Prevalence of scabies in long-term care hospitals in South Korea

Background Scabies is a common contagious skin disease. With the economic growth in South Korea, the incidence of scabies has decreased. However, with the recent advancements in medical facilities, mainly the establishment of long-term care hospitals (LTCHs), scabies is now considered an emerging public health problem. Methodology/Principal findings To examine the prevalence and management of scabies in LTCHs in South Korea, we contacted all 1,336 LTCHs registered at the Health Insurance Review and Assessment Service in South Korea in 2018. A total of 110 LTCHs completed a questionnaire, and we analyzed their responses. In the last 5 years, 71.8% (79/110) of LTCHs had a high incidence of scabies (suspected/confirmed cases). Usually, patients aged older than 80 years (45.5%) were diagnosed with the disease, with more women being affected than men. Only 30.0% of the patients were transferred to scabies-restricted rooms, and very few LTCHs (7.0%) had special departments for scabies. Fifty-five (61.1%) of 90 LTCHs reported contact between scabies patients and nurses, nurse aides, caregivers, and other employees (hereinafter, referred to as primary exposure), with 29 (32.2%) LTCHs reporting infections due to primary exposure. The most common challenges in managing scabies were patient isolation (47.8%), diagnosis (31.1%), management of individuals exposed to an individual with scabies (17.8%), lack of staff for managing the patients (16.7%), and treatment (11.1%). Conclusions The incidence rate of scabies in LTCHs in South Korea has increased. Regular and enhanced staff training is needed, considering that most hospitals rarely focused on the handling of equipment and furniture used by scabies patients and on educating their healthcare staff. These findings can be used to develop various strategies to reduce the prevalence of scabies.


Introduction
Scabies is an infectious skin disease caused by a mite (Sarcoptes scabiei var. hominis). It was considered one of the most commonly neglected tropical diseases by the World Health Organization (WHO) in 2017, and the parasite can quickly spread from one individual to another, resulting in an outbreak [1][2][3]. Several scabies outbreaks have been reported in nursing care homes (also referred to as nursing care facilities, elderly care facilities, long-term care facilities, and long-term care hospitals [LTCHs]) [4][5][6]. A review of institutional scabies outbreaks on a global scale revealed that 48% of the outbreaks were reported in LTCHs [7,8]. A review by Utsumi et al. in 2010 reported that 206 outbreaks in LTCHs caused by 37 pathogens, the scabies-causing mite was the fifth most frequently reported pathogen after influenza virus and norovirus, Salmonella spp., and group A Streptococcus [9]. The prevalence of institutional scabies is probably underestimated [10]. The incidence rate of scabies is expected to increase as the aging population grows.
Industrialization, poverty, overcrowding, and malnutrition are risk factors for infections [11][12][13]. Scabies is a contagious, itchy skin condition caused by mites burrowing and laying eggs under the skin. Scabies affects the infected individuals' daily lives due to itching and also affects the lives of others living with them; hence, scabies is considered a public health hazard. In particular, susceptible patients, such as children or elderly people, can acquire scabies through contact [14,15]. Scabies is also observed in people with normal immune system, and people do not become immune to the mites even after infection and recovery. Thus, prevention and treatment of scabies are considered important aspects.
Scabies can be transmitted among individuals in crowded or shared spaces (e.g., prisons or LTCHs) [16]. In South Korea, the number of LTCHs has doubled. There were 1,450 LTCHs nationwide in 2019, and the number has been increasing by 8% each year. Among the LTCHs, 401 had more than 14 elderly people in a room. The incidence of scabies among elderly people has increased due to the increase in facilities for elderly people, frequent transport of elderly patients to other facilities or hospitals, lack of attention and education about scabies, difficulty in diagnosis, and difficult to implement of certain treatments [17]. Elderly people with impaired immunity and neuropsychiatric or debilitating disease tend to develop crusted scabies; consequently, the risk of death increases [18]. Elderly people living in overcrowded rooms in LTCHs can be at risk of scabies.
The incidence rate of scabies in South Korea differs according to several reports, but ranged from 3.2% to 7.8% and from 3.7% to 9.1% in the 1970s and 1980s, respectively, in the outpatient dermatology departments in general hospitals [19]. Scabies has been commonly reported in the military, where military personnel live in groups; in rural areas, where sanitation is poorly implemented; and among socioeconomically backward sections of the society. Recently, many instances of group infections in LTCHs are being reported by the media in South Korea, suggesting an increase in the prevalence of scabies. A number of epidemiological and basic studies on the infection rates, clinical presentation, and risk factors of scabies have been conducted. However, few studies have investigated the prevalence of scabies at LTCHs nationwide in Korea. To our knowledge, no study has reported how LTCHs in South Korea manage scabies. Therefore, to develop effective strategies for scabies control, we investigated the incidence and management of scabies at LTCHs in South Korea.

