BACKGROUND: Intestinal parasitic infections remain a significant global health issue, particularly affecting poor and marginalised populations. These infections significantly contribute to children's diseases, malnutrition, poor school performance, cognitive disorders, and future economic losses. This study aimed to explore and compare the occurrence of intestinal parasites in early childhood among the group of infants from the Slovak majority population and from marginalised Roma communities (MRCs). Furthermore, it aimed to explore the health complaints of children with and without intestinal parasitic infection in the past month and assess the effect of various risk factors on the occurrence of intestinal parasitic infection in infants from MRCs. METHODS: We obtained cross-sectional data from mothers and stool samples of their children aged 13-21 months using the first wave of the longitudinal RomaREACH study. A total of 181 stools from infants were analysed: 105 infants from the Slovak majority population and 76 from MRCs. RESULTS: Infants from MRCs are significantly more often infected by Ascaris lumbricoides, Trichuris trichiura and Giardia duodenalis than their better-off peers from the majority population. Infection rates are 30% in infants from MRCs vs. 0% in the majority population (p < 0.001). Single and mixed infections were observed in children from MRCs. Infants with intestinal parasitic infections suffer significantly more often from various health complaints, particularly cough, stomach ache, irritability, and diarrhoea. Within MRCs, the risk of parasitic infections in infants is significantly increased by risk factors such as the absence of flushing toilets in households (OR = 4.17, p < 0.05) and contact with un-dewormed animals (OR = 3.61, p < 0.05). Together with the absence of running water in the household, these three factors combined increase the risk more than ten times (p < 0.01). CONCLUSION: Maintaining hygienic standards in conditions of socioeconomic deprivation in MRCs without running water and sewage in the presence of un-dewormed animals is problematic. These living conditions contribute to the higher prevalence of parasitic infections in children from MRCs, causing various health complaints and thus threatening their health and healthy development.

Department of Epidemiology Faculty of Medicine PJ Safarik University Kosice Slovakia

Department of Epizootiology and Parasitology and Protection of One Health University of Veterinary Medicine and Pharmacy in Košice Košice Slovakia

Department of Health Psychology and Research Methodology Faculty of Medicine PJ Safarik University Kosice Slovakia

Institute of Mathematics Faculty of Natural Sciences PJ Safarik University Kosice Slovakia

Olomouc University Social Health Institute Palacky University in Olomouc Olomouc Czechia Czechia

Zobrazit více v PubMed

Lustigman S, Prichard RK, Gazzinelli A, Grant WN, Boatin BA, et al. A Research Agenda for Helminth diseases of humans: intervention for control and elimination. PLOS Negl Trop Dis. 2012;6:4. doi: 10.1371/journal.pntd.0001549. PubMed DOI PMC

WORLD HEALTH ORGANIZATION (WHO). Soil-transmitted helminth infections. [online]. 2020, [cit. 2020-08-15]. Available on Internet: <https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections

EU FRA - European Union Agency for Fundamental Rights . Roma in 10 European countries: main results. Roma survey 2021. Luxembourg: Publications Office of the European Union; 2022.

Vacková J, Maňhalová J, Rolantová, Urban D. Health literacy in the Roma population. KONTAKT-Journal Nurs Social Sci Relat Health Illn 2020; 22(4).

Hajare ST, Gobena RK, Chauhan NM, Eriso F. Prevalence of intestinal parasite infections and their associated factors among food handlers working in selected catering establishments from Bule Hora, Ethiopia. Biomed Res Int. 2021 doi: 10.1155/2021/6669742. PubMed DOI PMC

Wakid MH. Intestinal parasitic infection among Food handlers in Holy City Makkah during Hajj season 1428 Hegira 2007. Med Sci. 2009;16:1. doi: 10.4197/Med.16-1.4. DOI

WORLD HEALTH ORGANIZATION (WHO). Soil-transmitted helminth infections. [online]. 2024, [cit. 2020-04-22].Available on Internet: <https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections

WORLD HEALTH ORGANIZATION (WHO). Zoonoses. [online]. 2020, [cit. 2020-12-08]. Available on Internet: <https://www.who.int/zoonoses/en/

