- Email: [email protected]
Occurrence of the most common helminth infections among children in the Eastern Slovak Republic
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
Available online at www.sciencedirect.com
Public Health journal homepage: www.elsevier.com/puhe
Original Research
Occurrence of the most common helminth infections among children in the Eastern Slovak Republic a a, Ingrid Papajova a,*, Jindrich Soltys b Jana Pipikova , Ingrid Schusterova
Institute of Parasitology, Slovak Academy of Sciences, Kosice, Slovak Republic a rik University, Faculty of Medicine, Kosice, Department of Paediatrics and Adolescent Medicine, Pavol Jozef Saf Slovak Republic a
b
article info
abstract
Article history:
Objectives: Ascariasis, trichuriasis and hymenolepiasis occur primarily within poor com-
Received 19 December 2016 Received in revised form
munities with low hygiene standards. This study examined the occurrence of intestinal ice and Pre helminth infections among children living in two counties (Kos sov) in the
1 March 2017
Eastern Slovak Republic.
Accepted 17 May 2017
Study design: Four hundred and twenty-six children were divided into groups according to ethnicity (non-Roma and Roma), age, sex, urban/rural residency and county of residence. Methods: Stool samples collected from participants were processed by formalineethyl ac-
Keywords:
etate sedimentation and examined microscopically.
Public health
Results: The overall prevalence of infection was 16.90% and the most prevalent species was
Children
Ascaris lumbricoides (14.32%). This was followed by Trichuris trichiura (3.76%), Hymenolepis
Rural and urban environment
nana (0.94%) and Hymenolepis diminuta (0.23%). The odds ratio for infection was 52 times
Helminth infections
higher among Roma children compared with non-Roma children. Among Roma children, the lowest prevalence of infection was reported in adolescents aged 16 years. No significant differences in the prevalence of helminths were found between different sexes, or between hospitalized and non-hospitalized participants. Roma children living in urban areas had a 3.36 higher probability of infection than those living in rural areas. Among ice County Roma children, helminth ova were found in 31.76% of the specimens from Kos ov County. Among non-Roma children, there was and 19.69% of the specimens from Pres only one positive finding in Pre sov County, and no cases in Ko sice County. Conclusions: Important risk factors associated with helminth infections are ethnicity, county of residence and urban/rural residency. Ascariasis, trichuriasis and hymenolepiasis still occur in children with low hygiene standards, and this needs to be addressed by local authorities. © 2017 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
* Corresponding author. Institute of Parasitology SAS, Hlinkova 3, 040 01 Ko sice, Slovak Republic. Tel.: +421 55 63 344 55. ). E-mail address: [email protected] (I. Papajova http://dx.doi.org/10.1016/j.puhe.2017.05.011 0033-3506/© 2017 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
72
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
Introduction Intestinal helminth infections are common in poor communities. Transmission of infections is associated with low personal hygiene and a contaminated environment. Large numbers of helminth infections are transmitted via the faecaleoral route where parasitic eggs are excreted into the environment in the stools of infected cases. The most common helminths are roundworms (Ascaris lumbricoides), whipworms (Trichuris trichiura) and hookworms (Necator americanus and Ancylostoma duodenale).1e4 All of these helminth infections are classified as neglected tropical diseases by the World Health Organization.5 According to World Health Organization,6 A. lumbricoides affect 1.2 billion people. T. trichiura affect 795 million people and hookworms affect 740 million people. Children are most vulnerable to helminth infections, with disease manifestation depending on both the parasite's developmental stage and the intensity of infection. Adult worms can survive in the gastrointestinal tract for approximately 1 year.7 Moreover, heavy gastrointestinal infection can lead to malabsorption, diarrhoea, anaemia and malnutrition.7e9 Helminth infections in children may also impair growth (stunting), cause intellectual retardation or affect cognitive and educational abilities.7,10 Infections primarily occur in remote or deprived urban settings among the poorest communities.4 Improved standards of personal hygiene, the development of an effective sewage system and waste water treatment have contributed to a reduction of environmental contamination and consequently lowered the spread of helminth infections.4,11,12 Most helminthiases are closely connected with socio-economically disadvantaged populations, which often live in areas with low hygiene standards. An estimated 16% of European Union citizens, or almost 80 million people, live below the poverty level.11 In Europe, the Roma population forms the largest minority13 and requires attention for their vulnerability to high rates of various neglected infections.11 While Roma people live around the world, they are concentrated mainly in Central Europe and the Balkans, with the highest numbers in Romania and Bulgaria.14,15 In the Slovak Republic, the total number of Roma residents is estimated to be 402,810, representing 7.43e9.70% of the entire population.16 Almost half of the Roma residents in the Slovak Republic are aged <18 years,17 and their level of education is significantly lower than that of the non-Roma population. Forty-four percent of the Roma population do not complete elementary education, and 37% of the Roma population only finish their primary education.18 According to Mu sinka et al.,16 168,940 Roma people live in marginalized or segregated settlements; this represents 42% of the Roma population of the Slovak Republic. These settlements can be situated inside villages but are more often found on the periphery of villages or are completely segregated. Significantly, the living conditions in such settlements are often inadequate, and the residents usually live in wooden or brick shacks that often lack basic infrastructural support. Roma people living in such conditions often share their living space with numerous dogs in the absence of veterinary care. As such, the health status of the Roma people is affected by
these differences in socio-economic settings.15 As there are no pertinent data available on this subject, the aim of this study was to investigate the occurrence of the most important helminth infections (ascariasis, trichuriasis and hymenolepiasis) in non-Roma and Roma child populations in the Eastern Slovak Republic.
Methods Study design This study was conducted in the towns and villages of Presov and Kosice Counties, representing 32.1% of the state territory. The population of Kosice County is 794,756 (14.7% of the Slovak population), including 126,675 Roma residents. The population of Presov County is 818,916 (15.1% of the Slovak population), including 114,207 Roma residents. According to the Atlas of Roma communities,16 there are 803 Roma settlements in the Slovak Republic. Of these, 30.70% of the Roma population live in the outskirts of villages (40.40%) or in segregated settlements (16.60%). However, most of the Roma population live with the non-Roma population (46.50%).16,19 Roma people live in shacks and houses in villages, apartments with reduced living standards and deserted apartments on housing estates in urban areas. This is associated with the accumulation of abandoned waste and a high density of rodents and insects. Regarding utilities in settlements, electricity is most commonly available (91.00%) and public sewerage is least accessible; only 41.70% of these settlements have access to the public sewer system. Gas is unavailable in 16.50% of settlements, and water pipes are unavailable in 17.40% of settlements. Up to 7.20% of dwellings do not have direct access to drinking water, so these residents regularly collect water from natural sources such as streams or creeks and consume this without proper sanitary treatment.16 Children in this study were either non-hospitalized (clinically healthy) or hospitalized. Additional parasitological examinations were performed among hospitalized children. For the analysis of helminth infections, both groups of children were examined according to age, sex and Roma or non-Roma ethnicity. The most common clinical symptoms during hospital admittance were anaemia, gastroenteritis, diarrhoea, abdominal pain, nausea and/or vomiting and fever of unknown origin.
