|Year : 2015 | Volume
| Issue : 2 | Page : 76-80
Differential effects of age and intestinal helminthiasis on positivity rate of skin prick reaction to environmental allergens among Nigerians
Edem Victory Fabian, Arinola Olatunbosun Ganiyu
Department of Chemical Pathology, College of Medicine, University of Ibadan, Ibadan, Nigeria
|Date of Web Publication||5-Aug-2015|
Arinola Olatunbosun Ganiyu
Department of Chemical Pathology, Immunology Unit, College of Medicine, University of Ibadan, Ibadan
Source of Support: None, Conflict of Interest: None
Background: Skin prick testing (SPT) conventionally used to investigate immediate type (type 1) hypersensitivity to allergens is reported to be affected by varying factors. It is hypothesized by present study that immunomodulation of T-cell by parasitic helminthic infection may affect skin prick reaction.
Study Objectives: The primary objective of this cross-sectional study is to determine the prevalence of intestinal helminthiasis and its effect on the outcome of SPT to environmental allergens.
Participants, Materials and Methods: Skin prick test was performed on 296 residents (113 adults and 183 children) rural and urban parts of Ibadan, South-West Nigeria. Stool specimen was also collected and examined for ova, cyst and larvae of intestinal worms.
Results and Conclusion: The prevalence of intestinal helminthiasis was 20.8% and 21.2% in children and adults respectively. Prevalence of intestinal helminthiasis in adults from rural settings was significantly higher when compared with adults from urban settings. Significantly higher positive skin test to dog allergen was observed in helminth infected participants when compared to uninfected participants. Furthermore, significantly higher positive skin test to cockroach, mite, mold, and mouse allergen was observed in adults when compared to children. This suggests that the intestinal helminthiasis is found among all age groups in this region, but do not affect skin reaction to environmental allergens as much as ages of participants.
Keywords: Age, environmental allergen, helminthiasis, hypersensitivity, skin prick reaction
|How to cite this article:|
Fabian EV, Ganiyu AO. Differential effects of age and intestinal helminthiasis on positivity rate of skin prick reaction to environmental allergens among Nigerians. J Med Trop 2015;17:76-80
|How to cite this URL:|
Fabian EV, Ganiyu AO. Differential effects of age and intestinal helminthiasis on positivity rate of skin prick reaction to environmental allergens among Nigerians. J Med Trop [serial online] 2015 [cited 2022 Oct 4];17:76-80. Available from: https://www.jmedtropics.org/text.asp?2015/17/2/76/162289
| Introduction|| |
Skin prick test (SPT) is recommended as the initial method to test for sensitization to environmental and food allergens.  The principle of SPT which is also used to investigate type 1 hypersensitivity to allergens,  is based on Th-2 immune response in which allergen-specific IgE are produced by plasma cells upon subsequent exposure to allergen. Though the method is safe, relatively inexpensive and rapid,  previous studies reported that SPT is affected by some factors such as drugs,  age, quality of testing reagents, testing devices, the part of the body utilized for testing  and skin pigmentation.  The primary aim of the present study is to find out if intestinal helminth will affect the outcome of SPT, thus screening for sensitization to environmental and food allergens.
In developing countries, intestinal helminths are known to be endemic due to gross environmental pollution, poor environmental sanitation, poor sanitary habits, and inappropriate management of waste, particularly fecal matter. These led to increasing prevalence of Ascaris, Trichuris, Taenia species and hookworm.  Helminth infections, though rarely fatal, may impair growth, physical fitness, cognition, and reduce performance and productivity.  Furthermore, helminth infection has been reported to modulate host immune system  which may hamper immune responses of the host to other agents.
The host immune response mounted to helminth infection is characterized by T-helper type 2 (Th-2) response, which was thought to be protective against these parasites.  However, there is accumulating evidence that these parasites enhance their survival by modulating the immune response of their host, inducing regulatory responses that dampen activity of effector cells.  This produces immune effector cell hyporesponsiveness, which is not only directed toward parasite antigens, but seems to extend to bystander antigens,  a mechanism that has been postulated as a means by which chronic helminth infection protects against allergic and autoimmune diseases. 
