Since healthcare personnel's hands can be the common mediator for microbial propagation in hospital environments, hand hygiene has been the best strategy to reduce the human-to-human transmission of microorganisms [1]. Hand hygiene is the most effective prevention method that protects both patients and visitors from healthcare-associated infections in hospital settings [2]. Because the hand hygiene compliance rate is the most basic and indispensable indicator for infection control [3], most Korean hospitals have conducted hand hygiene monitoring activities for their healthcare personnel [4]. According to the World Health Organization (WHO), hand hygiene compliance rates among healthcare personnel have been reported at around 30~80% in general since 2007 [3]. The hand hygiene compliance rate of healthcare personnel in Korea has been reported to be 32~95% [5, 6, 7]. A variety of interventions to improve hand hygiene compliance have been made around the world, including providing hand hygiene training to healthcare personnel to improve hand hygiene performance, improving the accessibility of alcohol-based gel hand sanitizers in hospitals, and developing hand hygiene monitoring and feedback programs [8, 9]. Some studies also reported that the improvement in hand hygiene performance as a result of these interventions significantly reduced the incidence of healthcare-associated infections [10, 11, 12].

Theoretically, not only healthcare personnel but also hospital visitors can be seen as sources of infectious agents [13], but the impact of hospital visitors on infection transmission has not been yet clearly assessed. Regarding the Middle East Respiratory Syndrome (MERS) epidemic that occurred in 2015, the Korea-WHO MERS Joint Assessment Team evaluated that visitors' unlimited access to hospital wards facilitated the rapid spread of MERS. In fact, among domestic MERS confirmed cases, 34.9%(N=65) were family members or visitors [14]. This indicates that the visitors' role in transmission of healthcare-associated infections in Korea is not negligible. However, since most infection control guidelines in healthcare settings are only for healthcare personnel or employees, the need for standardized infection control guidelines targeting visitors has been raised recently in various studies [15, 16, 17]. Although hand hygiene practices by visitors must be performed both before and after touching a patient [15], several studies abroad have reported that the hand hygiene performance of hospital visitors was significantly lower than that of healthcare personnel. According to an observational study that examined hand hygiene compliance among 3,000 total visitors in terms of the use of alcohol-based hand sanitizer at the hospital lobby of a U.S. hospital with 749 beds, the hand hygiene compliance rate of visitors was 0.52% before the intervention [18]. After the intervention of installing an alcohol-based hand sanitizer stand and an information display, the rate rose to 11.67%. These rates were substantially lower when considering that the study evaluated hand hygiene compliance only in a hospital lobby. Similarly, a previous study examined hand hygiene compliance among a total of 6,603 visitors after a different arrangement of alcohol-based hand sanitizer stands in the lobby of a US tertiary hospital with 560 beds, and it reported that the hand hygiene compliance rate was as low as 3.71% on average [19]. In a study conducted in the U.K., the direct, 24-hour observation of two internal medicine wards showed that the hand hygiene compliance of visitors was 57% [20]. According to a systematic literature review about the studies of hand hygiene compliance that covered publications up to May 2016, the hand hygiene compliance rates of visitors were 0.5~11% at the hospital entrance, 9~35% in the general ward and surgical ward, 11% in the isolation room, 39% in the pediatric ward, 3.95~49.1% at the patient's bedside, and 7~94% in the intensive care unit [21]. Nevertheless, considering the environments of Korean healthcare settings where visitors frequently spent time in patient rooms, infection control activities targeting visitors are very important, but research on the hand hygiene of visitors is insufficient in Korea due to a lack of resources and a shortage of healthcare personnel.

In Korea, the number of long-term care hospitals increased from 202 in 2005, to 900 in 2011, and to 1,428 in 2016, due to an increase in geriatric diseases as Korea has become an aged society [22]. Elderly patients admitted to a long-term care hospital are likely to be exposed to infectious diseases or opportunistic infections due to their longer stay of hospitalization, and their highly frequent social contacts that increase cross-infection risks, such as routine face-to-face contact with caregivers or other patients, have been reported to increase healthcare-related infections in long-term care hospitals [23]. Therefore, this study aimed to investigate the hand hygiene performance among visitors of a long-term care hospital, and to compare the hand hygiene compliance rate by age, gender, and behavior type in order to provide basic data which can contribute to the development of infection control guidelines and hand hygiene education programs for visitors to long-term care hospitals.

The targeted 1,000 observations of moments for hand hygiene were accomplished from a total of 766 visitors. The average number of hand hygiene moments per visitor was 1.31. The average hand hygiene compliance rate was 20.3%(i.e., 203 cases among a total of 1,000 observations).

The general characteristics of 766 visitors observed were summarized in Table 1. Regarding gender, males were more predominant (56.8%) than females (43.2%). In terms of the estimated age group, most of the visitors were adults (76.2%), then, adolescents (10.2%), elderly (9.7%), and children (3.9%) in order. The adults group showed the highest hand hygiene compliance rate of 23.4% among all the age groups, as they accounted for the most observed (N=730). The groups of children and elderly showed significantly lower hand hygiene compliance rates of 9.4% and 8.2%, respectively. Gender differences in hand hygiene compliance were not observed.