Faecal sample collection and examination Children's stools were collected in plastic containers after informed consent forms were signed by their parents and legal guardians. Each stool container was identified with a unique identifier number and handed out together with instructions on how to collect and return a small portion (about 10e15 g) of morning stool. Containers with stool samples were stored without refrigeration and transferred to the Institute of Parasitology Slovak Academy of Sciences in Kosice (IP SAS) for diagnosis within 24e48 h. Each sample specimen was supplemented with information about the age, sex, urban/rural residency, hospital
73
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
admission and Roma/non-Roma ethnicity of the participant. Samples missing more than one of these criteria were excluded from the study. In total, 426 samples were included in the study. All stool samples were collected with either the parent's assistance or by hospital staff and transported to IP SAS. Overall, the participant rejection rate due to incomplete data or non-cooperation was 15%. Stool samples were examined with commercially available kit (Paraprep L, Mondial, France). Briefly, for each sample, 2 ml of ethyl acetate solution and 0.5 g of stool sample was added to 6 ml of 10% formalin in a mixing chamber. The chamber was connected via a filter to a conical collection chamber. After 24 h of incubation at room temperature, the tube was centrifuged (1000 rpm, 1 min), and samples were collected in the collection chamber. The supernatant was discarded and the sediment was placed on a microscope slide, covered with a coverslip. The entire viewing area was examined with a Leica DM 5000B light microscope (Leica Microsystems, Wetzlar, Germany) at 100 and 400 magnification.
Statistical analysis Statistical analysis was performed using MedCalc Statistical Software version 14.8.1 (MedCalc Software).20 Odds ratios (ORs) and 95% confidence intervals were determined. Chisquared tests (if all expected cell values 5) or Fisher's exact tests (if any expected cell value was <5) were used to compare the potential risk factors.
Results Overall, 426 faecal samples of non-hospitalized and hospitalized Roma and non-Roma children were examined for the presence of eggs. The overall prevalence of infection was 16.90% (72/426), and the most prevalent parasite was A. lumbricoides. Ascaris eggs were found in 14.32% of stool samples (61/426). The eggs of T. trichiura were found in 3.76% of samples (16/426, Table 1). The eggs of Hymenolepis nana (0.94%) and Hymenolepis diminuta (0.23%) were observed less often. Out of 72 positive samples, 63 contained a single helminth species; the other nine cases had co-infection with two species. The most frequent co-infection was A. lumbricoides and T. trichiura (six samples). Children were divided by ethnic group. The prevalence of infection among non-Roma children was only 0.66%. Meanwhile, the prevalence among Roma children was 25.82%. This difference was highly significant (chi-squared ¼ 43.92, P < 0.0001), and Roma children were infected more often than non-Roma children (OR: 52.21, Table 2).
Roma and non-Roma children were divided into five age groups: babies and toddlers aged <2 years, preschool children (3e5 years), younger school children at first stage of primary education (6e10 years), older school children at second stage of primary education (11e15 years), and adolescents (aged 16 years). As shown in Table 3a, the prevalence of infection in Roma children of different ages ranged from 13.33% to 31.25%. Only one non-Roma child (aged <2 years) tested positive for the presence of helminths (Table 3b). The occurrence of helminth infections in Roma and nonRoma children from the Eastern Slovak Republic according to hospital admission, sex, urban/rural residency and county of residence is summarized in Table 4a and 4b. The prevalence of helminths between hospitalized and non-hospitalized Roma children was similar (Table 4a): 27.36% and 22.97%, respectively. The prevalence of infection in non-hospitalized non-Roma children was 0.87%, and no cases of infection were detected in hospitalized non-Roma children (Table 4b). Infections were more common among Roma girls than Roma boys: 26.13% and 20.47%, respectively (OR: 1.37). However, this difference was not significant (chi-squared ¼ 1.07, P ¼ 0.30; Table 4a). Only one non-Roma girl was infected (Table 4b). A significant difference (chi-squared ¼ 7.65, P ¼ 0.006) in the prevalence of infection was observed between Roma children living in rural (28.36%) and urban (10.53%) areas. No such difference was detected in non-Roma children; only one child in Presov County was infected (Table 4b). Significant differences in the prevalence of infection were also noted between the two counties (Table 4a and b). In Roma children living in Kosice County, eggs were present in 31.76% of specimens, compared with 19.69% in Roma children living in Presov County (OR: 1.90, chi-squared ¼ 5.15, P ¼ 0.02).
Discussion This study investigated the occurrence of helminth infections in children in the Eastern Slovak Republic. The results show that the total prevalence of helminths in Roma children was 25.82%, whereas only one helminth infection (0.66%) was observed in a non-Roma child. A study conducted in 2008e2009 found that the total prevalence of intestinal helminths among children in the Slovak Republic was approximately 2.55%,20 but residency and nationality data of participating children were not provided. The most prevalent helminth species detected in this study were A. lumbricoides and T. trichiura,21 which corresponds with the present data. et al.22 studied the prevalence of inSimilarly, Rudohradska testinal parasites in children from a minority ethnic group
Table 1 e Number of samples examined for the occurrence of selected helminthic infections. Parasite species
Positive
Negative
Total
Prevalence (%)
95% CI
61 16 4 1
365 410 422 425
426 426 426 426
14.32 3.76 0.94 0.23
11.31e17.97 2.33e6.02 0.37e2.39 0.04e1.31
Ascaris lumbricoides Trichuris trichiura Hymenolepis nana Hymenolepis diminuta Abbreviation: CI, confidence interval.
74
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
Table 2 e Number of samples with the occurrence of helminths in children according to Roma of non-Roma ethnicity. Ethnicity
Positive
Negative
Total
Prevalence (%)
95% CI
OR
95% CI
c2
P-value
Roma Non-Roma
71 1
204 150
275 151
25.82 0.66
21.01e31.30 0.12e3.65
52.21
7.17e380
43.92
<0.0001
Abbreviations: CI, confidence interval; OR, odds ratio.
Table 3 e Number of samples with occurrence of helminths in the group of (a) Roma children and (b) non-Roma children by age. Age group (years)
Positive
Negative
Total
Prevalence (%)
95% CI
10 20 16 8 2
62 44 41 26 13
72 64 57 34 15
15.15 31.25 30.19 23.53 13.33
8.44e25.69 21.23e43.39 19.52e43.54 12.44e40.00 3.73e37.88
1 0 0 0 0
23 39 37 21 20
24 39 37 21 20
4.17 0 0 0 0
0.74e20.25 0e8.97 0e9.41 0e15.46 0e16.11
(a) 0e2 3e5 6e10 11e15 16 (b) 0e2 3e5 6e10 11e15 16
Abbreviation: CI, confidence interval.
