies that included geriatric rehabilitation and long-term care beds.32,33 One report described an increase in the use of ABHGs (1.3 L to 2.0 L per 100 patient-days) over 6 years in a 2200-bed hospital that included 761 rehabilitation, geriatric, and long-term care beds. There was a non-significant (P = .82) improvement in rates of CDAD (numbers not reported) during that period.32 Another 287-bed facility with 120 long-term care beds reported that over 6 years the promotion of ABHGs resulted in no change in the rate of CDAD (3.24 to 3.38 cases per 10 000 patient care days, P = .78).33
At the 2009 Society for Healthcare Epidemiology of America 19th Annual Scientific Meeting, results of the efficacy of hand-wash products on spore removal were reported.35 Subjects whose palms were inoculated with C difficile spores performed a 15-second wash followed by a 15-second rinse with 3 products: a 4% chlorhexidine gluconate antimicrobial hand wash, a 0.3% triclosan antimicrobial hand wash, and a non-antimicrobial body wash. Tap water and a heavy-duty hand cleaner (used for extreme soiling in manufacturing environments) were used as controls. A log10 reduction in spore count from baseline was determined for each product. All products were statistically equivalent in their ability to reduce spore count and were comparable to tap water (achieving a reduction of approximately 1 log10), except for the heavy-duty hand cleaner (which achieved a significantly greater log10 reduction of 1.21 in spore count; no P values were provided).35
Conclusion
Choice of hospital decontamination products specified in CDAD cleaning protocols can influence the prevalence and environmental distribution of C difficile contamination and resulting patient colonization. Use of chlorine-releasing, hypochlorite-based cleaners or hydrogen peroxide in rooms exposed to C difficile spores can reduce the number of spores within the environment with some evidence to suggest it also can reduce the risk of recurrence and spread of CDAD. Evidence is strongest for products with higher concentrations of disinfecting agents (eg, 5000 mg/L free chlorine or 7% hydrogen peroxide). The benefits of chlorine use might be greater in units where rates of CDAD are high (eg, geriatric rehabilitation or assessment units) or in response to outbreaks of CDAD. Additionally, effectiveness of cleaning agents used in the hospital environment on levels of spores and, more important, rates of CDAD, might be related to training and time-constraints of cleaning staff.
Although wearing gloves and washing hands thoroughly are currently considered optimal strategies to reduce the hand carriage of C difficile spores among health care workers and hospital visitors, the use of alcohol-based hand rubs is unlikely to positively or negatively influence the rate of CDAD in any given environment.
Increased rates of CDAD, as recently published in the literature, translate to higher morbidity and mortality for patients, especially seniors, and create a greater burden on the health care system as a whole. Strategies aiming to reduce recurrence and spread of CDAD are needed. This is particularly true in geriatric rehabilitation units, where numerous providers are intimately involved in each patient’s care on a daily basis.
Family physicians can play an important role in providing leadership to ensure geriatric rehabilitation facility policies and protocols incorporate cleaning strategies into the bundle of infection control and prevention strategies employed. Awareness and knowledge of the evidence regarding CDAD risks and effective interventions are necessary to providing that leadership.
EDITOR’S KEY POINTS
Preventing occurrence and recurrence of Clostridium difficile–associated diarrhea (CDAD) is an essential aspect of geriatric practice in an institutional setting.
This article describes the available evidence for the role of cleaning products in preventing the spread of CDAD in hospitals and its relevance to the elderly population receiving inpatient rehabilitation care.
Of the commercially available products tested, those that contained high levels of chlorine (5000 mg/L free chlorine) showed consistent efficacy against C difficile spores. Lower dilutions of chlorine (1000 and 3000 mg/L free chlorine) showed inconsistent capacity to eradicate spores (1 study reported efficacy and 2 reported benefit only with extended exposure). Detergent alone or 70% isopropyl alcohol showed no benefit.
Although wearing gloves and washing hands thoroughly are currently considered optimal strategies to reduce the hand distribution of C difficile spores among health care workers and hospital visitors, use of alcohol-based hand rubs is unlikely to positively or negatively influence the rate of CDAD.
POINTS DE REPÈRE DU RÉDACTEUR
La prévention de l’éclosion et de la récurrence de la diarrhée due au Clostridium difficile (DDCD) est un aspect essentiel de la pratique gériatrique chez les patients institutionnalisés.
Cet article résume les données probantes concernant le rôle des produits de nettoyage pour prévenir la propagation de la DDCD à l’hôpital et son importance pour la population âgée recevant des soins hospitaliers de réadaptation.
Parmi les différents produits commerciaux testés, ceux contenant des niveaux élevés de chlore (5000 mg/L de chlore libre) se sont montrés régulièrement efficaces contre les spores du C difficile. Les dilutions plus faibles (1000 et 3000 mg/L de chlore libre) avaient une capacité inégale pour éradiquer les spores (une étude les trouvait efficaces et 2 autres, seulement avec une exposition prolongée). L’alcool isopropylique à 70 % ou un détergent seul n’étaient pas utiles.
Quoique le port de gants et le lavage minutieux des mains soient toujours considérés comme la meilleure façon de réduire la dissémination des spores du C difficile chez les intervenants de la santé et les visiteurs de l’hôpital, il est peu probable que le fait de se frotter les mains avec de l’alcool ait une quelconque influence sur le taux de DDCD.
Footnotes
This article has been peer reviewed.
Cet article a fait l’objet d’une révision par des pairs.
Contributors
Both authors contributed to the literature search and preparation of the article.
Competing interests
None declared
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