Healthcare-associated infections are a potential risk to patient safety and constitute a major cause of morbidity and mortality. In healthcare settings, there are three major types of healthcare-associated infections: surgical-site infections, central-line-associated bloodstream infections, and catheter-associated urinary tract infections. In dialysis units, infection is the first cause of hospitalization and the second most common cause of mortality among haemodialysis (HD) patients after cardiovascular disease [1] - [3] . HD patients are exposed to different types of infections which include bloodstream infections and localized infections of the vascular access (catheters and grafts), blood-borne infections with hepatitis B virus (HBV), hepatitis C virus (HCV), and/or human immunodeficiency virus (HIV), and airborne infections like tuberculosis. Sources of infections could be contaminated water, equipment, environmental surfaces in the treatment area, and patients with infections who pose a risk to other nearby patients being treated in the dialysis unit. The increased risk for contracting healthcare-associated infections (HAIs) among HD patients are mainly due to 1) immune compromised status, 2) frequent and prolonged blood exposure during HD treatments through the vascular access and extracorporeal circuit (with many ports and connections), 3) close proximity to other patients during treatment in the HD facility, 4) frequent contact with healthcare workers who frequently move between patients and between machines, 5) frequent hospitalization and surgery, and most importantly 6) non-adherence or a break in implementation of recommended practices, including hand hygiene and use of personal protective equipment.

The break in implementation of recommended practices may sometimes occur inevitably as a result of one or more of the following factors: 1) understaffing with poor nurse to patient ratio [4] - [6] , 2) frequent turn-over of nursing staff [4] - [9] , 3) lack of or inadequate training and lower level of competency among HD staff [5] [9] - [11] , 4) inadequate or lack of patient/family education, 5) inadequate provision of necessary supplies/equipment, including adequate clean sinks and/or alcohol-based hand rubs, soap and towels [10] [11] , 6) poor design of HD unit lay-out (congested and inadequate segregation/isolation) [11] , and 7) the urgency associated with dialysis complications (sometimes life-threatening situation) which may sacrifice adherence to standard precautions [9] [12] [13] .

Healthcare Infection Control Practices Advisory Committee (HICPAC) and Centers for Disease Control and Prevention (CDC) recommended two-level approach precautions to prevent the transmission of infectious agents in healthcare settings. These are 1) Standard Precautions and 2) Transmission-Based Precautions. Standard Precautions are the basic level of infection control practices to be applied in the care of all patients and in all healthcare settings, regardless of the suspected or confirmed infection status. Standard Precautions were based on the principle that all blood, body fluids, secretions, excretions (except sweat), non-intact skin, and mucous membranes may contain transmissible infectious agents [14] . The elements of Standard Precautions include: 1) hand hygiene, 2) use of personal protective equipment (PPE) such as gloves, gown, mask, eye protection (eye goggles or face shield), and 3) handling of equipment or items including surfaces in the patient environment in a manner that prevent transmission of infectious agents. CDC added new elements to be considered as a standard of care which include: a) respiratory hygiene/cough etiquette; b) safe injection practices; and c) use of masks for insertion of catheters [14] .

Transmission-Based Precautions are usually applied for patients who are known or suspected to be infected or colonized with infectious agents, including certain epidemiologically important pathogens that require additional control measures to effectively prevent transmission. Transmission-Based Precautions have three categories: 1) contact precautions, 2) droplet precautions, and 3) airborne precautions [14] .

In addition to Standard Precautions and Transmission-Based Precautions, CDC recommended more stringent measures for HD settings, which include non-sharing of supplies, instruments, medications and medication trays between patients, and prohibit the use of a common medication cart [15] - [18] . Unlike the conditions in general hospital wards, the typical lay-out and associated conditions in most HD units (wherein multiple patients receive extracorporeal treatment with prolonged blood exposures in the same area and usually with one healthcare worker (HCW) caring for more than one patient at the same time) are potential factors that may increase the transmission of infections. Therefore, strict implementation of Standard Precautions and in particular hand hygiene constitutes an essential measure of infection prevention and control. The aim of this narrative review is to mainly focus on hand hygiene and other related Standard Precautions in a HD facility, where the importance of implementation of such precautions is shared with other healthcare settings. Other more specific hemodialysis- related infection control measures, which include cleaning and disinfection of HD machine’s external surfaces, disinfection of internal fluid pathway of HD machines, handling of disposable supplies and reusable items in HD units, purity and testing of treated water, screening and routine serologic testing and patient placement, and immunization of patients and healthcare personnel are all reviewed in [19] .