Table 4 e Number of samples with the occurrence of helminths in (a) Roma children and (b) non-Roma children by hospital admission, sex, urban/rural residency and county. Variables (a) Hospitalized Non-hospitalized Girls Boys Rural Urban Ko sice County Pre sov County
Variables (b) Hospitalized Non-hospitalized Girls Boys Rural Urban Ko sice County Pre sov County
Positive
Negative
Total
Prevalence (%)
95% CI
OR
95% CI
c2
P-value
55 17 29 26 57 6 47 25
146 57 82 101 144 51 101 102
201 74 111 127 201 57 148 127
27.36 22.97 26.13 20.47 28.36 10.53 31.76 19.69
21.66e33.90 14.86e33.74 18.85e35.00 14.37e28.30 22.58e34.95 4.92e21.13 24.80e39.64 13.71e27.45
1.26
0.68e2.36
0.54
0.46
1.37
0.75e2.51
1.07
0.3
3.36
1.37e8.27
7.65
0.006
1.90
1.09e3.32
5.15
0.02
Positive
Negative
Total
Prevalence (%)
95% CI
0 1 1 0 0 1 0 1
36 114 70 58 26 93 26 80
36 115 71 58 26 94 26 81
0 0.87 1.41 0 0 1.06 0 1.23
0e9.64 0.15e4.76 0.25e7.56 0e6.21 0e16.02 0.19e5.78 0e12.87 0.22e6.66
Abbreviation: CI, confidence interval; OR, odds ratio; c2, chi square.
with low hygienic standards in the Slovak Republic, and A. lumbricoides was found to be the leading parasite (24.70%), followed by T. trichiura (17.30%). Tapeworm (Taenia spp.) eggs were detected in 4.90% of examined children.22 According to older data from the Slovak Republic,23 the prevalence of A. lumbricoides in children from the Martin District (Central Slovak Republic) was very low (0.14e2.30%). The eggs of T. trichiura were detected more often (0.52e5.70%). In comparison, a higher prevalence of T. trichiura was found in children
living in rural environments in Albania,24 and A. lumbricoides infection was more common in hospitalized children in Romania.25 This study detected five tapeworm infections: four samples (0.94%) contained eggs of H. nana and one sample (0.23%) contained eggs of H. diminuta. Cabeza et al.26 reported that H. nana is the most common tapeworm in humans. The prevalence of H. nana in Southern Spain from January 2000 to December 2013 ranged between 0.21% and 61.00% and was
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
higher in adults than in children.26 Occasional occurrence (1.84%) of Hymenolepis spp. among paediatric patients was described by Juri s et al.,27 and solitary cases have been reported from Italy and Poland.28,29 Current data on the prevalence of intestinal helminth infections among children in neighbouring countries in Central Europe are very limited. The prevalence of intestinal parasites in Poland between 2000 and 2006 ranged between 3.30% and 46.30%.30,31 This study could not detect significant differences between age groups; lower infection rates among infants aged et al.22 and LaBeaud <1 year were reported by Rudohradska 32 et al. In the present study, in three examined groups (age 3e15 years), the prevalence of helminth infections varied between 23.53% and 31.25% in Roma children, and a decrease was observed with age.33 Many authors have reported a similar decline in the prevalence of infection with A. lumbricoides and T. trichiura when approaching adulthood.34e36 A significant difference (P < 0.0001) was found in the prevalence of helminths in Roma children (25.82%) compared with non-Roma children (0.66%; OR: 2.21). A higher prevalence of intestinal parasites in healthy Roma children was recorded in a 2012 study that found a total prevalence of intestinal parasites of 56.80%.22 It is well known that a rural environment plays an important part in the spread of helminth infections, and improvement in health services and infrastructure in rural areas is necessary to control the high prevalence of parasitic infections.37 No significant difference in the occurrence of helminth diseases was found between the sexes. This finding is in accordance with the studies of Alemu et al.38 and Abossie and Seid.39 Other studies have suggested that infections are more common in girls than boys.40,41 Based on these results, it is concluded that helminth infections have not been eradicated completely. In particular, Roma children living in rural environments are at higher risk of infection than non-Roma children. It is likely that the higher prevalence of these infections in rural environments is due to environmental contamination that contributes to the occurrence of reinfection. Helminthiases still represent an actual health threat, especially for children in the Eastern Slovak Republic, and thus eradication and public health programmes addressing hygiene standards need to be implemented by local governmental authorities.
Author statements Ethical approval This study was approved by the Ethical Commission of Institute of Parasitology Slovak Academy of Sciences in Kosice. Children, parents and legal representatives agreed with all investigations and signed the informed consent form before examinations and hospitalizations.
Funding This work was supported by the Scientific Grant Agency of the Ministry of Education of the Slovak Republic, with support from the Slovak Academy of Sciences, VEGA no. 2/0125/17
75
(0.5), VEGA no. 2/0081/15 (0.1) and a project by the Ministry of Education, Science, Research and Sports of the Slovak Republic ‘Origin and pathogenesis of obesity in relation to nontraditional obesity risk factors’ (0.1). The publication was realized within the scope of the projects performed in the Centre of Excellence for Parasitology (Code ITMS: 26220120022) based on funding support from the Operational Programme ‘Research & Development’, which is funded by the European Regional Development Fund (0.3).
Competing interests None declared.
references
1. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors 2014;7:37. 2. Campbell SJ, Savage GB, Gray DJ, Atkinson JA, Soares € es RJ, Nery SV, et al. Water, sanitation, and hygiene Magalha (WASH): a critical component for sustainable soil-transmitted helminth and schistosomiasis control. PLoS Negl Trop Dis 2014;4:e2651. 3. Okoyo C, Nikolay B, Kihara J, Simiyu E, Garn JV, Freeman MC, et al. Monitoring the impact of a national school based deworming programme on soil-transmitted helminths in Kenya: the first three years, 2012e2014. Parasites Vectors 2016;9:408. 4. Yapi RB, CHammartin F, Hu¨rlimann E, Houngbedji CA, KD, et al. Bayesian risk profiling of soilN'Dri PB, Silue transmitted helminth infections and estimates of preventive ^ te d'Ivoire. chemotherapy for school-aged children in Co Parasites Vectors 2016;9:162. 5. World Health Organization. Accelerating work to overcome the global impact of neglected tropical diseases: a roadmap for implementation. Washington: WHO; 2012. p. 1e42. 6. World Health Organization. World health statistics 2014. Geneva: WHO; 2014. Available at: http://apps.who.int/iris/ bitstream/10665/112738/1/9789240692671_eng.pdf (last accessed 17 May 2017). 7. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 2006;367:1521e32. 8. Ehrenberg JP, Ault SK. Neglected diseases of neglected populations: thinking to reshape the determinants of health in Latin America and the Caribbean. BMC Public Health 2005;5:119. 9. Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Sachs SE, Sachs JD, et al. Control of neglected tropical diseases. N Engl J Med 2007;357:1018e27. 10. Guyatt HL. Do intestinal nematode affect productivity in adulthood? Parasitol Today 2000;16:153e8. 11. Hotez PJ, Gurwith M. Europe's neglected infections of poverty. Int J Infect Dis 2011;15:e611e9. z I, Pipikova J, Papaj J, Ci r A. Parasitic ma 12. Papajova contamination of urban and rural environments in the Slovak Republic: dog's excrements as a source. Helminthologia 2014;51:273e80. 13. Brearley M. The persecution of gypsies in Europe. Am Behav Sci 2001;45:588e99. 14. Rechel B, Blackburn CM, Spencer NJ, Rechel B. Access to health care for Roma children in Central and Eastern Europe:
76
15.
