Background
Scabies is an infectious disease caused by exposure to
Sarcoptes scabiei varietas hominis. It spreads through close skin-to-skin contact with an infected person [
1]. Infection with scabies causes symptoms, such as itching that worsens at night, rash, excoriated papules, eczematous lichenified plaques, and nodules [
2,
3]. Secondary bacterial infections are complications that cause significant morbidity and mortality [
4]. Scabies infection affects physical symptoms and quality of life, such as restriction of leisure activities and stigma [
5,
6]. It occurs worldwide, and its prevalence was estimated at 175.4 million in 2017 [
7]. The World Health Organization (WHO) classified scabies infection as a “neglected tropical disease” common in all races and classes [
8], meaning that a deep understanding of the social burden caused by scabies infection is needed. Scabies is a major public health problem to be addressed [
9].
Although parasitic infections play a significant role in nosocomial infections, awareness of parasitic infections is generally low compared to bacterial, fungal, and viral nosocomial infections. Consequently, diagnosis and treatment are significantly delayed [
10]. The period from the onset of the first symptoms to diagnosis was more than 2 weeks in 46.1% of the patients [
11]. Scabies transmission occurs when the diagnosis is delayed. The average number of infected patients per scabies outbreak was reported to be 18, and the average number of infected hospital care workers was 39, indicating high intrahospital transmission of scabies [
12]. Therefore, prompt diagnosis and treatment are necessary.
However, nonspecific skin symptoms are more common in scabies than in typical features, such as burrows. As the clinical morphology of scabies is diverse [
2,
13], it may be difficult to differentiate the diagnosis based on skin symptoms alone. Scabies is difficult to diagnose because it show a variety of clinical symptoms and severities [
14], and unfamiliar atypical symptoms can lead to misdiagnosis by medical personnel [
12]. Therefore, asking about risk factors for scabies, such as one’s living environment and skin symptoms, can provide insight into the diagnosis [
15,
16]. In addition, early diagnosis questionnaires assessing risk factors play an important role in screening individuals for diseases [
17,
18]. Hospital-based risk factors for scabies can also help distinguish scabies outbreaks.
To the best of our knowledge, systematic reviews of risk factors for scabies infection have primarily focused on community-based studies. Therefore, we aimed to identify the risk factors for patients with scabies in hospital settings, those who were diagnosed during outpatient visits, hospital admissions, or acquired within the hospital. Through this systematic review, we present the factors that help diagnosing scabies, with the intention of contributing to reducing disease transmission and burden.
Methods
Search strategy
The current systematic review was registered with the PROSPERO International Prospective Register of Systematic Reviews (ID: CRD42023363278). The study’s preliminary search was conducted on September 29, 2022, and the search was conducted from February 2 to 4, 2023. We searched the literature from the international PubMed, Embase, and CINAHL databases and the Korean domestic DBpia, KISS, RISS, and Science ON databases. The search terms were combinations of each database’s natural and control words for scabies, risk factors, and research settings (
S1 Table). In addition, we added a search term to rule out animal research. The Boolean operator was used to combine terms and concepts. The search terms for the same concepts were combined with OR. The concepts were combined with AND or NOT. In addition to the academic databases, the study searched using Google Scholar by combining the words “scabies,” “risk factors,” and “hospital”.
Article selection
The process of selecting studies is shown in S1 figure. We included a quantitative study of the risk factors for hospital infections of scabies. There were no restrictions on the year of publication or the age of the participants. The participants were not limited to patients but also included studies on hospital care workers.
First, duplicate papers were removed using the RefWorks program, and duplicate papers were excluded by manually checking them again. Next, two authors screened the titles and abstracts and excluded studies that did not address scabies. Next, we checked the full text of all retrieved studies to assess eligibility according to the inclusion and exclusion criteria. The inclusion criteria were studies (a) identifying risk factors for scabies infection; (b) hospital-based; (c) on the factors using calculated risk estimates with a 95% confidence interval; and (d) published either in English or Korean. The exclusion criteria were (a) Irrelevance (studies conducted in non-hospital settings, those not using statistical analysis for risk estimates with a 95% confidence interval, or those that do not identify risk factors); (b) conference abstracts, letters, posters, comments, or editorials; (c) protocols; (d) theses; (e) reviews; and (f) qualitative research.