Allergens like helminth antigens are potent inducers of Th-2 responses characterized by increased levels of immunoglobulin IgE, tissue eosinophilia and mastocytosis along with preferential secretion of Th-2 cytokines,  and it is known that allergic diseases including asthma, eczema and rhinitis are associated with Th-2 inflammation. , Nonetheless, despite the close parallels between immune responses that characterize helminths infection and allergic diseases, the clinical outcome with respect to immediate hypersensitivity and inflammation is clearly not the same. ,
Allergies and helminthiasis stimulate similar Th-2 based immune mechanism. Helminth infection is possible in populations where screening for allergic reaction to environmental and food allergens is carried out. Our present study is therefore designed to provide information on prevalence of helminthiasis in a heterogenous population of children and adults in Ibadan, as well as examine the influence of helminthiasis and age on skin prick responses to environmental allergens.
| Participants, Materials and Methods|| |
A total of 296 residents of Ibadan, South-West Nigeria were recruited for this cross-sectional study. Those on treatment with antihistamine drugs or oral corticosteroid within 3 months prior to recruitment, those with history and findings suggestive of skin diseases, chronic pulmonary diseases, cardiovascular diseases, renal and hepatic diseases were excluded from this study. The study group comprised of 113 adults and 183 children who were apparently healthy individuals. The children recruited for this study were between 6 and 14 years of age whereas the adults were between 23 and 41 years of age. Each study participant was supplied with a labeled screw-cap polystyrene bottle with spatula to collect stool sample. Informed consent was obtained from adults, and parents of children recruited for this study.
Skin Prick Test
Skin prick test reactivity to common environmental allergen was tested with extracts of cat, dog, grass, cockroach, mango, mite, mold and mouse (Greer Lenoir, USA). A histamine positive control and saline negative control was used to reduce false positives and negatives. SPT was done on the volar side of the lower arm using skin prick lancets. The wheal size was measured after 20 min. Skin prick reactivity was considered positive when the longest diameter of wheal size was greater than or equal to 3 mm.
Stool Microbes Analysis
Fecal samples were examined for helminths in the laboratory by formol ether concentration method as previously described. 
Statistical analysis was performed using SPSS 17.0 (SPSS Inc., Chicago, Illinois, USA). Prevalence of intestinal worm in the study population was calculated, and Chi-square analysis was used to test proportions and prevalence of helminth infection.
| Results|| |
The total prevalence of helminthiasis in the study population was 21.3%, with Ascaris lumbricoides having the highest prevalence (13.9%) while Trichuris trichuria had the least prevalence (0.3%) [Table 1]. When the study population was subdivided into children and adults, the prevalence of helminthiasis was 20.8% and 21.2% in children and adults respectively [Table 1]. In children, A. lumbricoides had the highest prevalence (15.8%), followed by hookworm (4.9%), Taenia (1.1%) and T. trichuria (0.5%) [Table 1]. Taenia had the highest prevalence (10.6%) in adults, followed by A. lumbricoides (9.7%) and hookworm (3.5%) [Table 1].
|Table 1: Percentage prevalence of intestinal helminthiasis in study participants|
Click here to view
A significantly higher percentage of adults from a rural setting were infected with intestinal helminth when compared to adults from an urban setting [Table 2]. Nonetheless, there was no significant difference in percentage prevalence of intestinal helminthiasis in children from rural setting when compared with children from urban setting [Table 2].
|Table 2: Percentage prevalence of intestinal helminthiasis in study population classified by age group and setting|
Click here to view
Percentage skin test positivity to dog allergen was significantly higher in participants with intestinal helminthiasis when compared with participants without intestinal helminthiasis [Table 3]. There were no significant differences in percentages of skin test positivity to cat, grass, cockroach, mango, mite, mold and mouse allergens in helminth infected participants when compared with uninfected participants [Table 3].
|Table 3: Percentage positivity of environmental allergen in helminths infected and uninfected participants|
Click here to view
Percentage positivity of SPT to cockroach, mite, mold and mouse allergens were significantly higher in adults when compared with children [Table 4]. There were no significant differences in percentages of skin test positivity to cat, dog, grass and mango allergens in adults when compared with children [Table 4].