16.
17. 18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
findings from a qualitative study in Bulgaria. Int J Equity Health 2009;8:1. Geckova A, Babinska I, Boba kova D, Madarasova Veselska Z, Bosa kova L, Kolarc ı´k P, et al. Dankulincova Socioeconomic characteristics of the population living in Roma settlements and their association with health and health-related behaviour. Cent Eur J Public Health 2014;(Suppl):S57e64. ova K, Kling J. Atlas of Mu sinka A, Skobla D, Hurrle J, Matlovic Roma communities in Slovakia 2013. Regional centre for UN developmental programme for EU in Bratislava. Bratislava: UNDP; 2014. rova K. The health of the Roma people in Central and Eastern Rima a rik University; 2010. Europe. Ko sice: Pavol Jozef Saf Z. Promoting the social inclusion of Roma. A study of national Kusa policies. Bratislava: Institute for Sociology of the Slovak Academy of Sciences; 2011. J, Gerbery D, Skobla Filadelfiova D. Report on the living conditions of Roma in Slovakia. Bratislava: UNDP, Regional Bureau for Europe; 2007. MEDCALC STATISTICAL SOFTWARE VERSION 14.8.1. Ostend, Belgium: MedCalc Software bvba; 2016. https://www.medcalc. org. € nigova A, Kinc ekova J, Hrc kova G, Velebny´ S, Va rady M, Ko J, et al. Nematode infections in Slovak children Pavlinova hospitalised during 2008e2009. Helminthologia 2010;47:204e11. P, Hala nova M, Ravaszova P, Goldova M, Rudohradska a kova A, Hala n M, et al. Prevalence of intestinal Valenc parasites in children from minority group with low hygienic standards in Slovakia. Helminthologia 2012;49:63e6. Skra ikova J. Intestinal parasites in children Straka S, c collectives of Martin district, Czechoslovakia. A comparative study after 15 years. Mitt Osten Ges Tropenmed Parasitol 1987;9:59e64. Gjoni V, Abazaj E, Hysaj BV, Petri O, Ali E. Comparative study of the prevalence of intestinal parasites in low socioeconomic €z, Fier, Albania. Int J Sci Res condition in one village Balte 2015;4:1669e73. Neghina R, Neghina AM, Marincu I, Iacobiciu I. Intestinal nematode infections in Romania: an epidemiological study and brief review of literature. Vector-Borne Zoonot Dis 2011;11:1145e9. zquez J. Cabeza MI, Cabezas MT, Cobo F, Salas J, Va Hymenolepis nana infection: associated factors with this parasitism in a health area of Southern Spain. Rev Chil Infectol 2015;32:593e5. A, Fa bry J, Melter J, Miskovska M, Mindz kova E, a Juri s P, Dudlova et al. Endoparasitoses in hospitalised paediatric patients with pulmonary disease. Helminthologia 2014;51:98e102. Waloch M. Cestode infections in Poland in 2002. Przeglad Epidemiol 2004;58:165e9.
29. Patamia I, Cappello E, Castellano-Chiodo D, Greco F, Nigro L, Cacopardo B. A human case of Hymenolepis diminuta in a child from eastern Sicily. Korean J Parasitol 2010;48:167e9. ska M, Dzika E, Dziedziech M, Poz niak H, 30. Kubiak K, Wron Leokajtis M, et al. The prevalence of intestinal parasites in children in preschools and orphanages in the WarmiaMasuria province (North-Eastern Poland). Przeglad Epidemiol 2015;69:483. 31. Małafiej E, Spiewak E. Serological investigation in children infected with Ascaris lumbricoides. Wiadomosci Parazytol 2000;47:585e90. 32. Labeaud AD, Singer MN, McKibben M, Mungai P, Muchiri EM, McKibben E, et al. Parasitism in children aged three years and under: relationship between infection and growth in rural coastal Kenya. PLoS Negl Trop Dis 2015;9:e0003721. 33. Krause RJ, Koski KG, Pons E, Sinisterra O, Scott ME. Ascaris and hookworm transmission in preschool children in rural Panama: role of subsistence agricultural activities. Parasitology 2016;143:1043e54. 34. Lili Z, Bingxiang Z, Hong T, Shuhua X, Hotez P, Bing Z, et al. Epidemiology of human geohelminth infections (ascariasis, trichuriasis and necatoriasis) in Lushui and Puer Counties, Yunnan Province, China. Southeast Asian J Trop Med Public Health 2000;31:448e53. 35. O'Lorcain P, Holland CV. The public health importance of Ascaris lumbricoides. Parasitology 2000;121(Suppl. 1):S51e71. 36. Harhay MO, Horton J, Olliaro PL. Epidemiology and control of human gastrointestinal parasites in children. Exp Rev Anti Infect Ther 2010;8:219e34. ski TH. 37. Bitkowska E, Wnukowska N, Wojtyniak B, Dzben Occurrence of intestinal parasites among children attending first classes of the elementary schools in Poland in school year 2002/2003. Przeglad Epidemiol 2004;58:295e302. 38. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, Mathewos B, et al. Soil transmitted helminths and Schistosoma mansoni infections among school children in Zarima town, northwest Ethiopia. BMC Infect Dis 2011;11:189. 39. Abossie A, Seid M. Assessment of the prevalence of intestinal parasitosis and associated risk factors among primary school children in Chencha town, Southern Ethiopia. BMC Public Health 2014;14:1. 40. Haswell-Elkins M, Elkins D, Anderson BM. The influence of individual, social group and household factors on the distribution of Ascaris lumbricoides within a community and implications for control strategies. Parasitology 1989;98:125e34. 41. Kightlinger LK, Seed JR, Kightlinger MB. Ascaris lumbricoides intensity in relation to environmental, socioeconomic, and behavioral determinants of exposure to infection in children from southeast Madagascar. J Parasitol 1998;84:480e4.