In the case of Google Scholar, we combined search terms, such as scabies, risk factors, and hospitals. Then, we screened the titles and abstracts to extract our research topics and relevant studies and read the full texts to assess eligibility.
The process of selecting a study was conducted by two authors. If the two authors differed, the third author decided whether to include them.
Search outcome
A total of 121 studies were found in the seven databases. Twenty duplicate studies were removed using RefWorks, and five duplicate studies were removed manually. In addition, two authors screened the titles and abstracts of 96 studies and excluded 25 studies that did not address scabies and one study involving animals. 70 studies were retrieved; therefore, we checked the full text and reviewed whether it was included based on the criteria of this systematic review. As a result, seven studies were included in this review.
In Google Scholar, we could not evaluate all the documents retrieved, so we reviewed 150 papers based on the searched list in order of accuracy. As a result, the full text of 17 papers dealing with risk factors for scabies was reviewed, and five studies were included. In conclusion, 12 studies were included in our systematic review using academic databases and Google Scholar.
Data were extracted by two authors. Data extraction included a wide range of categories, such as author and publication information, study settings, study population, participant characteristics, diagnosis type, study design, prevalence, and risk factors evaluated in each study (
S2 Table). Not clearly data were verified by emailing the authors.
Quality assessment
Two authors independently performed a quality assessment using the Joanna Briggs Institute critical appraisal tools [
19]. The designs of the studies in our review varied from cross-sectional, case-control, and cohort. We chose to use JBI’s critical appraisal tools because they offer quality assessment tools for all three designs. In summary, these tools assessed the quality of the participant selection, confounders, measures, and statistics. We judged the risk of bias to be low if 50% or more of the answers were “yes.” In contrast, the risk of bias was high if 50% or more of the responses were “no,” and the risk of bias assessment was if 50% or more of the “unclear” answers were judged as uncertain [
19].
Table
1 shows the results of the qualitative assessment. Three studies did not meet the 50% “yes” criteria [
20‐
22]. In addition, we emailed the original authors of one of the retrospective studies to confirm the concept of the study [
23], such as cohort or case-control but did not receive a response. After discussion among the three authors, we determined that the purpose and design of the studies were acceptable for inclusion in our systematic review.
Table 1
Quality assessment
1st author (year) | Q1 | Q2 | Q3 | Q4 | Q5 | Q6 | Q7 | Q8 | Rate of Y | |
| Y | Y | N | Y | N | N | Y | Y | 62.5% | |
| Y | Y | N | Y | N | N | U | Y | 50% | |
| N | Y | N | Y | N/A | N | Y | Y | 50% | |
| Y | Y | U | Y | N | N | U | Y | 50% | |
Case-control studies | |
1st author (year) | Q1 | Q2 | Q3 | Q4 | Q5 | Q6 | Q7 | Q8 | Q9 | Q10 | Rate of Y |
| Y | Y | Y | Y | Y | Y | Y | Y | Y | Y | 100% |
| N | Y | Y | N | Y | N | N | U | U | Y | 40% |
| Y | Y | Y | N | Y | Y | Y | Y | Y | Y | 90% |
| Y | Y | Y | Y | Y | N | N | Y | U | Y | 70% |
| N | N | N | N | Y | N | N | Y | U | Y | 30% |
| Y | Y | Y | Y | Y | N | N | Y | U | Y | 70% |
Cohort study | |
1st author (year) | Q1 | Q2 | Q3 | Q4 | Q5 | Q6 | Q7 | Q8 | Q9 | Q10 | Q11 | Rate of Y |
| Y | Y | Y | N | N | U | Y | U | U | U | Y | 45.5% |
Discussion
We conducted a systematic review to identify the risk factors for scabies to prevent infection; in this study, 12 hospital-based studies identified risk factors for scabies. The studies were divided into personal and clinical risk factors and confirmed that scabies was a multifactorial occurrence.