Study design
A retrospective, cross-sectional study was conducted to determine the prevalence of scabies and the related management strategies in LTCHs.

Participants
Of the 1336 nursing homes registered at the Health Insurance Review and Assessment Service in 2018, 256 LTCHs agreed to voluntarily participate in this study. We distributed the survey questionnaires, and 110 LTCHs completed them (Fig 1).

Data collection
Data were collected from August to September 2018 using a structured questionnaire consisting of questions on the general characteristics and prevalence of scabies and the management of patients with scabies via online and offline surveys. The researchers contacted the infection control department or personnel in charge of infection control at all LTCHs nationwide. After agreeing to participate in this study, one survey questionnaire was sent to each of the LTCHs. Survey was completed based on hospital records by infection control personnel.

Ethical considerations
The study was approved by the Ethical Review Committee of Pusan National University Hospital, and each participant provided informed consent before enrollment (H-1805-010-067). Participation was entirely voluntary. Participants were informed of the purpose of the study and research ethics, including confidentiality and anonymity. The purpose of the study and procedures were explained to the participants. Those who voluntarily provided written informed consent were eligible for the survey. The participants were free to withdraw from the study at any point without penalty. All the participants were assured that the identity of the hospital would be deleted after coding for research analysis.

Instruments
Given the lack of a valid and reliable instrument for this study, a structured questionnaire was developed by the research team consisting of one parasitologist, one dermatologist, one health educator, one infection control specialist, and five nursing staff members who cared for scabies patients. We reviewed the literature on scabies including the US Centers for Disease Control and Prevention (CDC), Korea CDC, and European guidelines and research papers and textbooks on PubMed, CINAHL, RISS, and DBpia. We also interviewed medical doctors and nurses working at LTCHs to understand the situation in the LTCHs. A preliminary survey was conducted among the following: two department heads from the department of infection, two https://doi.org/10.1371/journal.pntd.0008554.g001 department heads from the nursing department, and two infection-specialist nurses who have been involved in nursing care for > 5 years in LTCHs. Based on the results, we revised the text and confirmed the final version of the questionnaire used in our study (S1 text).

Data analyses
Data were analyzed using the Statistical Package for the Social Sciences version 22.0 (International Business Machines Corporation, Armonk, NY, USA). Descriptive statistics were used to summarize the demographic characteristics of the participants and the prevalence and management of scabies. Differences in the prevalence of scabies according to the general characteristics of the participants were tested using the χ 2 test or Fisher's exact test.

General characteristics of the participants
In all, 110 LTCHs in 14 of the 17 administrative districts in Korea participated in this study. Among the 110 LTCHs, 60.0% had 100-200 beds, and 80.0% had grade 1 nursing staff. The numbers of patients managed by the healthcare staff were as follows: 31.1 ± 10.0 patients by one physician, 10.6 ± 4.9 by one nurse, 9.3 ± 9.1 by one nurse assistant, and 8.8 ± 5.8 by one care worker. Approximately 23% of hospitals had an infection control department, and 9.1% had administrative facilities such as a ward or unit for patients with infection. Approximately 89% of hospitals were equipped with scabies prevention and management guidelines, and 90.9% conducted staff training for scabies prevention and management. Moreover, 79% of hospitals had reporting systems for scabies ( Table 1).