Available online at www.sciencedirect.com
Public Health journal homepage: www.elsevier.com/puhe
Original Research
Occurrence of the most common helminth infections among children in the Eastern Slovak Republic a a, Ingrid Papajova a,*, Jindrich Soltys b Jana Pipikova , Ingrid Schusterova
Institute of Parasitology, Slovak Academy of Sciences, Kosice, Slovak Republic a rik University, Faculty of Medicine, Kosice, Department of Paediatrics and Adolescent Medicine, Pavol Jozef Saf Slovak Republic a
b
article info
abstract
Article history:
Objectives: Ascariasis, trichuriasis and hymenolepiasis occur primarily within poor com-
Received 19 December 2016 Received in revised form
munities with low hygiene standards. This study examined the occurrence of intestinal ice and Pre helminth infections among children living in two counties (Kos sov) in the
1 March 2017
Eastern Slovak Republic.
Accepted 17 May 2017
Study design: Four hundred and twenty-six children were divided into groups according to ethnicity (non-Roma and Roma), age, sex, urban/rural residency and county of residence. Methods: Stool samples collected from participants were processed by formalineethyl ac-
Keywords:
etate sedimentation and examined microscopically.
Public health
Results: The overall prevalence of infection was 16.90% and the most prevalent species was
Children
Ascaris lumbricoides (14.32%). This was followed by Trichuris trichiura (3.76%), Hymenolepis
Rural and urban environment
nana (0.94%) and Hymenolepis diminuta (0.23%). The odds ratio for infection was 52 times
Helminth infections
higher among Roma children compared with non-Roma children. Among Roma children, the lowest prevalence of infection was reported in adolescents aged 16 years. No significant differences in the prevalence of helminths were found between different sexes, or between hospitalized and non-hospitalized participants. Roma children living in urban areas had a 3.36 higher probability of infection than those living in rural areas. Among ice County Roma children, helminth ova were found in 31.76% of the specimens from Kos ov County. Among non-Roma children, there was and 19.69% of the specimens from Pres only one positive finding in Pre sov County, and no cases in Ko sice County. Conclusions: Important risk factors associated with helminth infections are ethnicity, county of residence and urban/rural residency. Ascariasis, trichuriasis and hymenolepiasis still occur in children with low hygiene standards, and this needs to be addressed by local authorities. © 2017 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
* Corresponding author. Institute of Parasitology SAS, Hlinkova 3, 040 01 Ko sice, Slovak Republic. Tel.: +421 55 63 344 55. ). E-mail address: [email protected] (I. Papajova http://dx.doi.org/10.1016/j.puhe.2017.05.011 0033-3506/© 2017 The Royal Society for Public Health. Published by Elsevier Ltd. All rights reserved.
72
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
Introduction Intestinal helminth infections are common in poor communities. Transmission of infections is associated with low personal hygiene and a contaminated environment. Large numbers of helminth infections are transmitted via the faecaleoral route where parasitic eggs are excreted into the environment in the stools of infected cases. The most common helminths are roundworms (Ascaris lumbricoides), whipworms (Trichuris trichiura) and hookworms (Necator americanus and Ancylostoma duodenale).1e4 All of these helminth infections are classified as neglected tropical diseases by the World Health Organization.5 According to World Health Organization,6 A. lumbricoides affect 1.2 billion people. T. trichiura affect 795 million people and hookworms affect 740 million people. Children are most vulnerable to helminth infections, with disease manifestation depending on both the parasite's developmental stage and the intensity of infection. Adult worms can survive in the gastrointestinal tract for approximately 1 year.7 Moreover, heavy gastrointestinal infection can lead to malabsorption, diarrhoea, anaemia and malnutrition.7e9 Helminth infections in children may also impair growth (stunting), cause intellectual retardation or affect cognitive and educational abilities.7,10 Infections primarily occur in remote or deprived urban settings among the poorest communities.4 Improved standards of personal hygiene, the development of an effective sewage system and waste water treatment have contributed to a reduction of environmental contamination and consequently lowered the spread of helminth infections.4,11,12 Most helminthiases are closely connected with socio-economically disadvantaged populations, which often live in areas with low hygiene standards. An estimated 16% of European Union citizens, or almost 80 million people, live below the poverty level.11 In Europe, the Roma population forms the largest minority13 and requires attention for their vulnerability to high rates of various neglected infections.11 While Roma people live around the world, they are concentrated mainly in Central Europe and the Balkans, with the highest numbers in Romania and Bulgaria.14,15 In the Slovak Republic, the total number of Roma residents is estimated to be 402,810, representing 7.43e9.70% of the entire population.16 Almost half of the Roma residents in the Slovak Republic are aged <18 years,17 and their level of education is significantly lower than that of the non-Roma population. Forty-four percent of the Roma population do not complete elementary education, and 37% of the Roma population only finish their primary education.18 According to Mu sinka et al.,16 168,940 Roma people live in marginalized or segregated settlements; this represents 42% of the Roma population of the Slovak Republic. These settlements can be situated inside villages but are more often found on the periphery of villages or are completely segregated. Significantly, the living conditions in such settlements are often inadequate, and the residents usually live in wooden or brick shacks that often lack basic infrastructural support. Roma people living in such conditions often share their living space with numerous dogs in the absence of veterinary care. As such, the health status of the Roma people is affected by
these differences in socio-economic settings.15 As there are no pertinent data available on this subject, the aim of this study was to investigate the occurrence of the most important helminth infections (ascariasis, trichuriasis and hymenolepiasis) in non-Roma and Roma child populations in the Eastern Slovak Republic.
Methods Study design This study was conducted in the towns and villages of Presov and Kosice Counties, representing 32.1% of the state territory. The population of Kosice County is 794,756 (14.7% of the Slovak population), including 126,675 Roma residents. The population of Presov County is 818,916 (15.1% of the Slovak population), including 114,207 Roma residents. According to the Atlas of Roma communities,16 there are 803 Roma settlements in the Slovak Republic. Of these, 30.70% of the Roma population live in the outskirts of villages (40.40%) or in segregated settlements (16.60%). However, most of the Roma population live with the non-Roma population (46.50%).16,19 Roma people live in shacks and houses in villages, apartments with reduced living standards and deserted apartments on housing estates in urban areas. This is associated with the accumulation of abandoned waste and a high density of rodents and insects. Regarding utilities in settlements, electricity is most commonly available (91.00%) and public sewerage is least accessible; only 41.70% of these settlements have access to the public sewer system. Gas is unavailable in 16.50% of settlements, and water pipes are unavailable in 17.40% of settlements. Up to 7.20% of dwellings do not have direct access to drinking water, so these residents regularly collect water from natural sources such as streams or creeks and consume this without proper sanitary treatment.16 Children in this study were either non-hospitalized (clinically healthy) or hospitalized. Additional parasitological examinations were performed among hospitalized children. For the analysis of helminth infections, both groups of children were examined according to age, sex and Roma or non-Roma ethnicity. The most common clinical symptoms during hospital admittance were anaemia, gastroenteritis, diarrhoea, abdominal pain, nausea and/or vomiting and fever of unknown origin.
