ORIGINAL ARTICLES

Effects of soil-transmitted nematode infection on wheezing, asthma, and skin prick test positivities in rural preschool children

  • LI Fang ,
  • WANG Shufang ,
  • HE Pengfei ,
  • XU Shuhui
Expand
  • 1 Department of Microbial Immunology Teaching and Research Office, Yuncheng Nursing College, Yuncheng 044000, Shanxi, China
    2 Department of Preventive Medicine, Yuncheng Nursing College, Yuncheng 044000, Shanxi, China
    3 Department of Physical Examination, Yuncheng Central Hospital, Yuncheng 044000, Shanxi, China
    4 Department of Clinical Laboratory Teaching and Research, Tropical Medical College, Hainan Medical College, Haikou 570100, China

Received date: 2022-10-28

  Revised date: 2023-03-28

  Online published: 2023-06-25

Abstract

Objective To investigate the effects of soil-transmitted nematode infection of mother and child on wheezing, asthma, and skin prick test (SPT) positive in rural preschool children. Methods Preschool children and their mohers in rural area were enrolled respectively, who underwent physical examination in the Yuncheng Central Hospital outpatient sector from April 2020 to March 2021. Basic information of mothers and children and children’s wheezing/asthma condition were collected through questionnaires. Fecal samples were collected from participants, and examined for soil-transmitted nematode eggs by the Kato-Katz thick smaear method, The SPT test was performed for children to collect allergic and atopic data. Multivariate unconditional logistic regression analysis was used to explore the relevant factors affecting asthma, wheezing, and SPT positivity in children. Results In this study, there were 2 014 children and their mothers each. The infection rate of soil-transmitted nematodes among the mothers was 14.40% (290/2 014), and among the preschool children was 7.99% (161/2 014). There were 117 children had wheezing symptoms, with an occurrence rate of 5.81% (117/2 014); 149 cases had asthma, with an occurrence rate of 7.40% (149/2 014) and 304 cases were positive for SPT, with a positive rate of 15.09% (304/2 014). Premature infants, mothers with a history of allergies, and family members smoking are risk factors for wheezing in children (P < 0.05, OR > 1); female gender and complete breastfeeding are protective factors for wheezing in children (P < 0.05, OR < 1). Mothers with a history of allergies, having someone smoking at home, and planting flowers and plants at home are risk factors for childhood asthma (P < 0.05, OR > 1); female and complete breastfeeding are protective factors for childhood asthma (P < 0.05, OR < 1). Mothers with a history of allergies is a risk factor for SPT positivity in children (P < 0.05, OR > 1), while the gender of the child, presence of soil-transmitted nematode infection in the child, and presence of soil-transmitted nematode infection in the mother are protective factors for SPT positivity in children (P < 0.05, OR < 1). Conclusion Mothers and children infected with soil-transmitted nematode may reduce the occurrence of allergic diseases in children.

Cite this article

LI Fang , WANG Shufang , HE Pengfei , XU Shuhui . Effects of soil-transmitted nematode infection on wheezing, asthma, and skin prick test positivities in rural preschool children[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2023 , 41(3) : 336 -343 . DOI: 10.12140/j.issn.1000-7423.2023.03.012

