Prevalence and age distribution of enterobiasis in North-Eastern Bulgaria

Enterobiasis (pinworm infection) is caused by the small intestinal nematode E. vermicularis. It has a worldwide distribution and is probably the most common helminth infection with prevalence rates reaching up to 30 – 50 % (Burkhart & Burkhart, 2005; Wendt et al., 2019). Children older than two years, especially those visiting childcare establishments and primary schools are the most affected group (Remm, 2006; Wendt et al., 2019). Adults contract enterobiasis usually from infected children by domestic or occupational exposure. Consequently, the prevalence in adults is low and thus seldom researched (Burkhart & Burkhart, 2005).

Hands contamination with the parasite’s eggs plays the most critical role for infection and autoinfection. It is the primary factor for the circulation of the disease in the population (Herrström et al., 2001; Wendt et al., 2019). The facilitated person-to-person transmission exempts enterobiasis from the principle that intestinal parasites are uncommon in developed regions. Infection can be observed in children of all strata regardless of socioeconomic level, culture or race (Boas et al., 2012; Wendt et al., 2019).

Despite its wide dissemination on the European continent, enterobiasis is rarely a subject of in-depth epidemiological inquiries. Due to its mild or asymptomatic manifestation, it is sometimes considered more as a nuisance than an actual health problem. The most recent data on prevalence rates of the infection in Europe vary depending on the scope of the research and the investigated population. The reported prevalence rates are 37 % in allergic and 23 % non-allergic children in Sweden (Herrström et al., 2001), 32.4 % in Polish children and adults (Heciak, 2006), 24.4 % in Estonian nurseries (Remm, 2006), 22 % in hospitalised children in Denmark (Lacroix & Sørensen, 2000), 18.2 % in children in Norway (Boas et al., 2012), 17.4 % in the population of Berlin area, Germany (Friesen et al., 2019), 7.73 % in children of central Greece (Patsantara et al., 2016), and 3.59 % in pre-school and school-aged children in the eastern Slovakia (Dudlová et al., 2018).

The aim of the current study was to establish the enterobiasis prevalence and its age distribution in Varna district population, North-eastern (NE) Bulgaria within 2009 – 2018 period and compare the results with the official countrywide data available for the same period.

The study was designed, conducted and reported in agreement with the Declaration of Helsinki (rev. 2013). Each patient or their legal representative gave informed consent for the laboratory testing as it is mandatory for all tests performed on an outpatient basis in clinical laboratories in Bulgaria. All data regarding the testing and detection of E. vermicularis performed between January 2009 and December 2018 were extracted retrospectively from the laboratory information system. Only study-relevant patient information (age, sex, residence, year of sample reception) was collected for the purpose of this research. The data was presented in the form of frequency tables containing combinations of factor levels and the corresponding number of positive and negative results. This data format makes it impossible to reconstruct the initial source completely and to identify the patients. Given the retrospective nature of the study and the preserved anonymity, no further ethical approval was required and requested.

With an average prevalence of 0.91 %, E. vermicularis was the most common intestinal parasite in Varna District for the last decade when compared with all other intestinal helminths and protozoa during an overlapping period (2007 – 2016) (Stoyanova, 2019). The rates in the NE region are equivalent to the average prevalence of enterobiasis in Bulgaria (0.90 %; n=4 4115/4 907 760) as reported by NCIPD (Harizanov et al., 2020; Rainova et al., 2018, 2018). It is important to note that the real prevalence might be even higher. The Bulgarian healthcare regulations do not require the adhesive tape tests to be carried out by a specialist personal, and this might increase the rate of false-negative results. Our results about the sex distribution of enterobiasis showed higher prevalence in males than females. Although the overall odds ratio suggested elevated risk in males (OR=1.47), further analysis demonstrated that sex differences are insignificant in adults (OR=1.40) as well as in children (OR=0.98). Thus, similarly with other researchers (Boas et al., 2012; Herrström et al., 2001), we conclude that the observed small discrepancies are not part of a regular pattern but arise from random variance and inhomogeneities within the tested populations.

We have found an alarming tendency for rising of enterobiasis after 2012 (Fig. 1). The average prevalence in Varna District tripled in the decade under observation and in 2018 (1.45 %) exceeded levels detected in the region at the end of the last century (1.11 % in 1989 and 1.20 % in 1990) (Ruseva & Popova, 1992). A similar pattern was observed throughout the whole country, as reported by NCIPD (Fig. 1).

The statistical models of the annual prevalence rates in children and adults (Fig. 2) clearly demonstrated that the increase in enterobiasis is specific and solely due to the elevated infection rates in childhood. The annual differences in prevalence were typical for the entire 10-year interval but did rise sharply in the second half of the decade.

Several factors may have contributed to this tendency. Regionally and countrywide, there is continuous overcrowding of child care facilities accompanied by a deficit of qualified and skilled personnel (Stoyanova, 2019; Stoyanova & Cvetkova, 2018). Additionally, during various periods in 2014, 2015 and 2016, anthelminthic drugs were absent from the pharmacy network in Bulgaria. This fluctuation in the availability of the medication and the complete absence of an appropriate administration form for younger children (suspension or syrup) lead to a delay of etiological therapy and prolonged the period in which the infected persons were epidemiologically active sources of infection (Stoyanova, 2019; Stoyanova et al., 2017).