Prevalence of scabies during the last 5 years
The prevalence of scabies during the last 5 years is shown in Table 2 and Fig 2. In the last 5 years, 71.8% (79 hospitals) of the hospitals had confirmed cases of scabies among both patients and staff. Calculations were based on the number of hospitals that reported scabies cases within 5 years (n = 79) for each year. In 2014, five hospitals had five patients with infection in total, which means that one patient was diagnosed with scabies per hospital. Three hospitals recorded infections in staff members. A total of seven employees had scabies, with up to three employees with scabies at one hospital. In 2015, nine hospitals had 11 patients with infection in total, with up to three patients with scabies in one hospital. Two hospitals had two employees with infection (one employee per hospital). In 2016, 16 hospitals had 35 patients with infection, with up to 12 patients in one hospital. Eight hospitals had a total of 65 employees with infection, with up to 40 in one hospital. In 2017, 38 hospitals had 98 patients with infection, with up to 30 in one hospital; 21 hospitals had 158 employees with infection, with up to 60 in one hospital. In 2018, 32 hospitals had 59 patients with infection, with up to eight in one hospital; 14 hospitals had 74 employees with infection, with up to 13 in one hospital. Of the scabies cases reported in the last 5 years, 20.3% of cases were those of crusted scabies. The percentage of cases that crusted scabies once occurred was 68.8%.

Characteristics of the most recently reported scabies cases
The characteristics of the most recently reported scabies cases are shown in Table 3. The incidence of scabies is increasing annually, and the highest rate was reported in 2018 (32.7%). Further, 61.8% of infections in LTCHs were primary infections, with patients as the primary source of infection in 97.2% of cases. The difficulty in identifying the primary source of infection is evidenced by the fact that 64.7% of the LTCHs tested their patients but could not confirm the diagnosis. The average time from the onset of suspicious symptoms to diagnosis was 10.00 ± 16.62 days, and 50.9% of the hospitals established the diagnosis of scabies within 1 week.

General characteristics of the patients with primary infection
The characteristics of the patients with primary infection are shown in Table 4. The calculations were based on the number of hospitals that reported patients with primary infection (n = 66). Of the total patients, 60.6% were women. The mean age was 77.60 ± 12.35 years; the most affected age group was 80-89 years (45.5%). The prevalence of crusted scabies was 22.8%. Regarding the admission route, 36.4% of the patients were admitted from other long-term care hospital. Approximately 83% of patients were suspected of having scabies at the time of admission. The most frequently observed symptoms were itching (83.6%) and skin lesions (58.2%).
The symptoms were usually observed on the whole body (36.4%) and on the fingers, hand, wrists, heel, foot, toes, and ears (15.2%); 19.7% of patients were taking steroid drugs. Table 5 shows the differences in the prevalence of scabies in the last 5 years according to the nursing homes' general characteristics. There was a difference in the incidence of scabies according to the number of hospital beds (p = 0.005) and the presence of an infection control department (p = 0.012). Regarding the number of hospital beds, 63.3% of the LTCHs with less than 100-200 hospital beds had patients with infection. Approximately 84% of the hospitals without an infection control department had cases of scabies.

Management of patients with scabies based on the most recently reported cases
Scabies management status was reported by 90 hospitals (81.8%), and the results are shown in Table 6. Calculations were based on the number of hospitals that reported their scabies  Number of individuals infected after being exposed to the patient with primary infection Table 7 shows the number of individuals who were infected by contact with a patient with scabies. Calculations were based on the number of hospitals that reported the number of individuals infected after being exposed to an individual with primary infection (n = 90). First exposure refers to direct contact with a patient with scabies, and the second exposure refers to the scenario in which the individual with first exposure comes in contact with another individual.   Table 8 outlines the difficulties and recommendations for infection control. Calculations were based on the number of hospitals that reported difficulties in infection control and suggestions for the same (n = 90). The most common problems were the isolation of patients (47.8%), diagnosis-related problems (31.1%), management of individuals who were in contact with patients with infection (17.8%), problems related to staff caring for patients with infection (16.7%), and treatment problems (11.1%). Regarding scabies prevention measures, educating the staff, including nurses, nursing assistants, and care workers, was the most frequently reported measure (80.0%), followed by ensuring a sufficient number of single rooms, isolation rooms, and personal protective equipment (77.8%); educating patients and their family (61.1%); preparing educational booklets, manuals, or guidelines for the prevention and management of scabies (54.4%); and establishing an infection control department (44.4%). Other measures included educating individuals responsible for the linen services in several hospitals.