Xiao L, Feng Y. Molecular epidemiologic tools for waterborne pathogens Cryptosporidium spp. and Giardia Duodenalis. Food Waterborne Parasitol. 2017;8:14–32. doi: 10.1016/j.fawpar.2017.09.002. PubMed DOI PMC

Certad G, Viscogliosi E, Chabé M, Cacció SM. Pathogenic mechanisms of Cryptosporidium and Giardia. Trends Parasitol. 2017;33(7):561–76. doi: 10.1016/j.pt.2017.02.006. PubMed DOI

Allain T, Buret AG. Pathogenesis and post-infectious complications in giardiasis. Adv Parasitol. 2020;107:173–99. doi: 10.1016/bs.apar.2019.12.001. PubMed DOI

Niehaus MD, Moore SR, Patrick PD, Derr LL, Lornitz DB, Lima AA, et al. Early childhood diarrhea is associated with diminished cognitive function 4 to 7 years later in children in a northeast Brazilian shantytown. ASTMH. 2002;665:590–3. doi: 10.4269/ajtmh.2002.66.590. PubMed DOI

Plutzer J, Ongerth J, Karanis P. Giardia taxonomy, phylogeny and epidemiology: facts and open questions. J Hyg Environ. 2010;213(5):321–33. doi: 10.1016/j.ijheh.2010.06.005. PubMed DOI

Dayao A, Sheoran A, Carvalho A, Xu H, Beamer G, Widmer G, et al. An immunocompetent rat model of infection with Cryptosporidium hominis and Cryptosporidium parvum. Int J Parasitol. 2020;50(1):19–22. doi: 10.1016/j.ijpara.2019.10.002. PubMed DOI

Putignani L, Menichella D. Global distribution, public health and clinical impact of the protozoan pathogen cryptosporidium. Interdiscip Perspect Infect Dis. 2010;2010:753512. doi: 10.1155/2010/753512. PubMed DOI PMC

Khalil IA, Troeger C, Rao PC, Blacker BF, Brown A, Brewer TG, et al. Morbidity, mortality, and long-term consequences associated with diarrhoea from Cryptosporidium infection in children younger than 5 years: a meta-analyses study. Lancet Glob Health. 2018;6(7):e758–68. doi: 10.1016/S2214-109X(18)30283-3. PubMed DOI PMC

Pumipuntu N, Piratae S, Cryptosporidiosis. A zoonotic disease concern. Vet World. 2018;5681–6. 10.14202/vetworld.2018.681-686 PubMed PMC

Ahmed M. Intestinal parasitic infections in 2023. Gastroenterol Res. 2023;16:127–40. doi: 10.14740/gr1622. PubMed DOI PMC

Bartsch SM, Hotez PJ, Asti L, Zapf KM, Bottazzi ME, Diemert DJ, et al. The global economic and health burden of human hookworm infection. PLoS Negl Trop Dis. 2016;e0004922. 10.9. PubMed PMC

Weatherhead JE, Hotez PJ, Meija R. The global state of helminth control and elimination in children. Clin Pediatr. 2017;64(4):867–77. doi: 10.1016/j.pcl.2017.03.005. PubMed DOI PMC

Zammarchi L, et al. Spectrum and burden of neglected tropical diseases observed in an infectious and tropical diseases unit in Florence, Italy (2000–2015) Intern Emerg Med. 2017;12:467–77. doi: 10.1007/s11739-016-1597-1. PubMed DOI

Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367:1521–32. doi: 10.1016/S0140-6736(06)68653-4. PubMed DOI

Khuroo MS, Rather AA, Khuroo NS, Khuroo MS. Hepatobiliary and pancreatic ascariasis. World J Gastroenterol. 2016;22(33):7507–17. doi: 10.3748/wjg.v22.i33.7507. PubMed DOI PMC

Gelanew T, Lalle M, Hailu A, Pozio E, Cacció SM. Molecular characterisation of human isolates of Giardia Duodenalis from Ethiopia. Acta trop. 2007;102(2):92–9. doi: 10.1016/j.actatropica.2007.04.003. PubMed DOI

Khan W, Rahman H, Rafiq N, Kabir M, Ahmed MS, Escalante PLR. Risk factors associated with intestinal pathogenic parasites in schoolchildren. Saudi J Biol Sci. 2022;42782–6. 10.1016/j.sjbs.2021.12.055 PubMed PMC