References

[1] Kowalczyk K, K?ape? T. Contamination of soil with eggs of geohelminths Ascaris spp., Trichuris spp., Toxocara spp. in Poland-potential source of health risk in farmers[J]. Ann Parasitol, 2020, 66(4): 433-440.
[2] Wu YF, Wei F, Chen QH, et al. Analysis of monitoring results of soil-borne nematode disease in Jianhe County of Guizhou in 2016[J]. Chin J Endem, 2018, 37(12): 1002-1005. (in Chinese)
  (吴运凤, 卫芳, 陈清花, 等. 2016年贵州省剑河县土源性线虫病监测结果分析[J]. 中华地方病学杂志, 2018, 37(12): 1002-1005.)
[3] Aemiro A, Menkir S, Tegen D, et al. Prevalence of soil-transmitted helminthes and associated risk factors among people of Ethiopia: a systematic review and meta-analysis[J]. Infect Dis (Auckl), 2022, 15: 11786337211055437.
[4] Brummaier T, Tun NW, Min AM, et al. Burden of soil-transmitted helminth infection in pregnant refugees and migrants on the Thailand-Myanmar border: results from a retrospective cohort[J]. PLoS Negl Trop Dis, 2021, 15(3): e0009219.
[5] Meng S, Sun C, Ye RX, et al. Evaluation of the effectiveness of prevention and control of soil borne nematode infections in children in underdeveloped rural areas of the Yi ethnic group in Liangshan Prefecture, Sichuan Province based on a dual difference model[J]. Chin J Parasitol Parasit Dis, 2019, 37(2): 183-188, 195. (in Chinese)
  (孟莎, 孙畅, 叶睿雪, 等. 基于双重差分模型对四川省凉山州彝族欠发达农村地区儿童土源性线虫感染防治效果评价[J]. 中国寄生虫学与寄生虫病杂志, 2019, 37(2): 183-188, 195.)
[6] Hotez PJ. Toxocariasis: a neglected infection for the Anthropocene epoch[J]. Adv Parasitol. 2020, 109: 879-883.
[7] Jin W, Guo JD, Zhang SQ, et al. Distribution and risk factors of soil-transmitted nematode diseases in Anhui Province[J]. Chin J Dis Control Prev, 2018, 22(10): 1041-1045. (in Chinese)
  (金伟, 郭见多, 张世清, 等. 安徽省土源性线虫病流行特征及相关因素分析[J]. 中华疾病控制杂志, 2018, 22(10): 1041-1045.)
[8] Hu B, Chen GZ, Huang P. Epidemiology related to soil-borne nematode disease in Danzhou City, Hainan Province[J]. Chin J Epidemiol, 2018, 39(4): 474-477. (in Chinese)
  (胡波, 陈国志, 黄平. 海南省儋州市2013—2016年人群感染土源性线虫状况分析[J]. 中华流行病学杂志, 2018, 39(4): 474-477.)
[9] Zhang YN, Li GH, Liu Y, et al. Report on surveillance of soil-transmittednematodeinfections in Shanxi Province in 2011[J]. Int J Med Parasit Dis, 2013(1): 25-28. (in Chinese)
  (张玉农, 李国华, 刘元, 等. 山西省2011年土源性线虫病监测报告[J]. 国际医学寄生虫病杂志, 2013(1): 25-28.)
[10] Takeuchi H, Alfazal Khan M, Zaman K, et al. Classification of wheezing children in rural Bangladesh by intensity of Ascaris infection, total and specific IgE levels, history of pneumonia, and other risk factors[J]. J Immunol Res, 2019, 2019: 4236825.
[11] Chico ME, Vaca MG, Rodriguez A, et al. Soil-transmitted helminth parasites and allergy: observations from Ecuador[J]. Parasite Immunol, 2019, 41(6): e12590.
[12] Cooper PJ, Chico ME, Vaca MG, et al. Effect of early-life geohelminth infections on the development of wheezing at 5 years of age[J]. Am J Respir Crit Care Med, 2018, 197(3): 364-372.
[13] Cooper PJ, Chis Ster I, Chico ME, et al. Impact of early life geohelminths on wheeze, asthma and atopy in Ecuadorian children at 8 years[J]. Allergy, 2021, 76(9): 2765-2775.
[14] Sousa-Santos ACAF, Moreno AS, Santos ABR, et al. Parasite infections, allergy and asthma: a role for tropomyosin in promoting type 2 immune responses[J]. Int Arch Allergy Immunol, 2020, 181(3): 221-227.
[15] Mohammadzadeh I, Rostami A, Darvish S, et al. Exposure to Ascaris lumbricoides infection and risk of childhood asthma in north of Iran[J]. Infection, 2019, 47(6): 991-999.
[16] Martin I, Kaisar MMM, Wiria AE, et al. The effect of gut microbiome composition on human immune responses: an exploration of interference by helminth infections[J]. Front Genet, 2019, 10: 1028.