Contaminated hands of HCW are among the most common modes of transmission of healthcare-associated infections. Pittet and colleagues [20] described a five-step sequence resulting in microbial transmission through contaminated hands during healthcare delivery. These are “1) pathogens shed by infected patients can contaminate surrounding environments, 2) HCW’s hands get contaminated by contact with patient skin or surrounding environment, 3) pathogen remains viable on the HCW’s hands for at least several minutes 4) HCW may omit hand decontamination or use inappropriate product or procedure, and 5) HCW’s contaminated hands can either transfer the pathogen directly to another patient or indirectly on a medical device or objects within the patient’s immediate vicinity”.

Different studies have confirmed that transiently contaminated hands of the HCW are the main route of transmission of healthcare-associated infections [21] - [29] . Hand hygiene, therefore, is singled out as the most important infection prevention intervention. However, the compliance rates of HCWs in hand hygiene is very poor, with an overall average of 40% or less [30] [31] . Based on hand hygiene indications per recommendations from Association for Professionals in Infection Control and Epidemiology (APIC) [32] , CDC [15] and World Health Organization (WHO) [33] (Table 1), the estimated number of times a single dialysis staff is required to perform hand hygiene per HD session per patient is shown in Table 2. The estimated number can be a minimum of 60 to 100 times when multiplied by the number of patients assigned per staff (e.g., 2 - 3 patients). The large number of times an HD staff is required to perform hand hygiene could be a reason for lack of compliance. However, compliance can be improved by continuous education, supervision and monitoring of hand hygiene behaviors, where the latter represents the most effective method in improving performance [34] .

Monitoring hand hygiene compliance is crucial and direct observation is the current gold standard method. However, direct observation has several limitations, among which are being labor intensive, small sample size (may cover only 1% of total hand hygiene activity), and not standardized. A new model device application developed by the Computational Epidemiology Research Group at the University of Iowa (the “iScrub Lite”, which is available for free download on the Apple iTunes store for Apple^® iPhone or iPod), can facilitate the work of the Infection Preventionist (IP) by recording the observations, which can be loaded to an excel spreadsheet for ready analysis. Advanced technologies, with automated electronic devices and software (Real Time Location System), can monitor the number of hand hygiene activity (10 to 50 thousands per month) in each department, floor or unit, and identify the HCW performing the hand hygiene through badge or wristband detection, with indication of the time of day and day of the week hand hygiene is performed, and even provide feedback/cueing to encourage proper hand hygiene [35] .

Compliance can also be improved by providing, in convenient locations, a sufficient number of sinks with

APIC = Association for Professionals in Infection Control and Epidemiology, CDC = Centers for Disease Control and Prevention, WHO = World Health Organization.

^*Most of the time, the activity is recently preceded by a hand hygiene performed at the end of one procedure/activity (between two different activities). Therefore, repetition of hand hygiene prior to an activity (wherein performance of hand hygiene is indicated per recommendation) is unnecessary. ^**Not included for patients with permanent arteriovenous (AV) access.

soap dispensers, paper towels, hand lotions (e.g., one for every 2 - 4 dialysis station), and alcohol-based hand rub (ABHR) placed at each patient station [32] . Because of the proven superior efficacy in decontamination, better skin tolerability and ease of use, ABHR is recommended to be used in all clinical situations if hands are not visibly soiled. If exposure to bacterial spores (i.e., bacillus anthracis and/or clostridium difficile) is suspected or proven, hand washing with soap and water is recommended, because spores are resistant to most antiseptic agents and requires physical removal by washing and rinsing [36] . Other preventive measures include restriction of having long nails and wearing of artificial fingernails or extenders by healthcare personnel who provide direct patient care, as artificial nails could harbor gram negative bacilli and yeasts [30] [32] [36] - [40] .