Benjamin-Chung J, Mertens A, Colford JM, et al. Early-childhood linear growth faltering in low- and middle-income countries. Nature. 2023;621:550–7. doi: 10.1038/s41586-023-06418-5. PubMed DOI PMC

Olopade BO, Idowu CO, Oyelese AO, Aboderin AO. Intestinal parasites, nutritional status and cognitive function among primary school pupils in ile-ife, Osun state, Nigeria. Afr J Infect Dis. 2018;12(2):21–8. doi: 10.21010/ajid.v12i2.4. PubMed DOI PMC

Bogitsh BJ, Carter CE, Oeltmann TN. Human parasitology. 4th Edition. Oxfort, UK: Elsevier, 2013, 430, ISBN 978-0-12-415915-0.

Deplazes P, Eckert J, Mathis A, Samson-Himmelstjerna G, Zahner H. Parasitology in Veterinary Medicine. The Netherlands, 2016, 650, ISBN 97890-8686-274-0.

Dickson R, Awasthi S, Williamson P, Demellweek C, Garner P. Effects of treatment for intestinal helminth infection on growth and cognitive performance in children: systematic review of randomised trials. BMJ. 2000;320:1697–701. doi: 10.1136/bmj.320.7251.1697. PubMed DOI PMC

Galgamuwa LS, Iddawela D, Dharmaratne SD. Prevalence and intensity of Ascaris lumbricoides infections in relation to undernutrition among children in a tea plantation community, Sri Lanka: a cross-sectional study. BMC Pediatr. 2018;13:211–21. doi: 10.1186/s12887-018-0984-3. PubMed DOI PMC

De Lima Corvino DF, Horrall S. Ascariasis. Stat Pearls (Internet). 2022. https://www.ncbi.nlm.nih.gov/books/NBK430796/ PubMed

Khalil IA, Troeger C, Rao PC, Blacker BF, Brown A, Brewer TG, et al. Morbidity, mortality, and long-term consequences associated with diarrhoea from Cryptosporidium infection in children younger than 5 years: a meta-analyses study. Lancet Glob Health. 2018;6(7):e758–68. doi: 10.1016/S2214-109X(18)30283-3. PubMed DOI PMC

Mohd-shaharuddin N, Lian Lim YA, Ngui R, Nathan S. Expression of Ascaris lumbricoides putative virulence-associated genes when infecting a human host. Parasit Vectors. 2021;14:1–12. doi: 10.1186/s13071-021-04680-y. PubMed DOI PMC

Phuphisut O, Poodeepiyasawat A, Yoonuan T, Watthanakulpanich D, Chotsiri P, Reamtong O, Mousley A, Gobert GN, Adisakwattana P. Transcriptome profiling of male and female Ascaris lumbricoides reproductive tissues. Parasit Vectors. 2022;15(1):477. doi: 10.1186/s13071-022-05602-2. PubMed DOI PMC

Kache S, et al. COVID-19 PICU guidelines: for high-and limited-resource settings. Pediatr Res. 2020;88(5):705–16. doi: 10.1038/s41390-020-1053-9. PubMed DOI PMC

Lim-leroy A, CHua TH. Prevalence and risk factors of geohelminthiasis among the rural village children in Kota Marudu, Sabah, Malaysia. PLoS ONE. 2020;15:e0239680. doi: 10.3390/jcm11102847. PubMed DOI PMC

Pullan RL, Brooker SJ. The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors. 2012;5:81. doi: 10.1186/1756-3305-5-81. PubMed DOI PMC

Else KJ, Keiser J, Holland CV, Grencis RK, Sattelle DB, Fujiwara RT, Bueno LL, Asaolu SO, Sowemimo OA, Cooper PJ. Whipworm and roundworm infections. Nat Rev Dis Primers. 2020; 28;6(1):44. 10.1038/s41572-020-0171-3. PMID: 32467581. PubMed

Brustoloni YM, Chang MR, Lyrio de Oliveira AM, Silva de Alexandre A. Trichiura eggs found in oral mucosal lesions in a child in Brazil. Parasitol Int. 2009;58:1. doi: 10.1016/j.parint.2008.09.002. PubMed DOI