Table 1 Summary of Results of Hand Hygiene Practices among Visitors in a Long-term Care Hospital (Total Number of Hand Hygiene Opportunities=1,000) Click for larger image

Among the 203 cases of hand hygiene compliance, hand hygiene was performed using soap and water in 109 cases (53.7%), and alcohol-based gel was used in 84 cases (46.3%). Of note, 78.9% of compliant adolescents (N=15) used alcohol-based gel for their hand hygiene more frequently than soap and water. Regarding the type of hand hygiene indication, the hand hygiene method using alcohol-based gel was used more frequently than soap and water only in the cases of “before touching a patient” which was the most frequently observed (N=620).

Although the most frequently observed indications were “before touching a patient” (16.1%) and “after touching a patient” (14.0%), the hand hygiene compliance rates for these two types of behaviors were significantly low at 16.1% and 14.0%, respectively. In particular, in the case of “after touching the patient's surroundings,” the hand hygiene compliance rate was the lowest at “7.5%,” and was extremely low at 0% (N=14) in all the age groups, except the adult group which showed a hand hygiene compliance rate of 9.1% (Table 2). In the case of the group of children, the number of observed cases of moments for hand hygiene per child was 1.77, which was higher than the average of 1.31 cases per visitor. In the total number of observations, the cases of “after touching a patient” accounted for 37.7% (20/53), which was higher compared to 18.4% (134/730) in the adult group and 22.7% (22/97) in the elderly group. In the group of children, 4 out of 5 cases of hand hygiene compliance were performed following their parents' behaviors or with their parents' assistance.

Table 2 Hand Hygiene Compliance by Age Categories according to the Four Moments Click for larger image

In the case of “after body fluid exposure risk,” the hand hygiene compliance rate was the highest at 83.5%, and most of the subjects (93.9%) performed hand hygiene with soap and water (Table 1). The total 79 cases related to “after body fluid exposure risk” were more likely to be potential exposures to body fluids while visitors assisted patient daily care, for instance, when touching an inserted bile bag during changing clothes. Of these, 4 cases exposed to two types of fluids at the same time (Table 3). The most commonly exposed potential body fluid was saliva (48.1 %), followed by excretions (17.7%), secretions (17.7%), sputum (11.4%), and blood (10.1%) in order; there is a possibility of exposure to the blood of patients through touching the insertion site of a venous catheter.

Table 3 Visitors' Hand Hygiene Compliance and Potential Exposure Behaviors to Different Types of Body Fluid Click for larger image

This study investigated the hand hygiene compliance rate of visitors of a long-term care hospital by the covert observation method and reported a 20.3% compliance rate, which is significantly lower than 32~95% among healthcare personnel reported in other studies [5, 6]. Our hand hygiene compliance rate of hospital visitors was similar to the compliance rates (0.52~36.3%) reported in most studies on visitors' hand hygiene compliance from other countries [19, 26, 27]. Considering the domestic hospital environments and the Korean cultural aspects of visiting a sick friend or relative in the hospital characterized by frequent visitations, it is necessary to pay attention to the hand hygiene of visitors.

Our study found statistically significant differences in the hand hygiene compliance rate among age groups. In particular, the hand hygiene compliance rate in the age group of children was very low (9.4%). In the long-term care hospital in which this study was conducted, 5.3% of the visitors were children. Although children were not the main age group of the visitors, the average number of hand hygiene opportunities per child was 1.77 and the rate for the “after touching a patient” indication was 37.7%, which is higher than other age groups. In our study observation, since some parents had difficulty controlling the behavior of children, children ran around in the hospital after touching a patient and touched commonly shared items or patients' surroundings, which could cause spread of infections. In addition to children's likelihood of transmitting infection in the hospital environment, since children have immature immunity compared to adults [28], the need for hand hygiene is emphasized more when children visit a hospital. In particular, since children were observed carrying out hand hygiene mostly when following their parents' behavior or with their parents' help, it is necessary to develop a strategy for improving the hand hygiene performance of children in a long-term care hospital by including both children and their parents in the targets of a hand hygiene education program.

In our study, most visitors seemed sensitive to visible contaminations and tended to perform hand hygiene, but they did not routinely perform hand hygiene for hand hygiene moments that had invisible, potential contaminations. The most frequently observed hand hygiene moment among visitors was “before touching a patient”, but compliance was significantly low (16.1%). Conversely, the least observed hand hygiene moment was “after body fluid exposure risk”, but compliance was highest (83.5%). This is consistent with previous studies that reported a high hand hygiene compliance rate after behaviors involving body fluid exposure [3, 20]. Moreover, the hand hygiene compliance rate for “after touching a patient's surroundings” was extremely low (7.5%). In particular, except for the adult group, the other age groups did not perform any hand hygiene for “after touching a patient's surroundings.” This result is similar with another study's finding that hand hygiene performance was the lowest after touching the patient's surroundings [29]. Therefore, it is necessary to develop an educational program to change visitors' awareness on hand hygiene moments by showing that microbial propagation can be possible not only by contamination but also by simple skin contact or contact with the patient's surroundings.