Personal factors were grouped into demographic, economic, residential, and behavioral risk factors. Among the demographic characteristics, men were identified as at a greater risk for scabies than women. Community-based studies that support this result were conducted in Ethiopia [
32] and Liberia [
33], and a study in Nigeria contradicted these results [
34]. However, care must be taken in interpreting gender, as it may be a result of the cultural characteristics of the surveyed region or a result that does not reflect the population. In the case of education level, when the education level was low, the understanding of preventive behavior and treatment for infectious diseases was low, and the risk of scabies was greater. However, when the education level was higher and income was higher, the risk of scabies outbreaks was lower because patients could have more frequent medical consultations [
32]. Demographic characteristics can be recognized in screening for the diagnosis and identification of patients at risk for scabies infection.
Each of the five studies had different standards for economic levels, such as income, economic level, type of insurance, and occupational status. Taken together, it was judged that the risk of scabies is greater for individuals with lower economic income. A study identifying the risk factors for scabies in the community also reported that the lower the annual income level was, the greater the incidence of scabies [
32,
34,
35]. People with low economic status often have poor living conditions, which can lead to the transmission of scabies [
35]. In addition, treatment-related costs affect family income, and daily hospital visits are costly; economic problems are both a cause and consequence of illness [
36]. These studies suggest that economic level should be considered a major factor in the early screening for scabies.
Regarding the type of residence, each study reported various results making it difficult to merge; however, nursing homes and long-term care facilities show similar residence characteristics; for example, patients live in unavoidable contact for a long time. Closed communities experience higher incidences of scabies [
37,
38]. Moreover, scabies in nursing homes are particularly asymptomatic or atypical, reaching 51% [
37]. These factors may increase silent transmission, suggesting that hospital admissions or visits may not be aware of scabies infection. Therefore, patients who visit hospitals and have a history of living in a nursing home or long-term care facility should be thoroughly screened for the occurrence of scabies.
Among the behavioral factors, unsanitary behavior and sharing or contacting objects with others were identified as risk factors. While Dagne et al.’s (2019) and Yassin et al.’s (2017) studies in the community showed the same results [
39,
40], the results of the meta-analysis reported by Azene et al. (2020) were not significant [
41]. Hygiene behavior due to a lack of facilities in the home is difficult to modify, but it is a factor that can be sufficiently changed in terms of education. Previous studies have reported that the incidence of scabies decreased after education on personal hygiene [
42,
43]. Therefore, educational programs and preventive activities are needed to prevent the occurrence of scabies. Sharing or touching objects with others was also found to be a risk factor for scabies. Healthcare providers were responsible not only for treating scabies but also for preventing their spread. This is based on limiting contact with ticks, early diagnosis, and appropriate health education [
44]. When a patient with scabies symptoms visits a hospital, it is important to screen quickly. However, if immediate diagnosis or screening among patients with risk factors is not possible, it is necessary to educate patients to use individual objects during the incubation period of at least two weeks. Moreover, frequent contact with patients or failure to wear protective equipment were identified as risk factors for medical staff and hospital personnel. An infection control system, such as wearing personal protective equipment for infection protection by medical personnel dealing with symptomatic patients, should be established.