Khuroo MS, Khuroo MS, Khuroo NS. Trichuris dysentery syndrome: a common cause of chronic iron deficiency anemia in adults in an endemic area (with videos) Gastrointest Endoscopy. 2010;71:200–4. doi: 10.1016/j.gie.2009.08.002. PubMed DOI

Bundy DA, Cooper ES, Thompson DE, Didier JM, Simmons I. Epidemiology and population dynamics of Ascaris lumbricoides and Trichuris trichiura infection in the same community. Trans R Soc Trop Med Hyg. 1987;81:987–93. doi: 10.1016/0035-9203(87)90372-5. PubMed DOI

Kaminsky RG, Castillo RV, Flores CA. Growth retardation and severe anemia in children with Trichuris dysenteric syndrome. Asian Pac J Trop Biomed. 2015;5:591–7. doi: 10.1016/j.apjtb.2015.05.005. DOI

Hamid MMA, Eljack IB, Osman MKM, Elaagip HA, Muneer MS. The prevalence of Hymenolepis nana among preschool children of displacement communities in Khartoum state, Sudan: a cross-sectional study. Travel Med Infec Dis. 2015;13(2):172–7. doi: 10.1016/j.tmaid.2014.12.011. PubMed DOI

Dahmana H, Granjon L, Diagne C, Davoust B, Fenollar F, Mediannikov O. Rodents as hosts of pathogens and related zoonotic disease risk. Pathogens. 2020;10:202. doi: 10.3390/pathogens9030202. PubMed DOI PMC

Jarošová J, Antolová D, Šnábel V, Miklisová D, Cavallero S. The dwarf tapeworm Hymenolepis Nana in Pet rodents in Slovakia—epidemiological survey and genetic analysis. Parasitol Res. 2020;119:519–27. doi: 10.1007/s00436-019-06565-7. PubMed DOI

Dold Ch, Holland CV. Ascaris and ascariasis. Microbes Infect. 2011;13:632–7. doi: 10.1016/j.micinf.2010.09.012. PubMed DOI

Drake LJ, Jukes MCH, Sternberg RJ, Bundy DAP. Geohelminth infections (ascariasis, trichuriasis, and hookworm): cognitive and developmental impacts. Semin Pediatr Infect Dis. 2000;245–51. 10.1053/spid.2000.9638

GBD. Mortality and Causes of Death Collaborators Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980–2015: a systematic analysis for the global burden of Disease Study 2015. Lancet. 2016;388:1459–544. doi: 10.1016/S0140-6736(16)31012-1. PubMed DOI PMC

Tchuem Tchuenté LA. Control of soil-transmitted helminths in sub-saharan Africa: diagnosis, drug efficacy concerns and challenges. Acta Trop. 2011;120:4–11. doi: 10.1016/j.actatropica.2010.07.001. PubMed DOI

Ministry of the Interior of Slovak Republic. Atlas of Roma communities. (2019). http://www.minv.sk/?atlas-romskych-komunit-2019. March 20, 2022.

Kolarcik P, Madarasova Geckova A, Orosova O, van Dijk JP, Reijneveld SA. Predictors of health-endangering behaviour among Roma and non-roma adolescents in Slovakia by gender. JECH. 2010;64(12):1043–8. PubMed

Madarasova Geckova A, Babinska I, Bobakova D, Dankulincova Veselska Z, Bosakova L, Kolarcik P. Socioeconomic characteristics of the Population Living in Roma Settlements and Their Association with Health and Health-related Behaviour. CEJPH. 2014;22:57–64. doi: 10.21101/cejph.a3903. PubMed DOI

Garcia. 2016.