|Table 4: Percentage positivity of environmental allergen in children and adults|
Click here to view
| Discussion|| |
The term "This wormy world" was put forward in 1947 by Stoll to reflect the high prevalence of helminth infections in the then-global population of 2.2 billion people.  Though there has been a reduction in prevalence of helminth infection in industrialized countries, approximately one-quarter of the world's population is still infected with worms.  In Nigeria, parasitic worm infections are still of public health concern with much intervention strategies drawn toward eradication of childhood worm infections. This present study observed an overall percentage prevalence of 21.3%, with a 20.8% and 21.2% prevalence in children and adults respectively. This result represents a decline in the prevalence of intestinal helminth infections in Nigerian children resident in Ibadan, South-West Nigeria, as previous reports of helminthiasis in Nigerian children had percentage prevalence ranging from 30.2% to 74%. ,,,,
Nonetheless, despite the decline in childhood helminthiasis observed, the pattern of helminth infections in this study was in concert with previous studies, which reported that A. lumbricoides was the dominant helminth infection in Nigerian children. ,,, Sequel to the WHO consultation in 2002, much attention has been given to helminth infection in children compared with adults as a measure for helminths control and eradication.  This study observed a higher percentage prevalence of helminthiasis in adults than in children (21.2% and 20.8% respectively), with a significant percentage of infected adults in rural areas compared to urban areas. Higher prevalence of intestinal helminth infection in rural adults compared with urban adults may be related to socioeconomic status. Most adults in rural areas are farmers, kept in close relation with pets (dogs, goats, cats and chickens) and living in sub-standard hygienic conditions. Higher prevalence of intestinal helminthiasis in adults from a rural setting when compared with adults from an urban setting also supports previous reports.  Furthermore, the difference in the prevalence of intestinal helminthiasis in adults compared with children may also be due to increased school-based deworming programs in these regions.
Epidemiological studies have pointed to a higher frequency of allergies in economically developed countries than in developing countries. ,, This trend of increased prevalence of allergic diseases in industrialized countries has been explained by the hygiene hypothesis, which posits that decreased exposure to childhood infections through improvements in hygiene and greater access to antibiotics and vaccines alter host response to environmental allergens.  Such improved hygiene has been considered to alter the balance between helper T-cell type 1 (Th-1) and type 2 (Th-2) immune responses due to failure of immune regulation resulting in allergy-mediated Th 2 responses. 
Helminths infection which is more common in developing countries has also been reported to protect against development of allergic diseases by various mechanisms. ,,, The present study found a significantly higher proportion of SPT positivity to dog allergen in helminth infected participants when compared with uninfected participants. This supports the study of Olopade et al.  who reported significant positive correlation between the presence of Taenia in stool and skin test positivity to house-dust mites and mold in a population of adult asthmatics in South-West Nigeria. It also supports increased serum IgE in Nigerian children with helminthic infection as reported by Arinola et al.,  due to the well-known role of IgE in skin sensitivity testing. Although some studies have reported lower allergic propensity in helminth infected cohorts, ,,,, these were not carried out on Nigerian population. In addition, dog ownership was previously associated with, and identified as a risk factor for A. lumbricoides infection in a population of Nigerian children.  Traub et al.  also demonstrated that dogs were significant disseminators and environmental contaminators of A. lumbricoides. This may explain the observed significant increase in SPT positivity to dog allergen in intestinal helminth infected participants compared with uninfected participants.
The present study found significantly increased prevalence of positive SPT in adults when compared to children. This may be related to longer years of exposure of adults to environmental allergens compared with children. Our result is contrary to previous studies that reported age-related decrease in skin test positivity in a population of healthy participants , and a population of asthmatics and/or rhinitics. , These differences may be due to the age range of study participants, as elderly subjects (≥60 years) were included in these other studies but were not included in this present study. Nonetheless, the result of this study is similar to the findings of Barbee et al.  who reported peak prevalence of allergen positivity in individual aged 20-34 years compared to other age groups. This buttresses the need for consideration of age in interpretation of SPT results in allergic disease diagnosis.
| Conclusion|| |
Our data provide evidence that parasitic worm infections are found among all ages in this region. However, this did not affect skin response to environmental allergens as much as ages of the participants. This presents evidence of the need for further investigation of the "hygiene hypothesis" and screening for sensitization to environmental and food allergens in this region.
| Acknowledgment|| |
The authors would like to acknowledge Prof. Olopade C.O., Department of Medicine and the Center for Global Health, University of Chicago, Chicago, USA, for the gift of SPT kits.
| References|| |
Bernstein IL, Li JT, Bernstein DI, Hamilton R, Spector SL, Tan R, et al.
