Parasitic diseases caused by intestinal protozoa and helminths are among the most common illnesses and one of the major causes of increased morbidity and mortality among people in developing countries (Speich et al., 2016). It is generally acknowledged that parasitic diseases are the most common among children under the age of five as they are more vulnerable to soil-transmitted helminthic infections than adults. Nutritional disorders caused by the parasites may lead to iron deficiency anemia, malnutrition and they may have a negative impact on growth and cognitive development of a child (Bethony et al., 2006; Pullan et al., 2011). Despite all the medical and pharmaceutical advance as well as progress in sanitary engineering, intestinal parasitic infections remain the most prevalent in the world, especially in developing countries struggling with water scarcity, poor hygiene and lack of adequate health care services. Furthermore, it is difficult to control intestinal parasitoses in these regions due to the high cost of infrastructure improvements and lack of educational projects offered to the population (Speich et al., 2016; Ostan et al., 2007; Mehraj et al., 2008). Water is essential to life, but it is also an important vehicle for pathogen dissemination, and many invasive helminth eggs and larvae, and protozoan cysts are distributed via water in the environment. Protozoa such as
Hatam-Nahavandi et al., 2015). Incorrect landfilling of human and animal feces is also identified as a possible source of contamination of water sources (Smith et al., 2007) and recreational waters such as swimming pools, water parks and lakes (Savioli et al., 2006). Sometimes sewage overflows also contribute to pollution of surface water and farmland, which leads to the possibility of potential human infections. Food contamination can also occur during food processing, directly (through contaminated equipment or washing water) or indirectly (through contaminated irrigation water) (Dawson, 2005).
Cases of intestinal parasitoses in humans, both autochthonous and imported from other endemic regions of the world, are reported annually in Bulgaria. The aim of this study was to perform a retrospective analysis of the intestinal parasitic infections prevalence in the Bulgarian population for the period 2015 – 2017.
The study involved all persons, Bulgarians as well as foreign citizens residing in the country, tested for intestinal protozoa and helminths from January 2015 to December 2017. The patients were tested in the Independent Medical Diagnostic Laboratories (IMDL), Parasitological Laboratories at the Regional Health Inspectorates (RHI) and University Hospitals, and at the National Reference Laboratory for Diagnosis of Parasitic Diseases (NRL) at the National Centre of Infectious and Parasitic Diseases (NCIPD).
Fecal samples were investigated for intestinal protozoans and helminths using various methods such as: microscopic examination of direct wet smear, staining with Lugol’s iodine, enrichment helmintho-ovoscopic methods (sedimentation, flotation, formalin-ether concentration method), helmintho-larvoscopy by the methods of Berman and Harada-Mori, a perianal tape test for detection of
It was used descriptive statistics. The mean, standard deviation and confidence interval of the mean have been calculated in the study.
For the purposes of the present study no informed consent was required from the study participants.
Of this group two nematode infections i.e., ascariasis and trichuriasis have local transmission in Bulgaria and cases are recorded on the territory of the whole country. Table 1 shows the data on the number of persons tested and diagnosed with ascariasis or trichuriasis.
Distribution of the cases of ascariasis and trichuriasis for the period 2015 – 2017.
Year | Number of persons examined for ascariasis | Number positive | Prevalence (%) | Number of persons examined for trichuriasis | Number positive | Prevalence (%) |
---|---|---|---|---|---|---|
637 543 | 805 | 0.13 | 623 288 | 90 | 0.01 | |
499 729 | 678 | 0.14 | 493 063 | 71 | 0.01 | |
576 159 | 706 | 0.12 | 576 159 | 110 | 0.02 | |
1 713 431 | 2 189 | 1 692 510 | 271 | |||
571144 ± 69044 | 729.7 ± 66.73 | 0.13 ± 0.01 | 564170 ± 65935 | 90.33 ± 19.50 | 0.01333 ± 0.005774 | |
399630 | 563.9 | 0.1052 | 400379 | 41.89 | -0.001009 | |
742657 | 895.4 | 0.1548 | 727961 | 138.8 | 0.02768 |
This group includes three intestinal parasitic diseases: enterobiasis, giardiasis and hymenolepiasis. During the study period a large group of individuals (children, adolescents and adults) was screened for community-acquired parasitic diseases; the tests were performed for prophylactic, epidemiological or clinical indications The data are presented in Table 2.
