An increasing scabies incidence in Croatia: A call for coordinated action among dermatologists, physicians and epidemiologists

This is mixed ecological study that makes us of exploratory studies of both spatial and temporal patterns.

There are two types of units of observation included in this study. In an exploratory study of temporal patterns in Croatia a single year is the unit of observation, while in the exploratory study of temporal patterns of scabies occurrence in Zagreb in the present study the unit of observation is a month. In our exploratory study of spatial patterns, the unit of observation is a county and there are 21 units included in the research.

We analysed data from communicable disease notifications for scabies cases in Croatia for the period between 2007 and 2017, with more detailed analysis by the counties, age, facility and month in the period from 2014 to 2017. No identifiable personal were used for this study, and the dataset used is not openly available.

Reporting communicable diseases is mandatory in Croatia and regulated by the Health Care Act, the Act on the Protection of the Population against Communicable Diseases, the list of communicable diseases the control and prevention of which is of interest to Croatia and the ordinance on the method of reporting communicable diseases (16, 17, 18). Licensed health care professionals and health care institutions are required to report selected communicable diseases through the standardized questionnaire to the epidemiology service (part of the Croatian network of public health institutes), which is finally received and stored at the Croatian Institute of Public Health. The routinely collected health data used in this study were sourced from the state-owned Croatian Institute of Public Health database. This nationally representative database is available only on request. Therefore, in order to address our research objectives, our multidisciplinary team (consisting of epidemiologists, public health specialists and dermatovenereologists) utilized different mechanisms for sourcing and analysis of the data.

A scabies case is defined as an individual whose skin scrapings reveal mites, mite eggs or mite faeces, or as an individual with typical clinical signs epidemiologically linked to laboratory-confirmed cases. The average annual incidence rate per 100,000 inhabitants in Croatia was calculated by county using data from The Census of Population, Households and Dwellings 2011 from the Croatian Bureau of Statistics (19). Age specific annual incidences, along with seasonal trends, were both calculated on the national level. We also analysed outbreak reports by number of recognized and reported outbreaks, duration and facilities involved. In addition, we analysed percentile changes in relative (per capita) number of tourists, immigrants and patients with scabies by counties. The change over time is represented by standardized regression coefficient (beta) – ranging from -1 (complete negative linear association) over 0 (no association) to 1 (complete positive linear association).

For the analyses, we used SPSS FOR WINDOWS ver. 20.0 (SPSS, Chicago, IL, USA). Descriptive statistics were used to process data, calculate trends and create tables and graphs. Differences between the counties in the number of patients with scabies, relative to county size (The Census of Population, Households and Dwellings 2011 from the Croatian Bureau of Statistics) (19) were studied using Chi-square test, while Kendall’s tau (τ) correlation coefficient was used to calculate the correlations between the time changes in relative number of tourists, immigrants and patients with scabies by Croatian counties. Kendall’s tau was used due to small sample size (n=21) and non-normality of the parameter distributions.

Levels of significance were set to p<0.05 or p<0.01.

Our results show an increasing trend in scabies incidence across Croatia between 2007 and 2017. The incidence rate increased 6-fold during that 11-year period, with the steepest increase in the last four years (2014-2017) (Figure 1).

Figure 1

Within the 2014-2017 period, the highest average incidences in Croatia were recorded among children younger than 4 years old, preschool and elementary school children aged 5-9 years and adolescents of ages 1519 (Table 1). From 2014 to 2017, we observed a total of 106 outbreaks of scabies within families and within adult foster care homes, nursing homes and other facilities throughout Croatia. Health care professionals and assistants were among those infected.

In the City of Zagreb, the crude incidence rate increased 3-fold between 2014 and 2017 (Figure 2, Table 2), compared with the same period in Croatia. The majority of cases were recorded during winter and autumn.

Figure 2

Between 2014-2017, large discrepancies were observed at the county level, with some counties continuously having notably higher incidence rates (Sisak-Moslavina, Vukovar-Srijem, Osijek-Baranja and Međimurje County) or lower rates (Varaždin and Bjelovar-Bilogora County) than the national rate during the same period. In 2017, 2,224 cases were reported in Croatia, corresponding to a crude incidence rate of 51.90/100,000. Notably, four counties (Sisak-Moslavina, Vukovar-Srijem, Osijek-Baranja and Međimurje County) had almost twice the national incidence rate for 2017 (Table 2, Figure 3).