Faecal sample collection and examination Children's stools were collected in plastic containers after informed consent forms were signed by their parents and legal guardians. Each stool container was identified with a unique identifier number and handed out together with instructions on how to collect and return a small portion (about 10e15 g) of morning stool. Containers with stool samples were stored without refrigeration and transferred to the Institute of Parasitology Slovak Academy of Sciences in Kosice (IP SAS) for diagnosis within 24e48 h. Each sample specimen was supplemented with information about the age, sex, urban/rural residency, hospital
73
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
admission and Roma/non-Roma ethnicity of the participant. Samples missing more than one of these criteria were excluded from the study. In total, 426 samples were included in the study. All stool samples were collected with either the parent's assistance or by hospital staff and transported to IP SAS. Overall, the participant rejection rate due to incomplete data or non-cooperation was 15%. Stool samples were examined with commercially available kit (Paraprep L, Mondial, France). Briefly, for each sample, 2 ml of ethyl acetate solution and 0.5 g of stool sample was added to 6 ml of 10% formalin in a mixing chamber. The chamber was connected via a filter to a conical collection chamber. After 24 h of incubation at room temperature, the tube was centrifuged (1000 rpm, 1 min), and samples were collected in the collection chamber. The supernatant was discarded and the sediment was placed on a microscope slide, covered with a coverslip. The entire viewing area was examined with a Leica DM 5000B light microscope (Leica Microsystems, Wetzlar, Germany) at 100 and 400 magnification.
Statistical analysis Statistical analysis was performed using MedCalc Statistical Software version 14.8.1 (MedCalc Software).20 Odds ratios (ORs) and 95% confidence intervals were determined. Chisquared tests (if all expected cell values 5) or Fisher's exact tests (if any expected cell value was <5) were used to compare the potential risk factors.
Results Overall, 426 faecal samples of non-hospitalized and hospitalized Roma and non-Roma children were examined for the presence of eggs. The overall prevalence of infection was 16.90% (72/426), and the most prevalent parasite was A. lumbricoides. Ascaris eggs were found in 14.32% of stool samples (61/426). The eggs of T. trichiura were found in 3.76% of samples (16/426, Table 1). The eggs of Hymenolepis nana (0.94%) and Hymenolepis diminuta (0.23%) were observed less often. Out of 72 positive samples, 63 contained a single helminth species; the other nine cases had co-infection with two species. The most frequent co-infection was A. lumbricoides and T. trichiura (six samples). Children were divided by ethnic group. The prevalence of infection among non-Roma children was only 0.66%. Meanwhile, the prevalence among Roma children was 25.82%. This difference was highly significant (chi-squared ¼ 43.92, P < 0.0001), and Roma children were infected more often than non-Roma children (OR: 52.21, Table 2).
Roma and non-Roma children were divided into five age groups: babies and toddlers aged <2 years, preschool children (3e5 years), younger school children at first stage of primary education (6e10 years), older school children at second stage of primary education (11e15 years), and adolescents (aged 16 years). As shown in Table 3a, the prevalence of infection in Roma children of different ages ranged from 13.33% to 31.25%. Only one non-Roma child (aged <2 years) tested positive for the presence of helminths (Table 3b). The occurrence of helminth infections in Roma and nonRoma children from the Eastern Slovak Republic according to hospital admission, sex, urban/rural residency and county of residence is summarized in Table 4a and 4b. The prevalence of helminths between hospitalized and non-hospitalized Roma children was similar (Table 4a): 27.36% and 22.97%, respectively. The prevalence of infection in non-hospitalized non-Roma children was 0.87%, and no cases of infection were detected in hospitalized non-Roma children (Table 4b). Infections were more common among Roma girls than Roma boys: 26.13% and 20.47%, respectively (OR: 1.37). However, this difference was not significant (chi-squared ¼ 1.07, P ¼ 0.30; Table 4a). Only one non-Roma girl was infected (Table 4b). A significant difference (chi-squared ¼ 7.65, P ¼ 0.006) in the prevalence of infection was observed between Roma children living in rural (28.36%) and urban (10.53%) areas. No such difference was detected in non-Roma children; only one child in Presov County was infected (Table 4b). Significant differences in the prevalence of infection were also noted between the two counties (Table 4a and b). In Roma children living in Kosice County, eggs were present in 31.76% of specimens, compared with 19.69% in Roma children living in Presov County (OR: 1.90, chi-squared ¼ 5.15, P ¼ 0.02).
Discussion This study investigated the occurrence of helminth infections in children in the Eastern Slovak Republic. The results show that the total prevalence of helminths in Roma children was 25.82%, whereas only one helminth infection (0.66%) was observed in a non-Roma child. A study conducted in 2008e2009 found that the total prevalence of intestinal helminths among children in the Slovak Republic was approximately 2.55%,20 but residency and nationality data of participating children were not provided. The most prevalent helminth species detected in this study were A. lumbricoides and T. trichiura,21 which corresponds with the present data. et al.22 studied the prevalence of inSimilarly, Rudohradska testinal parasites in children from a minority ethnic group
Table 1 e Number of samples examined for the occurrence of selected helminthic infections. Parasite species
Positive
Negative
Total
Prevalence (%)
95% CI
61 16 4 1
365 410 422 425
426 426 426 426
14.32 3.76 0.94 0.23
11.31e17.97 2.33e6.02 0.37e2.39 0.04e1.31
Ascaris lumbricoides Trichuris trichiura Hymenolepis nana Hymenolepis diminuta Abbreviation: CI, confidence interval.
74
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
Table 2 e Number of samples with the occurrence of helminths in children according to Roma of non-Roma ethnicity. Ethnicity
Positive
Negative
Total
Prevalence (%)
95% CI
OR
95% CI
c2
P-value
Roma Non-Roma
71 1
204 150
275 151
25.82 0.66
21.01e31.30 0.12e3.65
52.21
7.17e380
43.92
<0.0001
Abbreviations: CI, confidence interval; OR, odds ratio.
Table 3 e Number of samples with occurrence of helminths in the group of (a) Roma children and (b) non-Roma children by age. Age group (years)
Positive
Negative
Total
Prevalence (%)
95% CI
10 20 16 8 2
62 44 41 26 13
72 64 57 34 15
15.15 31.25 30.19 23.53 13.33
8.44e25.69 21.23e43.39 19.52e43.54 12.44e40.00 3.73e37.88
1 0 0 0 0
23 39 37 21 20
24 39 37 21 20
4.17 0 0 0 0
0.74e20.25 0e8.97 0e9.41 0e15.46 0e16.11
(a) 0e2 3e5 6e10 11e15 16 (b) 0e2 3e5 6e10 11e15 16
Abbreviation: CI, confidence interval.