Distribution of the cases of enterobiasis, giardiasis and hymenolepiasis for 2015 – 2017.
Year | Number of persons examined for enterobiasis | Number positive / prevalence (%) | Number of persons examined for giardiasis | Number positive / prevalence (%) | Number of persons examined for hymenolepiasis | Number positive / prevalence (%) |
---|---|---|---|---|---|---|
479149 | 4604 / 0.96 | 481197 | 1245 / 0.26 | 388364 | 126 / 0.03 | |
388971 | 4403 / 1.13 | 471537 | 1367 / 0.29 | 363359 | 474 / 0.13 | |
451466 | 5472 / 1.21 | 438379 | 1156 / 0.26 | 327567 | 120 / 0.04 | |
1319586 | 14479/1.10 | 1391113 | 3768 / 0.27 | 1079290 | 720 / 0.07 | |
439862 ± 46195 | 4826 ± 568.1 | 463704 ± 22458 | 1256 ± 105.9 | 359763 ± 30558 | 240.0 ± 202.7 | |
325107 | 3415 | 407916 | 992.9 | 283854 | -263.5 | |
554617 | 6238 | 519493 | 1519 | 435672 | 743.5 |
A total of 53 individuals were diagnosed with taeniosis caused by beef tapeworm (n = 18 for 2015, n = 19 for 2016 and n = 16 for 2017) during the study period, with the mean annual incidence over the period of 0.25 per 100,000 (0.25 / 100,000 in 2015, 0.26 / 100,000 in 2016 and 0.23 / 100,000 in 2017). Infections with
The data on the prevalence of the two intestinal protozoan infections are presented in Table 3.
Distribution of blastocystosis and cryptosporidiosis for the period 2015 – 2017.
Year | Number of persons examined for blastocystosis | Number positive | Prevalence (%) | Number of persons examined for cryptosporidiosis | Number positive | Prevalence (%) |
---|---|---|---|---|---|---|
345549 | 660 | 0.19 | 352 | 0 | 0.00 | |
358697 | 769 | 0.21 | 479 | 4 | 0.84 | |
328315 | 858 | 0.26 | 231 | 14 | 6.06 | |
1032561 | 2287 | 1062 | 18 | |||
344187 ± 15237 | 762.3 ± 99.17 | 0.22 ± 0.04 | 354 ± 124 | 6 ± 7.21 | 2.3 ± 3.28 | |
306337 | 516.0 | 0.1304 | 45.94 | -11.91 | -5.856 | |
382037 | 1009 | 0.3096 | 662.1 | 23.91 | 10.46 |
Parasitic infections of the gastrointestinal tract have a cosmopolitan distribution. The analysis of our survey data (2015 – 2017) shows that a significant proportion of the country’s population were screened for the soil-transmitted helminth infections with local transmission (ascariasis and trichuriasis). A total of 1 713 431 persons were examined for ascariasis; the mean annual prevalence of the disease was 0.13 %. We found that the absolute number of people infected by
Trichuriasis is one of the most common helminth diseases world-wide (around 800 million infected individuals), with the highest incidence in warm and humid areas (Dori et al., 2011). The highest prevalence rate is recorded in Central Africa, South India and South East Asia (Alum et al., 2010). In Bulgaria, the disease is with local distribution and only a limited number of cases are recorded annually. Over the three-year study period were registered 271 cases of trichuriasis in the country, and the mean annual prevalence was 0.01 %. It should be pointed out that trichuriasis was recorded primarily among persons living in social institutions (e.g. for children deprived of parental care and adults with mental dis-abilities), which is in line with our previous findings (Harizanov et al., 2013; Rainova et al., 2018). As regards the age structure of the infected, the prevalence of trichuriasis was higher in the age group over 20 years, 89.3 % (n = 242), and significantly lower among children and adolescents 10.7 % (n = 29). This can be explained by the characteristics of patients staying in mental health facilities and the difficulties in maintaining good hygiene in such institutions, as well as the fact that the number of children’s homes or similar institutions has significantly decreased in recent years. However, it needs to be stressed that some of the social care establishments are active foci of soil transmitted helminth infections and greater efforts by the public health authorities are needed with regard to control measures related to diagnosis, timely treatment, environmental remediation. The spread of soil transmitted helminth infections, and ascariasis and trichuriasis in particular, is directly proportional to the population density in the region, education level, health protection measures for wastewater management, use of fertilizers, personal hygiene, available health care and socio-economic country status (Das, 2014). In this regard, the WHO Regional Office for Europe developed a strategy entitled “Framework Program for the Control and Prevention of Soil Transmitted Helminth Infections in the WHO European Region, 2016 – 2020” aiming at reducing the incidence of these parasitic diseases to an extent that they will no longer pose a problem for the public healthcare (WHO, 2016).