Figure 3

On average, around 40% of outbreaks in the observed period (2014-2017) lasted for several months due to late recognition and diagnosis, particularly among families. Regarding outbreaks of scabies within institutions, more than 80% were in institutions for adults and nearly half of them were recognized and resolved within one month. In Zagreb during the same period we detected 13 outbreaks, two-quarters within families. During autumn 2016, the first outbreak of scabies in an asylum centre (as part of the migrant crisis) was epidemiologically investigated and resolved within three months.

In each of the observed years (2014-2017) there was a large difference in scabies incidence among counties. According this statistical analysis of available data, the scabies incidence was not evenly distributed among counties, and this irregular distribution was statistically significant. Thus, some counties significantly deviated from the expected epidemiological data. In the 2014 χ2=416.95, df=20, p<0.01; in 2015 χ2=679.44, df=20, p<0.01, in 2016 χ2=919.71, df=20, p<0.01, and in 2017 χ2=556.14, df=20, p<0.01. The largest discrepancy between the observed and theoretically expected cases of scabies in 2014 were found in Karlovac County (fo=104, ft=46.4), in 2015 in Vukovar-Srijem County (fo=167, ft=59), in 2016 in Varaždin County (fo=13, ft=89.1) and in 2017 in Vukovar-Srijem County (fo=177, ft=93.2).

Figure 4 represents the percentile change in relative (per capita) number of tourists, immigrants and patients with scabies in Croatia. An almost linear trend of increase can be observed for the number of tourists and immigrants. On the other hand, for the number of patients with scabies, there is a small decrease from 2014 to 2015, then sharp increase from 2015 to 2016, followed by relative stability from 2016 to 2017.

Figure 4

The results in Table 3 show that the change in the relative number of tourists over observed time period is positive in all counties. In most of the counties the trend is almost linear (close to 1). The time trend of the relative number of immigrants by counties is also positive in most of the Croatian counties. The exceptions are Šibenik-Knin County, with no change (β=-.033), and Dubrovnik-Neretva County with a small and insubstantial change (β=-.181). However, the trend of change in the relative number of patients with scabies is not uniform, and varies greatly across the counties – from an evident increase (i.e. Osijek-Baranja County - β=.990) to relative stability (i.e. Međimurje County - β=-.003) to a substantial decrease (i.e. Primorje-Gorski Kotar County - β=-.704).

The correlations between trends of the relative number tourists and relative number of patients with scabies was τ=-.052 (p=.878), and between those of the relative number of immigrants and relative number of patients with scabies was τ=.153 (p=.345). These insignificant (p>.05) correlations indicate that time trends of relative change in number of tourists or immigrants by counties are unrelated to the time trends of relative change in number of patients with scabies in the respective counties.

According to our research and the obtained data, our initial suspicion on the increasing trend in scabies incidence in Croatia was confirmed on the national level in this study. Thus, in the period between 2007 and 2017, a 6-fold increase of the scabies incidence rate was found, and the steepest increase was in the last four 4 years of the analysed period. Most of the scabies cases were among children and adolescents. These results indicate the need to raise awareness among health care providers, especially those working with children and adolescents with itches, with the aim not to misdiagnose scabies.

Concerning the possible associations among scabies incidence, tourists and immigrants, we confirmed an increasing number of tourists and immigrants in the period 2014-2017. However, time trends of the relative change in number of tourists and immigrants by counties were not related to the relative change of scabies infestations. Although statistical significance was not present, the highest scabies incidence rates were recorded in Međimurje and Vukovar-Srijem counties, which indicates moderate influence of the proximity of the border and influence of movements of people on scabies outbreaks.

Concerning seasonal variations of scabies, our data for the City of Zagreb (monitored over a period of four years, 2014-2017) showed that infestation counts multiplied in winter and autumn months, thus confirming an influence of seasonal trends on scabies outbreaks. Therefore, our results may be a basis for the planning of further preventive measures.

According to the data in the literature, worldwide, scabies affects an estimated 100 million people across all continents and countries. Regardless, scabies is not a priority on the global health agenda, even though interest in the disease is increasing (11). However, outbreaks and management vary from country to country, and thus priority and management do as well (22).