Personal Protective Equipment (PPE) refers to a variety of barriers and respirators used alone or in combination to protect mucous membranes, airways, skin, and clothing from contact with infectious agents, which includes: gloves, gowns, masks, eye goggles, face shields, and respirators [36] . In the HD setting, gloves are recommended to be worn whenever caring for a dialysis patient; whether touching patient’s intact skin (e.g., taking blood pressure) or patient’s equipment at the dialysis station. Gloves should be removed and followed by hand hygiene between patients or stations [16] [32] . The recommended practice of glove use for every contact with the patient(s) and equipment(s) at the dialysis station requires an enormous amount of glove supply, which is not always realistic in many HD units. However, when visible soil is present and/or contact precautions are indicated, wearing gloves is a must. Sterile gloves must be used during procedures requiring sterile aseptic technique, such as during catheter insertion or at any time a dialysis catheter is handled/manipulated [41] - [43] . Wearing gown (fluid-resistant with full coverage of the arms and body front and preferably disposable ones) over the uniform, and use of face mask and eye goggles or face shield is recommended when performing procedures wherein splashes of blood can be anticipated, especially during initiation and discontinuation of dialysis [16] [32] [36] . If a face shield is used during catheter handling, a surgical mask should be worn underneath to protect patient from HCW’s respiratory droplets [32] . Equally important is that patient should also wear a mask and asked to turn his/her face away from the catheter site to reduce contamination from infectious droplets [32] [43] - [45] . Furthermore, wearing a mask is important when a staff member, a patient or a visitor is experiencing cold or cough [32] [36] . A respirator should be used by HCWs only when taking care of a patient with an airborne infection. HCWs uniforms can be colonized with potentially pathogenic bacteria for up to 60% [46] - [51] and therefore should be laundered and changed daily in order to decrease the bacterial load.

In the healthcare setting, contamination of environmental surfaces with various pathogens and the persistence of these pathogens on surfaces [52] - [58] can be an important and frequent source of transmission of infectious agents through the frequent hand touching of HCWs [59] [60] . The environment in HD units is particularly prone for contamination with blood-borne pathogens such as HBV, HCV and HIV, and other infectious agents such as methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococci (VRE), and Clostridium difficile (C. difficile). Microorganisms can survive on environmental surfaces for varying periods of time ranging from few hours to days and months. Low temperature, high humidity and high inoculums favor the long persistence of pathogens on inanimate surfaces [52] . In order to prevent and control spread of environmentally transmitted pathogens, cleaning and disinfection of the external surfaces of equipment (i.e., HD machine, dialysis chair or bed, procedure trolley) and other environmental surfaces inside HD units, especially those that are frequently touched by patients and staff, should be performed between all patient treatments (irrespective of the patient diagnosis) [16] [32] [43] . The application of friction during cleaning is emphasized since some organisms like C. difficile are not easily inactivated by most surface disinfectants (except bleach) and require removal by friction [32] [36] .

Auxiliary equipment used in HD may include reusable jugs for mixing bicarbonate solution, reusable priming buckets, and external pressure transducers. As per recommendation, any reusable item should be cleaned and disinfected prior to being used on another patient, and external pressure transducers should be changed between patients’ uses. Nowadays, many units have shifted to use the more hygienic automated process of mixing bicarbonate powder in cartridge on the individual machines eliminating the use of reusable bicarbonate jugs. If bicarbonate solution in a jug is used, any “left-over” solution must be discarded and opened jugs should not be used after 24 hours because sodium bicarbonate solution substitute a good media for bacterial growth [32] . Reusable priming buckets are now seldom used since most dialysis companies include a disposable prime collection bag in each pack of sterile bloodline set, and also with pre-attached external pressure transducers. With improved and better technology in some latest model of HD machines, prime collection bags or transducer protectors are not even required, because drainage of priming solutions can be done by connecting the bloodline to a drainage port in the machine, and blood pressure sensors are completely non-invasive without using transducer connections and protectors.