Table 4 e Number of samples with the occurrence of helminths in (a) Roma children and (b) non-Roma children by hospital admission, sex, urban/rural residency and county. Variables (a) Hospitalized Non-hospitalized Girls Boys Rural Urban Ko sice County Pre sov County
Variables (b) Hospitalized Non-hospitalized Girls Boys Rural Urban Ko sice County Pre sov County
Positive
Negative
Total
Prevalence (%)
95% CI
OR
95% CI
c2
P-value
55 17 29 26 57 6 47 25
146 57 82 101 144 51 101 102
201 74 111 127 201 57 148 127
27.36 22.97 26.13 20.47 28.36 10.53 31.76 19.69
21.66e33.90 14.86e33.74 18.85e35.00 14.37e28.30 22.58e34.95 4.92e21.13 24.80e39.64 13.71e27.45
1.26
0.68e2.36
0.54
0.46
1.37
0.75e2.51
1.07
0.3
3.36
1.37e8.27
7.65
0.006
1.90
1.09e3.32
5.15
0.02
Positive
Negative
Total
Prevalence (%)
95% CI
0 1 1 0 0 1 0 1
36 114 70 58 26 93 26 80
36 115 71 58 26 94 26 81
0 0.87 1.41 0 0 1.06 0 1.23
0e9.64 0.15e4.76 0.25e7.56 0e6.21 0e16.02 0.19e5.78 0e12.87 0.22e6.66
Abbreviation: CI, confidence interval; OR, odds ratio; c2, chi square.
with low hygienic standards in the Slovak Republic, and A. lumbricoides was found to be the leading parasite (24.70%), followed by T. trichiura (17.30%). Tapeworm (Taenia spp.) eggs were detected in 4.90% of examined children.22 According to older data from the Slovak Republic,23 the prevalence of A. lumbricoides in children from the Martin District (Central Slovak Republic) was very low (0.14e2.30%). The eggs of T. trichiura were detected more often (0.52e5.70%). In comparison, a higher prevalence of T. trichiura was found in children
living in rural environments in Albania,24 and A. lumbricoides infection was more common in hospitalized children in Romania.25 This study detected five tapeworm infections: four samples (0.94%) contained eggs of H. nana and one sample (0.23%) contained eggs of H. diminuta. Cabeza et al.26 reported that H. nana is the most common tapeworm in humans. The prevalence of H. nana in Southern Spain from January 2000 to December 2013 ranged between 0.21% and 61.00% and was
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
higher in adults than in children.26 Occasional occurrence (1.84%) of Hymenolepis spp. among paediatric patients was described by Juri s et al.,27 and solitary cases have been reported from Italy and Poland.28,29 Current data on the prevalence of intestinal helminth infections among children in neighbouring countries in Central Europe are very limited. The prevalence of intestinal parasites in Poland between 2000 and 2006 ranged between 3.30% and 46.30%.30,31 This study could not detect significant differences between age groups; lower infection rates among infants aged et al.22 and LaBeaud <1 year were reported by Rudohradska 32 et al. In the present study, in three examined groups (age 3e15 years), the prevalence of helminth infections varied between 23.53% and 31.25% in Roma children, and a decrease was observed with age.33 Many authors have reported a similar decline in the prevalence of infection with A. lumbricoides and T. trichiura when approaching adulthood.34e36 A significant difference (P < 0.0001) was found in the prevalence of helminths in Roma children (25.82%) compared with non-Roma children (0.66%; OR: 2.21). A higher prevalence of intestinal parasites in healthy Roma children was recorded in a 2012 study that found a total prevalence of intestinal parasites of 56.80%.22 It is well known that a rural environment plays an important part in the spread of helminth infections, and improvement in health services and infrastructure in rural areas is necessary to control the high prevalence of parasitic infections.37 No significant difference in the occurrence of helminth diseases was found between the sexes. This finding is in accordance with the studies of Alemu et al.38 and Abossie and Seid.39 Other studies have suggested that infections are more common in girls than boys.40,41 Based on these results, it is concluded that helminth infections have not been eradicated completely. In particular, Roma children living in rural environments are at higher risk of infection than non-Roma children. It is likely that the higher prevalence of these infections in rural environments is due to environmental contamination that contributes to the occurrence of reinfection. Helminthiases still represent an actual health threat, especially for children in the Eastern Slovak Republic, and thus eradication and public health programmes addressing hygiene standards need to be implemented by local governmental authorities.
Author statements Ethical approval This study was approved by the Ethical Commission of Institute of Parasitology Slovak Academy of Sciences in Kosice. Children, parents and legal representatives agreed with all investigations and signed the informed consent form before examinations and hospitalizations.
Funding This work was supported by the Scientific Grant Agency of the Ministry of Education of the Slovak Republic, with support from the Slovak Academy of Sciences, VEGA no. 2/0125/17
75
(0.5), VEGA no. 2/0081/15 (0.1) and a project by the Ministry of Education, Science, Research and Sports of the Slovak Republic ‘Origin and pathogenesis of obesity in relation to nontraditional obesity risk factors’ (0.1). The publication was realized within the scope of the projects performed in the Centre of Excellence for Parasitology (Code ITMS: 26220120022) based on funding support from the Operational Programme ‘Research & Development’, which is funded by the European Regional Development Fund (0.3).
Competing interests None declared.
references
1. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors 2014;7:37. 2. Campbell SJ, Savage GB, Gray DJ, Atkinson JA, Soares € es RJ, Nery SV, et al. Water, sanitation, and hygiene Magalha (WASH): a critical component for sustainable soil-transmitted helminth and schistosomiasis control. PLoS Negl Trop Dis 2014;4:e2651. 3. Okoyo C, Nikolay B, Kihara J, Simiyu E, Garn JV, Freeman MC, et al. Monitoring the impact of a national school based deworming programme on soil-transmitted helminths in Kenya: the first three years, 2012e2014. Parasites Vectors 2016;9:408. 4. Yapi RB, CHammartin F, Hu¨rlimann E, Houngbedji CA, KD, et al. Bayesian risk profiling of soilN'Dri PB, Silue transmitted helminth infections and estimates of preventive ^ te d'Ivoire. chemotherapy for school-aged children in Co Parasites Vectors 2016;9:162. 5. World Health Organization. Accelerating work to overcome the global impact of neglected tropical diseases: a roadmap for implementation. Washington: WHO; 2012. p. 1e42. 6. World Health Organization. World health statistics 2014. Geneva: WHO; 2014. Available at: http://apps.who.int/iris/ bitstream/10665/112738/1/9789240692671_eng.pdf (last accessed 17 May 2017). 7. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 2006;367:1521e32. 8. Ehrenberg JP, Ault SK. Neglected diseases of neglected populations: thinking to reshape the determinants of health in Latin America and the Caribbean. BMC Public Health 2005;5:119. 9. Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Sachs SE, Sachs JD, et al. Control of neglected tropical diseases. N Engl J Med 2007;357:1018e27. 10. Guyatt HL. Do intestinal nematode affect productivity in adulthood? Parasitol Today 2000;16:153e8. 11. Hotez PJ, Gurwith M. Europe's neglected infections of poverty. Int J Infect Dis 2011;15:e611e9. z I, Pipikova J, Papaj J, Ci r A. Parasitic ma 12. Papajova contamination of urban and rural environments in the Slovak Republic: dog's excrements as a source. Helminthologia 2014;51:273e80. 13. Brearley M. The persecution of gypsies in Europe. Am Behav Sci 2001;45:588e99. 14. Rechel B, Blackburn CM, Spencer NJ, Rechel B. Access to health care for Roma children in Central and Eastern Europe:
76
15.