Several trends and related factors have been found to be important for scabies outbreaks. Thus, a strong connection among scabies, migration and travel has been reported (11, 12, 15, 23). Since scabies moves with people, mass migration due to political and socioeconomic factors can promote its spread, as seen recently with the influx of asylum seekers arriving in Western Europe from high-prevalence countries (11, 12). Since scabies is transmitted by close person-to-person contact, it is logical that outbreaks have been reported in reception centres for asylum seekers across Europe (11). Previous studies claim that immigrants are at a higher risk of acquiring common communicable diseases compared to the native Western European population (23). Although most refugees in Croatia are only in transit, refugee and migration flows can still have an impact on the occurrence of scabies in the country. A recent study suggested that scabies cases rose at the time when refugees and migrants were intensively coming from the Middle East to Western Europe via the Southeastern European route (Turkey-Greece-Serbia-Croatia-Slovenia-Austria) (15). Data presented in this study supports this observation, since an approximately 6-fold increase in scabies incidence was confirmed in Croatia between 2007-2017. According to our results, local geography could have a great influence on this, as indicated by the increased scabies incidence in areas close to the borders with Serbia and Bosnia and Herzegovina, and those along refugee migration routes. Late recognition and the delay of proper treatment, along with an increase in regular and irregular migration from neighbouring countries with high incidence rates of scabies (Bosnia and Hercegovina, Kosovo, Serbia), likely caused this upward trend in scabies cases in Croatia during this time.

According to data from Germany, the prevalence of scabies is higher among refugees than in the general population; however, the risk of outbreaks themselves is not high (24). Recent analysis of the health status and disease burden of unaccompanied asylum-seeking adolescents in Germany (cross-sectional pilot study) showed the highest prevalence of infestation in sub-Saharan Africans (86.7%), including the highest prevalence of parasites in general (46.7%), with a higher disease burden among females (25). Similar results were obtained by Kortas et al., who found a total of 47.7% of the subjects with scabies infestations originated from Afghanistan and 25.0% from Eritrea (26). Consequently, there is a need for thorough medical and psychological screenings after the arrival of such individuals in order to reduce the individual disease burden and risk of infestation for others. It is also necessary to lower barriers to health care access for unaccompanied asylum-seeking minors and allow for need-specific health care and prevention (27).

Significantly, another possible cause for the increase could be Croatia’s 2013 admission into the European Union and the consequent increase in travel to the country (23). An important, related factor could be the increase in Croatia’s tourism rate over the last few years, which might indicate the influence of travel and tourism on the scabies rate. Our results indicate linear increases in the number of tourists, immigrants and scabies infestations on the national level for the analysed period, although with no statistically significant association. According to a previous study of skin disorders among travellers returning from tropical and non-tropical countries, more than 20% of all such disorders were caused by arthropods and about 50% by infectious pathogens (27). As such, pre-travel consultations should include specific prophylaxis and consider the most common risk factors for each destination (28).

Moreover, close contact among young people during travel, concerts and festivals can influence scabies rates. Large summer concerts and festivals have become popular in Croatia in recent years, and it is possible that casual sex and poor hygiene in these crowded conditions contribute to incidence rates (29). This corresponds to our results, as they have confirmed that young people predominated among scabies patients. More public attention should thus be directed to the prevention of scabies among youth, especially due to their lifestyles. Appropriate hygiene in overcrowded places, such as mass gathering events, is also important. According to a previous retrospective analysis (data from 145 countries) of the infection burden from inadequate water, sanitation and hygiene in low- and middle-income settings, there is a need for better risk reduction, including the provision of reliable piped water, treatment of community sewage and awareness of hand hygiene (30).

Seasonal variations should be also mentioned, since a connection between scabies occurrence and weather conditions and the seasons was observed (31). According to previously published data, scabies infestations are especially common in winter (31). Thus, Liu et al. monitored the influence of temperature on scabies incidence and observed that, overall, the incidence of scabies was negatively correlated with temperature but positively correlated with humidity (30). Our results support the seasonal character of scabies, as the majority of cases were recorded during winter, but also in autumn (Zagreb). It is possible that increased scabies infestation in winter is a result of closer contact between people in indoor environments. It should also be considered that scabies cases are often reported weeks or even months after the patient has contracted it. For example, a case is only reported in winter months when the patient first sees their physician, when the symptoms are troublesome enough, but the infestation could actually have started in the summer or autumn, coinciding with the patient’s travel during vacation.