Both CDC and APIC recommended specific measures which include the following: 1) items taken into an individual patient’s HD station should be used only for that patient and be disposed of after use, 2) unused item(s) should be cleaned and disinfected before returning to a common clean area or used on another patient, or be disposed of if it cannot be disinfected, and 3) non-disposable items that cannot be comprehensively cleaned and disinfected (e.g., adhesive tape, cloth-covered blood pressure cuffs) should be dedicated for use on a single patient [16] [32] . In reality, allocating a blood pressure cuff for each patient may not be practical as too frequent detachment and re-attachment of the cuff can cause imminent damage to the line connections. Reusable blood pressure cuffs that are covered with waterproof material with smooth surface (instead of cloth-covered cuffs) can be an attractive alternative, as they can be comprehensively cleaned and disinfected between patient uses. There should also be a clear separation for storage and handling of clean supplies and medications from contaminated items (i.e., used supplies/equipment, blood samples, biohazard containers).

Aside from the basic principles of aseptic technique, there are specific complementary recommendations for HD published by the CDC and APIC, which include the following: 1) all single-use injectable medications and solutions should be dedicated for use on a single patient and be entered one time only, 2) medications packaged as multi-dose should be assigned to a single patient whenever possible, 3) medication preparation should occur in a clean area away from the patient treatment area, and be delivered separately for each patient, 4) not to carry multi-dose vials from station to station or carry medication vials, syringes, alcohol swabs or supplies in pockets, 5) unused medications or supplies taken to the patient’s station should be used only for that patient and should not be returned to a common clean area or used on other patients, 6) not to use common medication carts to deliver medications to patients, and if trays are used to deliver medications to individual patients, they must be cleaned between patients [16] [32] [61] . CDC’s full recommendations on safe injection practices are shown in Table 3.

Infection rates with tunneled dialysis catheters has been estimated to be 10 times higher than that of arteriovenous fistula (AVF) or AV graft [32] , and found to be the leading risk factor of bacteremia in chronic HD patients [62] . The international bodies are in concert with the guidelines that vascular access should be a native AV fistula whenever possible, AV graft as the next preferred option, and the use of catheters to be avoided as much as possible [17] [32] [42] - [45] . Vascular access infection prevention measures unanimously recommended by the international bodies are outlined in Table 4, and varying messages on dialysis catheter recommendations are outlined in Table 5. The relevance of “rubbing and soaking the catheter hub with the cap on with a povidone iodine swab for 3 - 5 minutes before the cap is removed” (as recommended by KDOQI) is understandably to disinfect the outside surface thereby preventing inadvertent contamination of the inner hub and ultimate bloodstream contamination. In the 2011 update of CDC Guidelines for the Prevention of Catheter-Related Infections,

Content source: CDC. Guide to Infection Prevention for Outpatient Settings: Minimum Expectation for Safe Care. http://www.cdc.gov/HAI/pdfs/guidelines/standards-of-ambulatory-care-7-2011 [15] .

KDOQI = Kidney Disease Outcomes Quality Initiative.

scrubbing of the access port with an appropriate antiseptic (chlorhexidine, povidone iodine, an iodophor, or 70% alcohol) was recommended for needleless intravascular catheter systems [17] . The routine scrubbing of dialysis catheter hubs (after cap removal before accessing, and before replacing a new cap) with an appropriate antiseptic was included as part of a recent CDC’ score interventions for dialysis bloodstream infection (BSI) prevention (Table 6) [18] . Dialysis providers are cautioned to avoid introduction of the used antiseptic solution into the bloodstream [63] . In an in vitro study by Salzman et al. [64] , the potential for the antiseptic used in cleaning the open catheter hub as well as few strands of cotton fibers to enter the bloodstream (simulated), and the effectiveness of normal saline solution (used as control) to reduce the microbial load at a level greater than 99% of the total number of microorganisms (suggesting mechanical removal) was demonstrated. The cumulative effect of minute residues of toxic antiseptics and foreign substance that may get into the patient’s bloodstream when applied repeatedly on open catheter hubs among chronic HD patients have not, and may not be studied. Therefore, it is prudent to choose a safe and non-toxic solution for cleaning open catheter hubs and to emphasize the application of friction while cleaning (scrubbing not just wiping).