Clinically related risk factors were divided into individual medical characteristics and hospital environments. Among the individual clinical characteristics, there were two studies on activity status, and the results of each study were contradictory. In a study by Tsutsumi et al. (2005), the incidence of infection was higher when there was frequent movement [
31]. As scabies infection occurs through contact, Hay et al. (2012) showed the same outcome [
38]. In contrast, Wang’s (2012) study indicated that patients in a bedridden state were at greater risk of occurrence [
26]. Patients in a bedridden state may be vulnerable to infections owing to reduced immunity [
45,
46]. Immunosuppression, such as immunodeficiency, the presence of immunosuppressive factors, or malnutrition, increases the incidence of scabies [
47‐
49]. In addition, nosocomial scabies was associated with an immunocompromised status [
12]. Moreover, bedridden patients may have difficulty expressing pruritus, a major symptom of scabies. Skin-to-skin contact is the most common transmission route for scabies, and even healthy individuals can become infected with scabies through contact [
1,
38]. In this context, the possibility of healthcare workers transmitting infection to bedridden patients can also be considered. Therefore, regular skin screening in hospitals for bedridden patients is necessary. Wang et al. (2012) reported that patients with higher APACHE scores, more catheters, and longer hospital stays were more susceptible to scabies infection. This suggests a correlation between the severity of the patient’s condition and scabies infection [
26]. Only one study identified patient severity as a risk factor for scabies, so further research is needed.
In two studies, itching in close family members or acquaintances was significantly associated with scabies [
25,
29]. This is supported by findings from previous community studies [
34,
41]. Therefore, when taking the history of patients with skin diseases, checking whether a family member has pruritus is an important question in diagnosing scabies.
Hospital environmental risk factors were found in only one study, making integration difficult. As environmental factors also affect the occurrence of scabies [
38], follow-up studies on the degree of scabies occurrence according to hospital characteristics are necessary. Additionally, regarding environmental risk factors, patients in long-term wards were more vulnerable to scabies [
28]. Therefore, we again emphasize screening patients hospitalized for a long time.
Recently, active research has been conducted on the early screening of patients with risk factors. For example, Quéreux et al. (2010) developed a self-assessment questionnaire using risk factors for melanoma [
50]. Nichol et al. (2019) created a self-screening tool using risk factors for hand dermatitis among healthcare workers [
51]. These screening tools reduce the efforts of medical staff by helping to select subjects for full skin examination and play a significant role in determining individuals with the possibility of disease detection [
17,
18]. Diagnostic programs incorporating new technologies, such as a deep-learning system that predicts diseases using images of skin lesions, are also being developed [
52,
53]. Even in deep learning, genetic, life, and demographic risk factors can be input and combined as variables to achieve better model performance. In addition, risk factors can be input as data variables [
53,
54]. The risk factors for scabies identified in our study can be used to develop various screening tools or programs.
Of the studies included in our systematic review, 10 of the 12 were conducted in Asia/Pacific [
22‐
31]. Most research on scabies has focused on countries with a low-to-moderate United Nations Human Development Index (HDI) or disadvantaged populations in countries with high HDI. Thus, nonindigenous population data for North America, most of Europe, and Australia were lacking [
55]. However, the prevalence and incidence of scabies have increased in high-sociodemographic index countries and high-income North America [
7]. Therefore, further research is needed to identify the risk factors for scabies outbreaks in countries, such as North America and Europe, which have been less studied.
We attempted to integrate the results based on the hospital settings in which the study was conducted. For outpatients, personal characteristics, such as lack of hygiene, emerged as risk factors [
25,
27]. In contrast, inpatients living in communal settings [
21,
24,
26] were vulnerable to scabies infection, and clinical factors such as severity [
26] and walking conditions [
31] tended to be more pronounced compared with outpatients. These results provide information on the factors that should be emphasized in screening for scabies tailored to each outpatient and inpatient setting. In nosocomial scabies, characteristics classified as clinical factors, such as contact [
20] and hospital environment [
28], were highlighted as risk factors. Based on these results, to prevent the spread of scabies within hospitals, wearing protective equipment is necessary to prevent direct contact with patients and establish infection control policies within hospitals. However, only one study reported factors such as severity, walking conditions, and hospital environment. This indicates a lack of studies on the risk factors associated with scabies occurrence and suggests that more research should be conducted.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.