Discussion
Although most LTCHs in this study had manuals for the prevention and management of scabies and reporting systems in their hospitals, the prevalence of scabies during the last 5 years has increased. Moreover, most LTCHs in this study experienced difficulty in controlling scabies. In this study, we investigated the characteristics of the staff and hospitals where scabies cases were reported; these features were analyzed to determine strategies to effectively control scabies. An estimated 200 million people worldwide have scabies [20]. Recently, instances of group infections in nursing homes or LTCHs have been consistently observed, with an increasing prevalence of scabies [15,21]. In the 1970s, the spread of scabies in South Korea was mainly restricted to homes, lodgings, and dormitories [22]. Since the 1980s, the prevalence of scabies in hospitals and facilities has increased due to the increase in LTCHs and nursing homes [23]. Scabies incidence in LTCH increased from 10% in 2014 to 58% in 2018, highest reported nearly 78% in 2017 Fig 2. Skin lesions or itching may not be present in people with severe crusted scabies. People with crusted scabies have numerous scabies mites and eggs, which are highly contagious [24]. The prevalence of crusted scabies was 22.8% among 66 patients with primary infection. Regarding the admission route, > 50% of patients with primary infection were admitted from other LTCHs. Further, 83% of patients had symptoms related to scabies at the time of admission, and 17% of patients did not have scabies-related symptoms (Table 4). That means we cannot rely on the occurrence of symptom. For suspected patients, contact precautions should be taken immediately until the diagnosis is confirmed. In the event of an unknown rash or itching in patients or staff, diagnostic tests should be performed immediately. Perhaps, new patients admitted to the hospitals can be screened for scabies and followed-up during the incubation period, as required. Calculations were based on the number of hospitals that reported the number of individuals with infection exposed to a patient with primary infection (n = 90).
It is interesting to note that LTCHs with larger number of beds (200-300) reported fewer scabies incidences than those with 100-200 beds, (23% vs 63% respectively). In South Korea, LTCHs with a larger number of beds seem to have better facilities and infection control system. Moreover, LTCHs with a larger number of beds employ infection control personnel as the South Korean government established a law that hospitals with > 150 beds should have an infection control room and dedicated personnel in 2018. Furthermore, LTCH with a large number of beds does not mean that many patients have stayed in a room.
LTCH with a large number of beds does not mean that many patients have stayed in a room. We found that confirmation of scabies diagnosis took over a week in approximately half of the cases (Table 3), resulting in the spread of secondary infections, making treatment difficult. Only 61.8% of hospitals reported difficulties in identifying individuals with infection (47.1%) and in accurately diagnosing an individual with scabies (Table 3). Abdel-Latif et al. showed that only 10%-22% of presumptive scabies diagnoses based on the results of skin scraping, adhesive tape testing, and dermoscopic examination were accurate [25]. Therefore, confirming the diagnosis of scabies is difficult and usually takes a long time. Although some molecular and immunological diagnostic tests have been suggested such as a nested polymerase chain reaction assay for detecting Sarcoptes scabiei DNA in skin scrapings or IgE specificity for a recombinant allergen of Sarcoptes scabiei [26,27], they are not widely used for scabies.
Scabies is a contagious skin infestation that is quickly transmitted from one individual to another. However, this transmission might be inhibited by quickly isolating the patients with infection and by properly managing them based on the guidelines for scabies with the help of an infection control specialist. Providing regular education to the hospital staff and patients about scabies is considered beneficial in the prevention and control of scabies [28]. In this study, although most hospitals reported that they provided education on scabies to the staff (Table 1), they also suggested that regular education was necessary to control scabies outbreaks (Table 8). Therefore, we are not sure whether the education provided to the staff was effective or sufficient. One-time training and educating the staff only are not enough for preventing the spread of scabies. Increased efforts are needed to increase the effectiveness of scabies-related education. A systemic approach, such as the Predisposing, Reinforcing, and Enabling Constructs in Educational Diagnosis and Evaluation: Policy, Regulatory, and Organizational Constructs in Educational and Environmental Development (PRECEDE-PROCEED) model-based education, can be used for designing, implementing, and evaluating education measures. In addition, information on scabies should be shared with all employees, besides the clinical staff, and with the patients and their guardians/families. Furthermore, administrative support for the prevention and management of scabies should be provided, including dedicated staff to manage scabies patients, adequate resources, and a clean environment.