Since HD patients are more immune compromised than other surgical patients, pre-surgical infection prevention measures are recommended, which include: 1) pre-surgical shower/bath with an antiseptic agent such as chlorhexidine, the night before and morning of surgery, 2) if hair removal is necessary, to use clippers instead of razors to prevent infection associated with micro-abrasions resulting from razor use, and 3) avoiding intravenous placements and phlebotomy in the arm where access is to be placed (helps prevent infection and maintains vasculature integrity) [32] . Screening and decolonization for MRSA before an elective surgery may be used as an additional measure.

Surveillance for infections (outcome measures), and monitoring adherence to recommended infection prevention practices (process measures) are important components of an infection prevention program [65] . To enable safety, accurate comparison and analyses of monthly rates within the same facility, or meaningful benchmarking with other units/centers, it is important that a standardized and validated surveillance protocol be used uniformly by all dialysis facilities [66] [67] . A centralized surveillance system for healthcare-associated infections like the CDC’s national healthcare safety network (NHSN) which requires all participating facilities to strictly follow very specific surveillance criteria, can provide accurate and reliable data that can be used to identify problem areas as well as measure progress of prevention efforts. Implementation of CDC’s NHSN Dialysis Event Protocol (accessible online: www.cdc.gov/nhsn/dialysis) by other dialysis facilities outside the United States have

KDOQI = Kidney Disease Outcomes Quality Initiative, EBPG/ERBP = European Best Practice Guidelines/European Renal Best Practice, APIC = Association for Professionals in Infection Control and Epidemiology, CDC/HICPAC = Centers for Disease Control and Prevention/Healthcare Infection Control Practices Advisory Committee.

^aPovidone-iodine (preferably with alcohol) or 70% alcohol by itself are alternatives for patients with chlorhexidine intolerance. ^bIf closed needleless connector device is used, disinfect connector device as per manufacturer’s instructions. ^cSee information on selecting an antimicrobial ointment for hemodialysis catheter exit sites on CDC website. Use of chlorhexidine-impregnated sponge dressing might be an alternative. Adapted from CDC. CDC Approach to BSI Prevention in Dialysis Facilities (i.e., the Core Interventions for Dialysis Bloodstream Infection (BSI) Prevention [18] .

been demonstrated to be feasible. Dialysis Events that should be reported include: 1) intravenous antimicrobial starts, 2) positive blood cultures, and 3) evidence of local access site infection (pus, redness, or increased swelling at the vascular access site), and data collected from these three events can generate four other types of Dialysis Events: bloodstream infection (BSI), local access site infection (LASI), access-related bloodstream infection (ARB), and vascular access infection (VAI). The number of maintenance HD outpatients who received HD in the unit/center during the first two working days of the month (including transient HD patients but excluding inpatients and peritoneal dialysis patients) should be reported on monthly basis and according to their vascular access type. This will serve as the denominators for rate calculation. Each patient is counted only once; if the patient has multiple vascular accesses, that patient is counted with the vascular access type of highest infection risk. Rates are calculated by dividing the number of events by the number of patient-months and multiplying the result by 100 [68] .

As a means to reduce infection transmission, each dialysis facility should also monitor other parameters like dialysis water and dialysis fluid cultures and endotoxin results, incidence of drug-resistant infections, hospitalizations, as well adherence to Standard Precautions (hand hygiene, glove use and other PPE, equipment and environmental cleaning, safe injection practices, etc.), and other recommended practices (screening for HBV, HCV, HIV and tuberculosis infections, and immunizations) [19] . Regular feedback of surveillance results to everyone involved in the healthcare delivery (especially the frontline staff) would help to stimulate and encourage active engagement and improve compliance with infection prevention efforts. At least one designated person with training in infection control and epidemiology (infection preventionist) should be responsible for oversight of the program as well as education of staff and patients related to infection prevention and control [15] [32] .