Allergy diagnostic testing: An updated practice parameter. Ann Allergy Asthma Immunol 2008;100:S1-148.
Berger A. Skin prick testing. BMJ 2002;325:414.
Kwong KY, Jean T, Redjal N. Variability in measurement of allergen skin testing results among allergy-immunology specialists. J Allergy Ther 2014;5:160.
McCann WA, Ownby DR. The reproducibility of the allergy skin test scoring and interpretation by board-certified/board-eligible allergists. Ann Allergy Asthma Immunol 2002;89:368-71.
Campo P, Kalra HK, Levin L, Reponen T, Olds R, Lummus ZL, et al.
Influence of dog ownership and high endotoxin on wheezing and atopy during infancy. J Allergy Clin Immunol 2006;118:1271-8.
WHO. Deworming for health and development. Report of the Third Global Meeting of the Partners for Parasite Control. Geneva, Switzerland: World Health Organization; 2005.
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.
Smits HH, Everts B, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections protect against allergic diseases by active regulatory processes. Curr Allergy Asthma Rep 2010;10:3-12.
Grencis RK, Hültner L, Else KJ. Host protective immunity to Trichinella spiralis in mice: Activation of Th cell subsets and lymphokine secretion in mice expressing different response phenotypes. Immunology 1991;74:329-32.
Flohr C, Tuyen LN, Quinnell RJ, Lewis S, Minh TT, Campbell J, et al.
Reduced helminth burden increases allergen skin sensitization but not clinical allergy: A randomized, double-blind, placebo-controlled trial in Vietnam. Clin Exp Allergy 2010;40:131-42.
Cooper PJ. Interactions between helminth parasites and allergy. Curr Opin Allergy Clin Immunol 2009;9:29-37.
Royer PJ, Emara M, Yang C, Al-Ghouleh A, Tighe P, Jones N, et al.
The mannose receptor mediates the uptake of diverse native allergens by dendritic cells and determines allergen-induced T cell polarization through modulation of IDO activity. J Immunol 2010;185:1522-31.
Arinola GO, Oluwole O, Oladokun R, Adedokun BO, Olopade OI, Olopade CO. Intestinal helminthic infection increases serum levels of IL-2 and decreases serum TGF-beta levels in Nigerian asthmatic patients. Open J Immunol 2014;4:1-8.
Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 2002;296:490-4.
Olopade CO, Arinola OG, Ige OM, Falade AG, Falusi AG, Aderemi T, et al
. Atopy, helminthic infection and serum immunoglobulins in adult asthma in SW Nigeria. A30 Asthma: Clinical Studies/Thematic Poster. Am J Respir Crit Care Med 2009;179:A1293.
Yazdanbakhsh M, van den Biggelaar A, Maizels RM. Th2 responses without atopy: Immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol 2001;22:372-7.
Arinola OG. Immunological aspects of urinary schistosomiasis in Ibadan, Southwestern Nigeria. Ann Ibadan Postgrad Med 2005;3:69-73.
Stoll NR. This wormy world 1947. J Parasitol 1999;85:392-6.
Fallon PG, Mangan NE. Suppression of TH2-type allergic reactions by helminth infection. Nat Rev Immunol 2007;7:220-30.
Arinola OG, Yaqub AS, Rahamon KS. Reduced serum Ige level in Nigerian children with helminthiasis compared with protozoan infection: Implication on hygiene hypothesis. Ann Biol Res 2012;3:5754-7.
Damen JG, Lar P, Mershak P, Mbaawuga EM, Nyary BW. A comparative study on the prevalence of intestinal helminthes in dewormed and non-dewormed students in a rural area of North-central Nigeria. Lab Med 2010;41:586-9.
Ekundayo OJ, Aliyu MH, Jolly PE. A review of intestinal helminthiasis in Nigeria and the need for school-based intervention. J. Rural Trop Public Health 2007;6:33-9.
Oninla SO, Owa JA, Onayade AA, Taiwo O. Intestinal helminthiases among rural and urban schoolchildren in south-western Nigeria. Ann Trop Med Parasitol 2007;101:705-13.
Salako AA. Effects of portable water availability on intestinal parasitism among rural school children with sewage disposal facilities in the Mjidun and Owulu sub-urban community of Lagos state. Niger Med Pract 2001;39:30-5.