It is important to understand whether the staff at LTCHs have the right information about scabies and to identify the source of this information so as to increase educational effectiveness. Further studies need to explore the knowledge level and content of the educational courses provided to the staff at LTCHs. That would provide information about the weaknesses and strengths of knowledge.
The staff have experienced difficulties in controlling the spread of scabies in their hospitals, with patient isolation and establishment of an accurate scabies diagnosis being the most prominent difficulties (Table 8). Regarding patient isolation, the following difficulties were encountered: insufficient facilities for long-term isolation, insufficient supplies such as linens and personal protective equipment, and difficulty in identifying and transferring patients with infection to other hospitals with facilities for long-term isolation [8,16]. Transferring elderly long-term inpatients to a dermatology outpatient clinic, due to the absence of a dermatologist at the LTCHs, was also problematic. Most LTCHs in Korea employ medical doctors who specialize in internal medicine or family medicine. If a suspected patient has sufficient mobility, the medical doctors in the LTCHs refer the patients to a dermatologist. If a patient is severely ill (or has poor mobility), the diagnosis of scabies depends on medical history and clinical symptoms and signs. We believe that medical doctors working at LTCHs should be familiar with scabies as it has become a common problem among elderly people living in LTCHs.
Additionally, early diagnosis of scabies was difficult because of the long latency period of the disease. Latent symptoms of itching occur due to suppression of innate immunity. Moreover, accurate diagnosis of scabies was difficult due to the inability of the physicians to differentiate scabies from other skin diseases, specifically contact dermatitis, and to confirm whether a patient transferred from another medical institution had the infection.
Specific difficulties in the management of individuals coming in contact with patients with infection are as follows. First, it is significantly difficult to determine all contacts, including other patients, visitors, and employees, for possible treatment because these individuals would not want to be treated and because of the insufficient number of isolation rooms. The management of these individuals is considered difficult considering that visitors and patients' families do not always cooperate with the healthcare staff because they have insufficient knowledge of scabies and they do not trust the hospitals. For instance, visitors and patients' families do not want to spend a significant amount of their time in a hospital. Difficulties pertaining to healthcare personnel are as follows: lack of healthcare staff (in charge staff or an infection control specialist) and insufficient knowledge regarding proper management of the infection. Limiting employees' direct contact with patients with infection/suspected infection is difficult considering the insufficiency in healthcare staff.
Second, with the absence of regular education on scabies, immediate management of patients with infection is difficult. Particularly, with the increase in the employment of Chinese care workers, proper education regarding scabies, with consideration given to Chinese culture, should be provided. Lack of education could lead to increased avoidance of care among the health workers and patients.
Third, the healthcare staff consider individuals who come in contact with patients suspected of having scabies overbearing because they refuse prophylactic dermatological care or preventive treatment. One scabies patient can spread the infection to more than 100 individuals, including employees, employees' families, and visitors. Hence, treating everyone suspected of having been in contact with scabies patients is considered difficult. If a patient or employee complains of chronic skin rash and pruritus, treatment is usually provided even if scabies is not yet confirmed because of the possibility of transmission and relapse.
Furthermore, patient rehabilitation is considered difficulties in an accurate diagnosis and treatment of scabies and the burden of isolation. Finally, it is difficult to claim medical expenses for scabies treatment. Hospital managers neglect scabies or hospitals tend to conceal rather than actively cope with scabies cases. Difficulty in reporting scabies is also observed due to lack of trust in medical institutions.
There are some limitations to this study. Only 10% of the LTCHs in the entire country participated in this study, probably resulting in a selection bias. Moreover, this was a retrospective cohort study, and thus, memory bias was also possible. Further studies with a prospective design are needed to reduce the potential sources of these biases. Despite these limitations, this study provided valuable information for understanding the prevalence of scabies and management of patients with scabies in LTCHs in South Korea. The incidence rate of scabies in LTCHs in South Korea has increased. The rate was significantly higher in hospitals without an infection control department than in hospitals with such a department. Our findings highlight the need for providing well-organized education on infection management to all employees, patients, caregivers, and their families. In addition to this mandate, special instructions, such as screening tests for newly admitted patients to LTCHs, should be prepared to reduce the transmission of scabies.
Supporting information S1 Text. Questionnaire for investigation of the prevalence and management of scabies in long-term care hospitals in South Korea. (DOCX)