16.
17. 18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
p u b l i c h e a l t h 1 5 0 ( 2 0 1 7 ) 7 1 e7 6
findings from a qualitative study in Bulgaria. Int J Equity Health 2009;8:1. Geckova A, Babinska I, Boba kova D, Madarasova Veselska Z, Bosa kova L, Kolarc ı´k P, et al. Dankulincova Socioeconomic characteristics of the population living in Roma settlements and their association with health and health-related behaviour. Cent Eur J Public Health 2014;(Suppl):S57e64. ova K, Kling J. Atlas of Mu sinka A, Skobla D, Hurrle J, Matlovic Roma communities in Slovakia 2013. Regional centre for UN developmental programme for EU in Bratislava. Bratislava: UNDP; 2014. rova K. The health of the Roma people in Central and Eastern Rima a rik University; 2010. Europe. Ko sice: Pavol Jozef Saf Z. Promoting the social inclusion of Roma. A study of national Kusa policies. Bratislava: Institute for Sociology of the Slovak Academy of Sciences; 2011. J, Gerbery D, Skobla Filadelfiova D. Report on the living conditions of Roma in Slovakia. Bratislava: UNDP, Regional Bureau for Europe; 2007. MEDCALC STATISTICAL SOFTWARE VERSION 14.8.1. Ostend, Belgium: MedCalc Software bvba; 2016. https://www.medcalc. org. € nigova A, Kinc ekova J, Hrc kova G, Velebny´ S, Va rady M, Ko J, et al. Nematode infections in Slovak children Pavlinova hospitalised during 2008e2009. Helminthologia 2010;47:204e11. P, Hala nova M, Ravaszova P, Goldova M, Rudohradska a kova A, Hala n M, et al. Prevalence of intestinal Valenc parasites in children from minority group with low hygienic standards in Slovakia. Helminthologia 2012;49:63e6. Skra ikova J. Intestinal parasites in children Straka S, c collectives of Martin district, Czechoslovakia. A comparative study after 15 years. Mitt Osten Ges Tropenmed Parasitol 1987;9:59e64. Gjoni V, Abazaj E, Hysaj BV, Petri O, Ali E. Comparative study of the prevalence of intestinal parasites in low socioeconomic €z, Fier, Albania. Int J Sci Res condition in one village Balte 2015;4:1669e73. Neghina R, Neghina AM, Marincu I, Iacobiciu I. Intestinal nematode infections in Romania: an epidemiological study and brief review of literature. Vector-Borne Zoonot Dis 2011;11:1145e9. zquez J. Cabeza MI, Cabezas MT, Cobo F, Salas J, Va Hymenolepis nana infection: associated factors with this parasitism in a health area of Southern Spain. Rev Chil Infectol 2015;32:593e5. A, Fa bry J, Melter J, Miskovska M, Mindz kova E, a Juri s P, Dudlova et al. Endoparasitoses in hospitalised paediatric patients with pulmonary disease. Helminthologia 2014;51:98e102. Waloch M. Cestode infections in Poland in 2002. Przeglad Epidemiol 2004;58:165e9.
29. Patamia I, Cappello E, Castellano-Chiodo D, Greco F, Nigro L, Cacopardo B. A human case of Hymenolepis diminuta in a child from eastern Sicily. Korean J Parasitol 2010;48:167e9. ska M, Dzika E, Dziedziech M, Poz niak H, 30. Kubiak K, Wron Leokajtis M, et al. The prevalence of intestinal parasites in children in preschools and orphanages in the WarmiaMasuria province (North-Eastern Poland). Przeglad Epidemiol 2015;69:483. 31. Małafiej E, Spiewak E. Serological investigation in children infected with Ascaris lumbricoides. Wiadomosci Parazytol 2000;47:585e90. 32. Labeaud AD, Singer MN, McKibben M, Mungai P, Muchiri EM, McKibben E, et al. Parasitism in children aged three years and under: relationship between infection and growth in rural coastal Kenya. PLoS Negl Trop Dis 2015;9:e0003721. 33. Krause RJ, Koski KG, Pons E, Sinisterra O, Scott ME. Ascaris and hookworm transmission in preschool children in rural Panama: role of subsistence agricultural activities. Parasitology 2016;143:1043e54. 34. Lili Z, Bingxiang Z, Hong T, Shuhua X, Hotez P, Bing Z, et al. Epidemiology of human geohelminth infections (ascariasis, trichuriasis and necatoriasis) in Lushui and Puer Counties, Yunnan Province, China. Southeast Asian J Trop Med Public Health 2000;31:448e53. 35. O'Lorcain P, Holland CV. The public health importance of Ascaris lumbricoides. Parasitology 2000;121(Suppl. 1):S51e71. 36. Harhay MO, Horton J, Olliaro PL. Epidemiology and control of human gastrointestinal parasites in children. Exp Rev Anti Infect Ther 2010;8:219e34. ski TH. 37. Bitkowska E, Wnukowska N, Wojtyniak B, Dzben Occurrence of intestinal parasites among children attending first classes of the elementary schools in Poland in school year 2002/2003. Przeglad Epidemiol 2004;58:295e302. 38. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, Mathewos B, et al. Soil transmitted helminths and Schistosoma mansoni infections among school children in Zarima town, northwest Ethiopia. BMC Infect Dis 2011;11:189. 39. Abossie A, Seid M. Assessment of the prevalence of intestinal parasitosis and associated risk factors among primary school children in Chencha town, Southern Ethiopia. BMC Public Health 2014;14:1. 40. Haswell-Elkins M, Elkins D, Anderson BM. The influence of individual, social group and household factors on the distribution of Ascaris lumbricoides within a community and implications for control strategies. Parasitology 1989;98:125e34. 41. Kightlinger LK, Seed JR, Kightlinger MB. Ascaris lumbricoides intensity in relation to environmental, socioeconomic, and behavioral determinants of exposure to infection in children from southeast Madagascar. J Parasitol 1998;84:480e4.