The community acquired parasitic diseases are of particular health importance in Bulgaria, because they most often affect children in organized facilities. Of these, enterobiasis continue to be the most common community acquired parasitic infection as its prevalence remains high. During the period of our study 14,479 cases of enterobiasis were recorded, of which 7,922 (54.7 %) in children attending organized children’s institutions. In this respect our data аrе similar to the data in available literature. Enterobiasis is a common disease occurring globally, including in countries in temperate zones. It most often affects children. The prevalence among the pediatric populations in different regions of the world varies from 4 to 28 % (Dori et al., 2011). The average prevalence among the subjects within the study period was 1.10 %, while the average prevalence in the general pediatric population in the country was found to be 1.59 %; however, it should be taken into consideration that the study group involved pre-school children attending child care institutions where annual parasitological testing is obligatory. The second most common of the community acquired parasitic diseases in our study was giardiasis with 3,768 reported cases.
Hymenolepiasis is a zoonotic disease caused by the
As regards taeniasis, cases caused by beef tapeworm have been sporadically recorded in the country, they are mainly seen in areas with livestock production. The causes of the disease are mainly a lack of awareness of the disease, slaughtering farm animals at home without the proper veterinary supervision. No cases of pork tapeworm infection were recorded during the study period and we were unable to access the official data on the number of cases of cysticercosis in swine.
Protozoa infections of the gastrointestinal tract are recorded worldwide. The most common outbreaks caused by protozoa are generally associated with
Cases of
The extent of the damage caused by intestinal parasites depends on: (a) the type of the parasite; (b) the parasitic load and clinical course of the disease; (c) the nature of the interactions between the parasitic species and the presence of concomitant infections; (d) the nutritional and immunological status of the population; and e) socio-economic factors. All of the above factors may additionally be affected by seasonal and climatic conditions. It is usually difficult to measure the suffering caused by infectious diseases, and in the case of intestinal parasitic infections, this is even more difficult, as many of the cases are asymptomatic and therefore remain undetected (WHO, 1987). In Europe, intestinal protozoan and helminth infections predominantly spread in Southeast Europe and Turkey where the living conditions are poorer and the socioeconomic status is lower (Hotez & Gurwith, 2011). Over 165 million people (more than 20 % of the European population) live below the poverty line and about 2 % of the European population lives in absolute poverty. This has a significant impact on the incidence and prevalence of parasitic diseases (Stuckler et al., 2009). Some population groups require particular attention because they are more vulnerable and susceptible to infections and parasitic diseases. One of these is the Roma population, which comprises between 7 and 9 million people living in Central and Eastern Europe. The largest numbers of the Roma people in Europe reside in Romania, Bulgaria, North Macedonia and Slovakia, where they account for over 8 % of the population (Rechel et al., 2009). Of these, 70 % to 80 %, mainly in Bulgaria and Romania, live in poverty, have poor housing conditions, poor hygiene habits and often suffer from malnutrition. Their susceptibility to intestinal parasitic diseases, bacterial and viral infections is very high (Rechel et al., 2009). Other population risk groups in Europe include immigrants, especially migrants from Africa, who often suffer from the so-called “neglected tropical diseases”, as well as the children deprived of parental care living in social institutions (Norman et al., 2010).
In Bulgaria, the existing regulations for surveillance and control of parasitic diseases provide for relatively high detection rates of parasitic infections. Many of the infected individuals are asymptomatic hosts of parasites. High detection rates can be attributed to annual prophylactic parasitological screening of children (attending children’s establishments/ institutions), adults (working in the food industry, retail outlets, catering establishments, etc.) and migrants. This allows timely treatment of the infected persons who might potentially become the source of infection for other individuals.
Authors declare no conflict of interest.