Enterobiasis (pinworm infection) is caused by the small intestinal nematode
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.
Varna District is one of the largest administrative areas in the Republic of Bulgaria. It is located in the North-Eastern region on the Black Sea coast. The administrative centre is Varna-city, and with a population of 336 505 for 2018, it is the third-largest town in Bulgaria (NSI, 2019).
Bulgarian healthcare legislation regulates the monitoring and prevention of local parasitic diseases. Testing for intestinal parasites, including
Once yearly in children at age two to seven;
During the enrollment and after a prolonged leave of absence in nurseries (children 0 – 3 years), in kindergartens and preschools (children 3 to 7 years);
In adults engaged in professions with an impact on public health.
This retrospective study was conducted in one of the largest Specialized Medical Diagnostic Laboratories in Varna, Bulgaria, where the Parasitology department carries out more than 10,000 diagnostic tests for the detection of human parasites annually.
The investigation encompassed 71 308 patients examined for
Of all 71 308 samples, 37 886 (53.1 %) belonged to children (<18 years of age), and 33 422 (46.9 %) to adults. Male to female ratio was 39.2 % (27 916) to 60.8 % (43 392).
Patient’s data were grouped by age in 2 categories – adults and children. The children’s group was further stratified according to age and child care facilities attendance:
Group 1: adults – all patients at the age of 18 years and older;
Group 2: infants attending nurseries – at age 1 – 3 years;
Group 3: preschool children between 3 and 6 years, attending kindergartens and mandatory (at five years) preschool education; Group 4: school attending children and adolescents at age 7 – 17 years.
The data were processed and analysed with the R language and environment for statistical computing (R Core Team, 2018; Devleesschauwer et al., 2015). All observations are reported within the 99.9 % confidence interval (CI) calculated by the Clopper-Pearson’s exact method for binomial proportions. Groups were compared using Pearson’s χ2-test (in 2-by-2 analyses) or likelihood ratio χ2-test (in binomial logit models). The size of the observed differences is represented by odds ratios (OR). Each OR is accompanied by its 99.9 % asymptotic CI and the value of the exact (in 2by2 analyses) or asymptotic (in binomial logit model) probability (p-value) for the OR being equal to 1.
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
From the total number of 71 308 individuals, examined with Graham’s adhesive test, eggs and/or adult forms of
The overall prevalence of enterobiasis for the period 2009 – 2018 was 0.91 % (CI:0.80 – 1.04). In children enterobiasis was significantly more prevalent – 1.49 % (CI:1.30-1.71), than in adults – 0.25 % (CI:0.17-0.36), with OR=5.95 (CI:4.05-8.73; p<2.2*10-16).
Table 1 demonstrates the distribution of enterobiasis by sex and age. The disease was more prevalent in males – 1.13 % (CI:0.94-1.36) than in females – 0.77 % (CI:0.64-0.92). The difference between the sexes, however, becomes negligible when the prevalence was analysed in children and adults separately.
Enterobiasis prevalence and distribution by age and sex, Varna District, NE Bulgaria, 2009 – 2018
Age | Sex | Positive | Negative | Prevalence % (CI) | OR (CI) | p |
---|---|---|---|---|---|---|
Children | Female | 277 | 18 057 | 1.51 (1.23 – 1.83) | 1 | – |
Children | Male | 289 | 19 263 | 1.48 (1.21 – 1.78) | 0.98 OR male vs female; | 0.80 |
OR children vs adults | ||||||
Adults | Female | 58 | 25 000 | 0.23 (0.14 – 0.35) | 1 | – |
Adults | Male | 27 | 8 337 | 0.32 (0.16 – 0.58) | 1,40 OR male vs female; | 0.17 |
OR male vs female; |
In the investigated period, we observed a steady, substantial increase in absolute numbers of positive samples through the years – n=10 in 2009 to n=140 in 2018. The total increment corresponded with the growing trend in the overall yearly prevalence. Fig. 1 compares the results in Varna District with the annual prevalence rate of enterobiasis in Bulgaria as reported by the National Centre of Infectious and Parasitic Diseases (NCIPD) (Harizanov et al., 2020; Rainova et al., 2019, 2018).
Initially, the prevalence of the disease followed a relatively flat trend. Starting from 2012, however, a steady increase was evident in both datasets. For the additional investigation, we compared the average rates for the periods – 2009 – 2012 and 2013 – 2018. The total prevalence before 2012 was 0.49 % (CI:0.34-0.69) whereas after 2012 it rised to 1.06 % (CI:0.92-1.21). This observation corresponded to an approximately two-fold increase in the odds of detecting the parasite in the studied population (OR=2.15; CI:1.72-2.69; χ2=47.55; p=3.3*10-13).
Since there is a significant difference in the rates between children and adults, where the age has the potential to play a major confounding role, we stratified the analysis further. We fitted the data for
Fig. 2 shows the model’s predictions and the observed annual point prevalence. The model was significantly better at explaining the observed data than the hypothetical model of random variance (χ2=513.24; p<2.2x10-16) and the model without interaction (χ2=42.3; p=7.85x10-11). The rates of
Age distribution of enterobiasis is demonstrated on Fig. 3. The lowest levels were recorded in children younger than 24 months (0.11 %; CI:0.01-0.50; n=3/2 794) with an subsequent increase (0.45 %; CI:0.24-0.75; n=36/8 000) at age of 24 – 36 months. The prevalence continued to grow throughout the preschool age until it peeked in group of 6-year old children (2.34 %; CI:1.63-3.25; n=92/3 925). At school age, we observed a sudden jump in the prevalence rates which reached the highest values in 9- (12.96 %; CI:5.81-23.64; n=21/162) and 10-year old (14.73 %; CI:6.32-27.34; n=19/129) children.
To reduce the bias introduced through the unbalanced number of test subjects, we stratified the children in the groups above and compared the average prevalence in each group with the adult population (Fig. 4). The prevalence in 0 – 2-years old kids was the lowest (0.36 %; CI:0.20-0.59) and comparable with the rate found in the adults (OR=1.42; CI:0.73-2.64; p=0.07). In children at kindergarten and preschool age enterobiasis affected 1.58 % (CI:1.34-1.86) of the population (OR=6.32; CI:4.33-9.53; p=2.2x10-16) while in 7 – 18 years old children reached its peak at 9.57 % (CI:7.01-12.63) with OR=41.49; CI:25.78-67.54; p=2.2x10-16).
With an average prevalence of 0.91 %,
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
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