Since the last wide-scale examination in Varna District, the levels of enterobiasis in children dropped approximately ten times from 12.4 % in 1975 – 1977 (Kovchazov, 1979) to 1.49 %. The same did not apply for the adult population, where the average prevalence diminished only by half – from 0.50 % (1975 – 1977) to 0.25 % (2009 – 2018). The prevalence levels for the adults have not changed substantially in the last 40 years as concurred by the annual model (Fig. 2). This finding indicates that there is a stable background level of enterobiasis in the adult population, and it can be used as a base level for comparison with other age groups.

The enterobiasis in adults is rarely researched in other European countries. One epidemiological study in Poland reported 2.59 % prevalence in children and 0.43 % in adults (Kasprzak et al., 2017). Another older survey in Lithuania revealed rates of 18.4 % and 1.3 % in children and adults, respectively (Mazhilene, 1991).

Fig. 3 demonstrates the growing rate of enterobiasis in children by age which is facilitated by increased exposure. In the older adolescent (>14 years), the level dropped and reached the background rates observed in the adult population. Despite the significantly higher prevalence, similar distributions are reported in different European countries. Investigation in healthy Norwegian children shows 2 – 3 years old kids as least affected (7.3 %), what is followed by 4 – 5 years-old group (14.1 %), and the highest prevalence (34.4 %) was observed in 5 – 14 years old children (Boas et al., 2012). Parallel age dependency was observed in Estonia where the prevalence was 16.2 % in 1 – 3 years-old kids, 16.0 % in 4-year-olds, 29.9 % in 5 and 6-year-olds and 42.0 % in 7 – 8 years old group (Remm, 2006).

The attendance in children’s collectives is a significant risk factor for the propagation of enterobiasis in Bulgaria (Genov et al., 1975; Rainova et al., 2018; Ruseva & Popova, 1992; Stoyanova, 2019). The age-dependent partitioning of the prevalence that was apparent in Fig. 3 also corresponded with the main types of facilities for child care and education. Infants attending nurseries (0 – 2-years old) are less exposed and less affected. Their primary contact with the disease is probably via infected family member – parent or older sibling, and thus the average level of the infection (0.36 %) is similar and insignificantly higher than in adults.

The disease rate increased substantially to 1.58 % in the age group attending kindergartens and preschool (2 – 6-year-olds) as the odds of contracting the disease here are about six times higher than in adults (OR=6.32).

These results also showed the encouraging trend that over the past 40 years, the enterobiasis prevalence in the childcare facilities in Varna District has decreased about 3 times in both age groups – from 1.1 % (1971 – 1975) (Kovchazov, 1979) to 0.36 % (2009 – 2018) in the nurseries and from 3.6 % to 1.58 % in the kindergartens.

Almost the same rate in reduction of enterobiasis was observed in the children in school age. It decreased from 35.6 % (1971 – 1975) (Kovchazov, 1979) to 9.57 % in our current study. Nevertheless, students remain the most affected by enterobiasis. The significant differences from younger age-groups can be attributed to the absence of any preventive measures that should focus on the children or on their close environment (schools). In contrast, there is an effective system for the prevention in nurseries, kindergartens and preschools. The higher prevalence detected at school-age must be interpreted cautiously. This group is not subjected to preventative screening and is comprised of a population tested for E. vermicularis either on clinical (manifested symptoms) or on epidemiological (contact with an infected) ground. Therefore, the observed rates are biased upwards, and the actual prevalence is probably lower. Still, there is a six-fold increase in odds as compared with kindergarten age group (OR=6.57; CI:4.59-9.41) and 41-fold in comparison with adults. This finding requires detailed proactive surveillance in this group and the implementation of focused preventive measures to limit disease circulation in schools. Similarly to our findings, higher rates of enterobiasis in older children were found in Denmark (29 % in 5 – 12 years old kids) (Lacroix & Sørensen, 2000), and in children from neighbouring Turkey where 10.1 % of the pupils in the primary schools in South-Western (Aksoy et al., 2007) and 18.2 % of the 7 – 14 year-old students in Western region (Okyay et al., 2004) were affected.

This research identifies an alarming upward trend in the annual enterobiasis prevalence in children within NE Bulgaria. The infection is most frequent in preadolescent and early adolescent age where targeted preventive measures should be introduced and enforced.

Our results about the prevalence of enterobiasis in Varna District and its rates in children and adults reflected the overall epidemic process of this helminthiasis in Bulgaria. The levels of E. vermicularis infection (regionally and countrywide) were significantly lower than the prevalence data reported from most of the European countries. Two factors were responsible for the observed discrepancy. Our pool of subjects included a vast number of children and adults, tested annually on prophylactic indications which rarely are an object of epidemiological studies available. More importantly, the Bulgarian proactive surveillance system for intestinal parasites serves as an effective approach to screen for such mild or generally asymptomatic infections. Consequently, the majority of the ‘hidden’ disease carriers are revealed, and subsequently treated and eradicated as potential sources of further transmission.