Considering the data in the literature, it is also important to mention an increased risk for outbreaks at nursing homes and extended-care facilities since elderly persons tend to develop crusted scabies due to disease- or medication-related immunosuppression (24, 32). According to a previous smaller study conducted in the City of Zagreb, 10% of scabies cases were found in medical health personnel, predominantly in those working in nursing homes and psychiatric wards (33). In our study, we found a prominent number of scabies outbreaks within families, adult foster care homes, nursing homes and other facilities throughout Croatia. Our results indicate a need for increased caution and preventive measures for these populations and settings. Since health care professionals and assistants were among those infected, focus should be also on appropriate hygienic measures while working with patients.

Unfortunately, although scabies is a major public health problem and causes a significant disease burden worldwide, there are no agreed-upon international diagnostic guidelines (34). Thus, we can mention that due to the frequent setting of the diagnosis based only on the clinical picture, it is difficult to know the real number of scabies cases. Thompson et al. found that only 56% of clinical trials in medical databases specified which clinical findings were used for diagnosis (predominantly rash, rash distribution, pruritus and mite burrows) (35). According to their findings, parasitological testing was used in 63% of trials, more frequently in clinic-based than in field studies, and nearly one-quarter of trials (24%) did not perform diagnostic methods at all, which can lead to the further spread of scabies. However, in field conditions, the psychological and physical profiles of scabies patients may help in the early recognition of scabies, which is very useful, especially at peripheral care centres (36).

This retrospective, observational study, based on the official data presents the first national research regarding scabies incidence in Croatia, with findings based on the obligatory report data collected from all health care institutions in Croatia (for the years between 2007 and 2017). To the best of our knowledge, this is the first recent epidemiologic analysis on this topic, not only in Croatia but within the wider geographic region as well.

However, the limitation of this study is the lack of detailed data regarding the trend of scabies incidence throughout the years, since health care providers who send the report about communicable disease do not always answer all the questions in the report form. Therefore, we provided a more detailed analysis for the City of Zagreb (the capital of Croatia), since it accounts for one-quarter of whole Croatian population and has the highest number of hospitals and medical professionals at the national level. This study also found a possible impact of changes in the Croatian population, for example due to migration. In addition, we could only assume that health care providers reported all the scabies cases for the analysed period, although this might not have happened.

The importance of this study is to emphasize the need for the implementation of existing standardized guidelines with the aim early recognition and timely reporting of scabies. Furthermore, despite a universal health care system that provides mandatory health insurance for all residents, there is some inequality in health status in Croatia, similar to as in neighbouring countries such as Slovenia (37).

Late recognition of scabies by physicians also presents a problem, and is likely linked to the country’s previously low rate – some medical doctors had not even seen scabies cases before, so did not think to suspect this infestation. It should also be remembered that some infected persons can have false negative results, leading to problems in practice when patients are treated ineffectively (38). When initial cases of scabies go undetected, these infected persons are then not able to prevent the spread of the disease in their immediate environments. Furthermore, there are many examples of non-compliance with treatment in practice. It is thus necessary to train general practitioners and medical staff on the early recognition, proper and timely diagnostics and notification of first cases. Special attention should be directed to the age groups with increased occurrence of scabies, such as children and adolescents. In addition, knowledge of basic hygienic measures is necessary from early childhood, and should be provided by kindergarten teachers (39), parents and other members of society. The epidemiology service has an important role in identifying contacts and applying preventive measures, stressing the necessity of conducting therapy and scabies management. Likewise, epidemiologists can do this only if they receive timely notification of the first sporadic case or early notification of an outbreak. Therefore, coordinated efforts between different sectors and collaboration among a range of health care providers (dermatologists, physicians and epidemiologists) is crucial (40).

This study opens a new perspective on the transmission dynamic for this important but neglected communicable disease. Further research should be focused on the relationship between scabies incidence and other factors, such as tourism, both in Croatia and elsewhere. More attention should be directed to the research of scabies incidence in those countries with an increased number of movements, especially those with a rapidly growing annual number of tourists and migrants. In addition, wider epidemiological studies should be conducted internationally in order to compare trends among countries and regions. More research on scabies in clinical practice is recommended, with the focus on other possible related factors on scabies outbreaks and misdiagnosing of this disease.