Kirwan P, Asaolu SO, Abiona TC, Jackson AL, Smith HV, Holland CV. Soil-transmitted helminth infections in Nigerian children aged 0-25 months. J Helminthol 2009;83:261-6.
Arinola O, Fawole O. Age and sex graded helminth infections in a Nigerian village. East Afr Med J 1995;72:110-2.
Ikeh E, Obadofin M, Brindeiro B, Baugher C, Frost F, Vanderjagt D, et al
. Intestinal parasitism in rural and urban areas of north central Nigeria: An Update.
Internet J Microbiol 2005;2:1-12.
Maizels RM. Infections and allergy - Helminths, hygiene and host immune regulation. Curr Opin Immunol 2005;17:656-61.
Worldwide variation in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema: ISAAC. The International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee. Lancet 1998;351:1225-32.
Strachan DP. Hay fever, hygiene, and household size. BMJ 1989;299:1259-60.
Matricardi PM, Bonini S. High microbial turnover rate preventing atopy: A solution to inconsistencies impinging on the hygiene hypothesis? Clin Exp Allergy 2000;30:1506-10.
McSorley HJ, Maizels RM. Helminth infections and host immune regulation. Clin Microbiol Rev 2012;25:585-608.
Rodrigues LC, Newcombe PJ, Cunha SS, Alcantara-Neves NM, Genser B, Cruz AA, et al.
Early infection with Trichuris trichiura
and allergen skin test reactivity in later childhood. Clin Exp Allergy 2008;38:1769-77.
Smits HH, Yazdanbakhsh M. Chronic helminth infections modulate allergen-specific immune responses: Protection against development of allergic disorders? Ann Med 2007;39:428-39.
Mingomataj EC, Xhixha F, Gjata E. Helminths can protect themselves against rejection inhibiting hostile respiratory allergy symptoms. Allergy 2006;61:400-6.
Rujeni N, Nausch N, Bourke CD, Midzi N, Mduluza T, Taylor DW, et al.
Atopy is inversely related to schistosome infection intensity: A comparative study in Zimbabwean villages with distinct levels of Schistosoma haematobium
infection. Int Arch Allergy Immunol 2012;158:288-98.
Araujo MI, de Carvalho EM. Human schistosomiasis decreases immune responses to allergens and clinical manifestations of asthma. Chem Immunol Allergy 2006;90:29-44.
van den Biggelaar AH, Rodrigues LC, van Ree R, van der Zee JS, Hoeksma-Kruize YC, Souverijn JH, et al.
Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren. J Infect Dis 2004;189:892-900.
Medeiros M Jr, Figueiredo JP, Almeida MC, Matos MA, Araújo MI, Cruz AA, et al. Schistosoma mansoni
infection is associated with a reduced course of asthma. J Allergy Clin Immunol 2003;111:947-51.
Traub RJ, Robertson ID, Irwin P, Mencke N, Thompson RC. The role of dogs in transmission of gastrointestinal parasites in a remote tea-growing community in northeastern India. Am J Trop Med Hyg 2002;67:539-45.
Kerkhof M, Dubois AE, Postma DS, Schouten JP, de Monchy JG. Role and interpretation of total serum IgE measurements in the diagnosis of allergic airway disease in adults. Allergy 2003;58:905-11.
Wüthrich B, Schindler C, Medici TC, Zellweger JP, Leuenberger P. IgE levels, atopy markers and hay fever in relation to age, sex and smoking status in a normal adult Swiss population. SAPALDIA (Swiss Study on Air Pollution and Lung Diseases in Adults) Team. Int Arch Allergy Immunol 1996;111:396-402.
Karakaya G, Kalyoncu AF. The natural course of atopy determined by skin prick tests in patients with bronchial asthma and/or rhinitis. Allergol Immunopathol (Madr) 2006;34:257-62.
Eriksson NE, Holmen A. Skin prick tests with standardized extracts of inhalant allergens in 7099 adult patients with asthma or rhinitis: Cross-sensitizations and relationships to age, sex, month of birth and year of testing. J Investig Allergol Clin Immunol 1996;6:36-46.
Barbee RA, Brown WG, Kaltenborn W, Halonen M. Allergen skin-test reactivity in a community population sample: Correlation with age, histamine skin reactions and total serum immunoglobulin E. J Allergy Clin Immunol 1981;68:15-9.
[Table 1], [Table 2], [Table 3], [Table 4]