Steps that should be taken to control spread of infection, especially if there is an incidence of a positive seroconversion or outbreak in the HD unit, include the following: 1) revision of the laboratory test results of all patients dialyzing in the same unit to identify any additional case(s), 2) performance of additional testing as indicated in Table 7, 3) determination/tracking of potential sources for infection, which includes a) revision of newly infected patients’ recent history of blood transfusion, invasive procedure(s) and/or hospitalization, and b) high risk behavior such as history of injection drug use and sexual activity, and 4) revision of HD unit’s practices and procedures of infection control [16] .

Education and training in infection prevention and control should be provided to all HCWs upon hire and to be repeated regularly (at least once yearly). Basic principles and practices, including hand hygiene and wearing PPE, for preventing the spread of infections should be covered and monitored, and staff competencies should be assessed and documented upon orientation to the facility and to be repeated as appropriate for the specific staff and position [15] [69] . The patient(s) and/or caregiver(s) should also be educated on hand hygiene and the care of new vascular access and whenever there is a change in access type and repeated at least every year [70] [71] . Key areas for patient education as outlined by CDC are shown in Table 8.

Content source: 2001 CDC recommendations for preventing transmission of infections among chronic haemodialysis patients [35] , and 2008 KDIGO clinical practice guidelines for the prevention, diagnosis, evaluation and treatment of hepatitis c in chronic kidney disease [72] . HBsAg: Hepatitis B surface Antigen; HCV: Hepatitis C Virus; NAT: Nucleic Acid Amplification.

Content source: Centers for Disease Control and Prevention (CDC), National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Healthcare Quality Promotion (DHQP) [70] .

Contaminated hands of healthcare workers are among the most common modes of transmission of healthcare-associated infections. Hand hygiene is singled out as the most important infection prevention intervention. Compliance can be improved by continuous education, supervision and monitoring of hand hygiene behaviors, providing, in convenient locations, a sufficient number of sinks with soap dispensers, paper towels, hand lotions, and alcohol-based hand rub placed at each patient station. Equally important is the adherence to other Standard Precautions including glove and other PPE use, equipment and environmental cleaning, and safe injection practices, as well as other recommended practices of screening for HBV, HCV, HIV, tuberculosis infections, and immunizations. Regular feedback of surveillance results and steps taken to control spread of infection to everyone involved in the healthcare delivery would help to stimulate and encourage active engagement and improve compliance with infection prevention efforts. Education and training and full awareness of infection control policies and procedures should be provided to all HCWs and to be repeated regularly. The patient and/or caregiver should also be educated on hand hygiene and the care of new vascular access. Finally, implementation of evidence-based international guidelines is of great value and instrumental in helping reduce healthcare-asso- ciated infections, where patient’s safety and well-being remain a top priority.

No conflict of interest.

Ayman Karkar, (2016) Hand Hygiene in Haemodialysis Units. Open Access Library Journal,03,1-15. doi: 10.4236/oalib.1102953

ABHR Alcohol-Based Hand Rub

ARB Access-Related Bloodstream Infection

AVF Arteriovenous Fistula

AVG Arteriovenous Graft

APIC Association for Professionals in Infection Control and Epidemiology

BSI Bloodstream Infection

CDC Centers for Disease Control and Prevention

C. difficile Clostridium Difficile

DHQP Division of Healthcare Quality Promotion

EBPG/ERBP European Best Practice Guidelines/European Renal Best Practice

HAIs Healthcare-Associated Infections

HICPAC Healthcare Infection Control Practices Advisory Committee

HCW Healthcare Workers

HD Hemodialysis

HBsAg Hepatitis B Surface Antigen

HBV Hepatitis B Virus

HCV Hepatitis C Virus

HIV Human Immunodeficiency Virus

KDOQI Kidney Disease Outcomes Quality Initiative

LASI Local Access Site Infection

MRSA Methicillin-Resistant Staphylococcus Aureus

NAT Nucleic Acid Amplification

NCEZID National Center for Emerging and Zoonotic Infectious Diseases

NHSN National Healthcare Safety Network

PPE Personal Protective Equipment

VA Vascular Access

VAI Vascular Access Infection

VRE Vancomycin-Resistant Enterococci

WHO World Health Organization

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