[17] Zakzuk J, Casadiego S, Mercado A, et al. Ascaris lumbricoides infection induces both, reduction and increase of asthma symptoms in a rural community[J]. Acta Trop, 2018, 187: 1-4.
[18] Mohammed SH, Jabbr AS, Ibrahim NK. Impact of parasitic infection with Ascaris lumbricoides on pulmonary function tests in asthmatic and non-asthmatic children[J]. Respir Med Case Rep, 2021, 34: 101552.
[19] Dos S Jesus T, Dos S Costa R, Alcantara-Neves NM, et al. Variants in the CYSLTR2 are associated with asthma, atopy markers and helminths infections in the Brazilian population[J]. Prostaglandins Leukot Essent Fatty Acids, 2019, 145: 15-22.
[20] Wang J, Huang Y, Zhang XL, et al. An analysis of skin prick test reactivity to dustmite in overweight and normal weight children with allergic asthma before and after specific immunotherapy[J]. Chin J Contemp Pediatr, 2016, 18(4): 329-334. (in Chinese)
  (王健, 黄英, 张学莉, 等. 超重与正常体重过敏性哮喘儿童特异性免疫治疗前后尘螨皮肤点刺试验强度分析[J]. 中国当代儿科杂志, 2016, 18(4): 329-334.)
[21] Abera D, Wordofa M, Mesfin A, et al. Intestinal helminthic infection and allergic disorders among school children enrolled in mass deworming program, Sululta, Ethiopia[J]. Allergy Asthma Clin Immunol, 2021, 17(1): 43.
[22] Caraballo L, Zakzuk J, Acevedo N. Helminth-derived cystatins: the immunomodulatory properties of an Ascaris lumbricoides cystatin[J]. Parasitology, 2021: 1-13.
[23] Pitrez PM, Gualdi LP, Barbosa GL, et al. Effect of different helminth extracts on the development of asthma in mice: the influence of early-life exposure and the role of IL-10 response[J]. Exp Parasitol, 2015, 156: 95-103.
[24] Alcantara-Neves NM, Veiga RV, Ponte JCM, et al. Dissociation between skin test reactivity and anti-aeroallergen IgE: determinants among urban Brazilian children[J]. PLoS One, 2017, 12(3): e0174089.
[25] Sanya RE, Nkurunungi G, Hoek Spaans R, et al. The impact of intensive versus standard anthelminthic treatment on allergy-related outcomes, helminth infection intensity, and helminth-related morbidity in lake Victoria fishing communities, Uganda: results from the LaVIISWA cluster-randomized trial[J]. Clin Infect Dis, 2019, 68(10): 1665-1674.
[26] Mkhize-Kwitshana ZL, Naidoo P, Nkwanyana NM, et al. Concurrent allergy and helminthiasis in underprivileged urban South African adults previously residing in rural areas[J]. Parasite Immunol, 2022, 44(4/5): e12913.
[27] Brandt O, Wegenstein B, Müller I, et al. Association between allergic sensitization and intestinal parasite infection in schoolchildren in Gqeberha, South Africa[J]. Clin Exp Allergy, 2022, 52(5): 670-683.
[28] Staal SL, Hogendoorn SKL, Voets SA, et al. Prevalence of atopy following mass drug administration with albendazole: a study in school children on Flores Island, Indonesia[J]. Int Arch Allergy Immunol, 2018, 177(3): 192-198.
[29] Beckmann J, Lang C, du Randt R, et al. Prevalence of stunting and relationship between stunting and associated risk factors with academic achievement and cognitive function: a cross-sectional study with South African primary school children[J]. Int J Environ Res Public Health, 2021, 18(8): 4218.
[30] Lim-Leroy A, Chua TH. Prevalence and risk factors of geohelminthiasis among the rural village children in Kota Marudu, Sabah, Malaysia[J]. PLoS One, 2020, 15(9): e0239680.
[31] Sadowska N, Tomza-Marciniak A, Juszczak M. Soil contamination with geohelminths in children’s play areas in Szczecin, Poland[J]. Ann Parasitol, 2019, 65(1): 65-70.
[32] Khan W, Khatoon N, Arshad S, et al. Evaluation of vegetables grown in dry mountainous regions for soil transmitted helminths contamination[J]. Braz J Biol, 2021, 82: e238953.
Outlines

/

〈 〉