Cotton JA, Beatty JK, Buret AG. Host parasite interactions and pathophysiology in Giardia infections. Int J Parasitol. 2011;419:925–33. doi: 10.1016/j.ijpara.2011.05.002. PubMed DOI

Gelanew T, Lalle M, Hailu A, Pozio E, Cacció SM. Molecular characterisation of human isolates of Giardia Duodenalis from Ethiopia. Acta trop. 2007;102(2):92–9. doi: 10.1016/j.actatropica.2007.04.003. PubMed DOI

Perruccci S, Berrilli F, Procopio C, Di Filippo MM, Pierini A, Marchetti A. Giardia duodenalis infection in dogs affected by primary chronic enteropathy. Open Vet J. 2020;10(1):74–9. doi: 10.4314/ovj.v10i1.12. PubMed DOI PMC

Scorza AV, Ballweber LR, Tangtrongsup S, Panuska C, Lappin MR. Comparisons of mammalian Giardia duodenalis assemblages based on the β-giardin, glutamate dehydrogenase and triose phosphate isomerase genes. Vet Parasitol. 2012;189(2–4):182–8. doi: 10.1016/j.vetpar.2012.04.032. PubMed DOI

Homan WL, Mank, Theo G. Human giardiasis: genotype linked differences in clinical symptomatology. Int J Parasitol. 2001;31(8):822–6. doi: 10.1016/s0020-7519(01)00183-7. PubMed DOI

Muadica AS, Koster PC, Dashti A, Bailo B, Hernandéz de Mingo M, Reh L, et al. Molecular diversity of Giardia Duodenalis, Cryptosporidium spp. and Blastocystis sp. in asymptomatic school children in Leganés, Madrid (Spain) Microorganism. 2020;8(4):466. doi: 10.3390/microorganisms8040466. PubMed DOI PMC

Łanocha A, Lanocha –Arendarczyk N, Wilczýnska D, Zdziarska B. Kosik –Bogacka D. Protozoan intestinal parasitic infection in patients with hematological malignancies. J Clin Med. 2022;11:2847. doi: 10.3390/jcm11102847. PubMed DOI PMC

Rudohradská P, et al. Prevalence of intestinal parasites in children from minority group with low hygienic standards in Slovakia. Helminthologia. 2012;49:63–6. doi: 10.2478/s11687-012-0013-2. DOI

Štrkolcová G, Goldová M, Bocková E, Mojžišová J. The roundworm Strongyloides Stercoralis in children, dogs, and soil inside and outside a segregated settlement in Eastern Slovakia: frequent but hardly detectable parasite. Parasitol Res. 2017;116:891–900. doi: 10.1007/s00436-016-5362-1. PubMed DOI

Štrkolcova G, Mravcová K, Barbušinová E, Mucha R, Várady M, Goldová M. Prevalence of intestinal parasites in Children living in various living conditions in Slovakia. J Paediatr Child Health. 2019;174–85. 10.26502/jppch.74050028

Pipíkova J, Papajová I, Šoltýs J, Schusterová I, Kočišová D, Tothayová A. Segregated settlements present an increased risk for the parasite infections spread in Northeastern Slovakia. Helminthologia. 2017;53(3):199–210. doi: 10.1515/helm-2017-0026. DOI

Šmigová J, Šnábel V, Cavallero S, Šmiga Ľ, Šoltys J, Papaj J, Papajová I. Neglected diseases-parasitic infections among Slovakian children from different populations and genotypes of Giardia Duodenalis. Microorganisms. 2022;6(2):381. doi: 10.3390/microorganisms10020381. PubMed DOI PMC

Giacometti A, Cirioni O, Fortuna M, Osimani P, Antonicelli L, Del Prete MS, et al. Environmental and serological evidence for the presence of toxocariasis in the urban area of Ancona, Italy. Eur J Epidemiol. 2000;16:1023–6. doi: 10.1023/A:1010853124085. PubMed DOI

Martínez-Moreno FJ, Hernandéz S, López-Cobes E, Becerra C, Acosta L, Martinéz- Moreno A. Estimation of canine intestinal parasites in Cordoba (Spain) and their risk to public health. Vet Parasitol. 2007;143(1):7–13. doi: 10.1016/j.vetpar.2006.08.004. PubMed DOI

Garzon DL. Contributing factors to preschool unintentional injury. J Pediatr Nurs. 2005;206:441–7. doi: 10.1016/j.pedn.2005.03.014. PubMed DOI

Steketee RW. Pregnancy, nutrition and parasitic diseases. Nutr J. 2003;1335:S1661–7. doi: 10.1093/jn/133.5.1661S. PubMed DOI