Our study finding that only adolescents used alcohol-based gel more than soap and water is similar to another study's result that the younger-aged group preferred to use alcohol-based gel compared with middle-aged and elderly groups [19]. This difference in the hand hygiene methods may be affected by the fact that alcohol-based gel sanitizers were not placed in patient rooms or near the beds but placed only at the entrance of each ward to prevent any harmful accidents, due to the frequent prevalence of dementia among hospitalized elderly patients in the study hospital. In addition, a single sink location for using soap and water in a shared patient room (i.e., 5~6 patients per a room) might affect visitors' hand hygiene compliance and hand hygiene methods.

Importantly, the results of this study revealed that visitors were also exposed to body fluids such as saliva, urine, feces, and sputum. Most family visitors had skin contacts with the patient, such as greeting, arm or leg massage, or moving support. Moreover, they were likely exposed to the patient's body fluids through contact with an inserted device (e. g., urine bag) while assisting patient care in ways that are commonly expected from the traditional Confucian ideals of caring for elderly parents. In some rare cases, some visitors were exposed to the blood of the patient through the contact with the insertion site of the central venous catheter or peripheral venous catheter of the patient. Fortunately, it was found that the hand hygiene compliance rate was much higher (83.5%) “after body fluid exposure risk,” and that most visitors performed hand hygiene with soap and water in such cases (93.9%). However, since it was shown that there is a sufficient possibility that visitors of long-term care hospital will be exposed to body fluids, it is necessary to implement active educational interventions to increase the hand hygiene performance among visitors.

This study has the following limitations. First, our study's compliance results among visitors are not generalizable, because hand hygiene observations were conducted for limited weekend meal-time periods when most visitors were present in the studied long-term care hospital. Second, although the direct observation method with the advantage of examining details such as the degree and duration of hand hygiene during observation [1] was applied, one observer had to observe a maximum of 3 visitors perform hand hygiene compliance at the same time around meal hours when there were a number of visitors. Thus, our study could not measure the duration of hand hygiene and the adequacy of the hand hygiene performance by visitors. In order to supplement this limitation, the two observers-method could be adopted for monitoring the hand hygiene performance at the same time, but inter-observer reliability between two observers needs to be secured. Moreover, in a rather uncrowded place like a long-term care hospital, some difficulties are expected to conceal the presence of two observers naturally and conduct covert observation. Third, there may be the limitation of excluding overlapped people from the observation of the next sessions based on the memory of the sole observer. Fourth, because the study was conducted by the covert observation method which makes it possible to accurately examine the actual performance of the subject because the subject does not know that his or her hand hygiene performance is being observed, factors which may influence hand hygiene performance such as the age, the education level, and the experience of hand hygiene education could not be examined and included in the analysis. Fifth, since the subject's age could not be accurately confirmed by the limitation of covert observation, the estimated age groups of visitors were divided only into children, adolescents, adults, and elderly, and could not be divided in a more specific manner. Sixth, since our study observation were conducted only during the specific time periods of weekends and the single holiday, our study could not monitor all of the hand hygiene compliance during 24 hours.

Despite the above limitations, this study is the first research attempt to examine the hand hygiene compliance rate among the visitors of long-term care hospitals in Korea, and provides meaningful basic data on the hand hygiene compliance rate of hospital visitors. In fact, to improve hand hygiene performance, multi-modal interventions are necessary because hand hygiene compliance is affected by various factors, such as the system change of healthcare institutions, policies, and social norms, as well as education and training [30]. Therefore, our study results are expected to contribute to the improvement of the hand hygiene compliance of visitors by being adopted for the development of the guidelines for infection control and the hand hygiene education program for hospital visitors.

This study was conducted to investigate the hand hygiene compliance rate among visitors of long-term care hospitals. A total of 1,000 cases of moments for hand hygiene were observed from 766 visitors, and the overall hand hygiene compliance rate of the visitors of a long-term care hospital was 20.3%. Therefore, hand hygiene education programs and infection control guidelines for hospital visitors in long-term care hospitals need to be developed and implemented.

Based on our study results, the following future studies are recommended. First of all, more studies on hand hygiene compliance among visitors are necessary at a number of different long-term care hospitals with various numbers of visitors. Moreover, not only limited to long-term care hospitals, more expanded research on visitors' hand hygiene compliance need to be conducted across healthcare settings, such as tertiary hospitals and general hospitals. Further studies on visitors' knowledge, attitude, and factors related hand hygiene performance would be essential to understand visitors' hand hygiene performance better. In addition, it would be meaningful to conduct a covert observation study to investigate the overall performance of the infection control guidelines for visitors, such as standard precautions and mask-wearing, not only for hand hygiene, at long-term care hospitals. Given the lack of standardized hospital visitors' infection control guidelines, we need more evidence to understand visitors' characteristics by age group, gender, and behaviors or interactions at each hospital setting. Based on our study results showing the differences in the hand hygiene compliance rate and the frequency of the use of hand hygiene methods among visitors, customized, effective educational programs for hospital visitors need to be established reflecting patient characteristics, hospital environments, and visitors' needs for education on infection control.