Comparative analysis of poliovirus-specific IgA and cytokine levels in the sera of Ascaris lumbricoides-infected and helminth-negative Nigerian children after oral poliovirus vaccination

Abstract

Background: Intestinal helminth infection is associated with altered immune responses and compromised vaccine efficacy in infected children. Altered immune response due to Ascaris lumbricoides infection may compromise efficacy of oral poliovirus vaccination in children. There is no information on humoral immune response during oral poliovirus (OP) vaccination of A. lumbricoides–infected Nigerian children. The objective of this study is to determine the serum levels of cytokines (tumour necrosis factor–alpha TNF-α, interferongamma IFN–γ, interleukins -4, -6, -8, -10) and poliovirus-specific IgA (PV-IgA) antibody in children infected with A. lumbricoides compared with helminth-negative children (control) before and after oral poliovirus vaccination.
 Methodology: Twenty-three A. lumbricoides-infected children between ages 5-15 years (13 males and 10 females) and 23 age (4-15 years) and sex-matched helminth-negative children who met selection criteria were enrolled into the study after ethical approval and informed consent. Their stool samples were examined for helminth ova using concentration technique. Sera were collected before and 3 weeks after OP vaccinations, and serum concentrations of IFN–γ, TNF–α, IL-4, -6, -8, -10, and poliovirus-specific IgA concentrations were determined by enzyme-linked immunosorbent assay. The level of statistical significance was set at α0.05.
 Results: Pre-vaccination serum levels of IFN–γ, IL–4, IL-6 and IL-8 were significantly higher in A. lumbricoides–infected children compared with pre-vaccination levels in helminth-negative children. Postvaccination serum levels of IFN–γ, IL–4 and IL-8 were significantly higher in A. lumbricoides–infected children compared with post-vaccination serum levels in helminth-negative children. In the A. lumbricoides-infected children, pre-vaccination serum levels of IL-6 and IL-8 were significantly higher compared with post vaccination levels while pre-vaccination serum levels of IFN–γ, IL–4 and IL-8 were significantly higher in helminth-negative children compared with the post-vaccination levels. There was no significant reduction in post-vaccination median serum level of PV-IgA compared with level before vaccination in A. lumbricoides-infected children. Also, there was no significant increase in post-vaccination median serum level of PV-IgA compared with level before vaccination in helminth-negative children.
 Conclusion: Oral polio vaccine administration caused decrease expression of inflammatory cytokines (IL-6 and IL-8) in A. lumbricoides-infected school children, and A. lumbricoides infection may reduce PV-IgA production following OP vaccination.
 Keywords: Ascaris lumbricoides infection, cytokines, children, poliovirus vaccination

The effect of helminth infection on vaccine responses in humans and animal models: A systematic review and meta‐analysis

“…One article each identified for rubella, 15 meningococcal 39 and cholera 39 vaccines showed no association with helminth infection status. We found one article on the effect of direct helminth exposure on live, oral polio vaccine which reported lower responses among uninfected compared to infected individuals 40 . Similarly, findings from two articles reporting on the effect of prenatal helminth exposure on live, oral polio vaccine suggested lower responses among children of mothers without helminths (SMD −0.24, 95% CI −0.33 to −0.14 and I 2 = 0.01%).…”

“…We found one article on the effect of direct helminth exposure on live, oral polio vaccine which reported lower responses among uninfected compared to infected individuals. 40 Similarly, findings from two articles reporting on the effect of prenatal helminth exposure on live, oral polio vaccine suggested lower responses among children of mothers without helminths (SMD À0.24, 95% CI À0.33 to À0.14 and I 2 = 0.01%). The only study we found on live, oral rotavirus also reported significantly lower response levels in children born to helminth uninfected compared to infected mothers.…”