The impact of soil transmitted helminth on malaria clinical presentation and treatment outcome: A case control study among children in Bagamoyo district, coastal region of Tanzania.


Journal

PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488

Informations de publication

Date de publication:
12 Aug 2024
Historique:
received: 12 03 2024
accepted: 29 07 2024
medline: 12 8 2024
pubmed: 12 8 2024
entrez: 12 8 2024
Statut: aheadofprint

Résumé

Parasitic infectious agents rarely occur in isolation. Epidemiological evidence is mostly lacking, and little is known on how the two common parasites Plasmodium and soil transmitted helminths (STH) interact. There are contradictory findings in different studies. Synergism, antagonism and neutral effect have been documented between Plasmodium and STH. This study investigated the impact of STH on clinical malaria presentation and treatment outcome. A matched case control study with a semi longitudinal follow up according to World Health Organization (WHO) antimalarial surveillance guideline was done among children aged 2 months to 9 years inclusively living in western rural areas of Bagamoyo, coastal region of Tanzania. Cases were children with uncomplicated and severe malaria enrolled from the health facilities while controls were children with asymptomatic Plasmodium parasitemia enrolled from the same community. In simple conditional regression analysis there was a tendency for a protective effect of STH on the development of clinical malaria [OR = 0.6, 95% CI of 0.3-1.3] which was more marked for Enterobius vermicularis species [OR = 0.2, 95% CI of 0.0-0.9]. On the contrary, hookworm species tended to be associated with increased risk of clinical malaria [OR = 3.0, 95% CI of 0.9-9.5]. In multiple conditional regression analysis, the overall protective effect was lower for all helminth infection [OR = 0.8, 95% CI of 0.3-1.9] but remained significantly protective for E. vermicularis species [OR = 0.1, 95% CI of 0.0-1.0] and borderline significant for hookworm species [OR = 3.6, 95% CI of 0.9-14.3]. Using ordinal logistic regression which better reflects the progression of asymptomatic Plasmodium parasitemia to severe malaria, there was a 50% significant protective effect with overall helminths [OR = 0.5, 95% CI of 0.3-0.9]. On the contrary, hookworm species was highly predictive of uncomplicated and severe malaria [OR = 7.8, 95% (CI of 1.8-33.9) and 49.7 (95% CI of 1.9-1298.9) respectively]. Generally, children infected with STH had higher geometric mean time to first clearance of parasitemia. The findings of a protective effect of E. vermicularis and an enhancing effect of hookworms may explain the contradictory results found in the literature about impact of helminths on clinical malaria. More insight should be gained on possible mechanisms for these opposite effects. These results should not deter at this stage deworming programs but rather foster implementation of integrated control program for these two common parasites.

Sections du résumé

BACKGROUND BACKGROUND
Parasitic infectious agents rarely occur in isolation. Epidemiological evidence is mostly lacking, and little is known on how the two common parasites Plasmodium and soil transmitted helminths (STH) interact. There are contradictory findings in different studies. Synergism, antagonism and neutral effect have been documented between Plasmodium and STH. This study investigated the impact of STH on clinical malaria presentation and treatment outcome.
METHODS METHODS
A matched case control study with a semi longitudinal follow up according to World Health Organization (WHO) antimalarial surveillance guideline was done among children aged 2 months to 9 years inclusively living in western rural areas of Bagamoyo, coastal region of Tanzania. Cases were children with uncomplicated and severe malaria enrolled from the health facilities while controls were children with asymptomatic Plasmodium parasitemia enrolled from the same community.
RESULTS RESULTS
In simple conditional regression analysis there was a tendency for a protective effect of STH on the development of clinical malaria [OR = 0.6, 95% CI of 0.3-1.3] which was more marked for Enterobius vermicularis species [OR = 0.2, 95% CI of 0.0-0.9]. On the contrary, hookworm species tended to be associated with increased risk of clinical malaria [OR = 3.0, 95% CI of 0.9-9.5]. In multiple conditional regression analysis, the overall protective effect was lower for all helminth infection [OR = 0.8, 95% CI of 0.3-1.9] but remained significantly protective for E. vermicularis species [OR = 0.1, 95% CI of 0.0-1.0] and borderline significant for hookworm species [OR = 3.6, 95% CI of 0.9-14.3]. Using ordinal logistic regression which better reflects the progression of asymptomatic Plasmodium parasitemia to severe malaria, there was a 50% significant protective effect with overall helminths [OR = 0.5, 95% CI of 0.3-0.9]. On the contrary, hookworm species was highly predictive of uncomplicated and severe malaria [OR = 7.8, 95% (CI of 1.8-33.9) and 49.7 (95% CI of 1.9-1298.9) respectively]. Generally, children infected with STH had higher geometric mean time to first clearance of parasitemia.
CONCLUSION CONCLUSIONS
The findings of a protective effect of E. vermicularis and an enhancing effect of hookworms may explain the contradictory results found in the literature about impact of helminths on clinical malaria. More insight should be gained on possible mechanisms for these opposite effects. These results should not deter at this stage deworming programs but rather foster implementation of integrated control program for these two common parasites.

Identifiants

pubmed: 39133750
doi: 10.1371/journal.pntd.0012412
pii: PNTD-D-24-00378
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0012412

Informations de copyright

Copyright: © 2024 Salim Masoud et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Auteurs

Nahya Salim Masoud (N)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.
Department of Pediatrics and Child Health, Muhimbili University Health and Allied Sciences (MUHAS), Dar es Salaam, United Republic of Tanzania.
Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland.
University of Basel, Basel, Switzerland.

Stefanie Knopp (S)

Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland.
University of Basel, Basel, Switzerland.

Nicole Lenz (N)

Food Microbial Systems, Risk Assessment and Mitigation Group, Agroscope, Bern, Switzerland.

Omar Lweno (O)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.

Ummi Abdul Kibondo (U)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.

Ali Mohamed (A)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.

Tobias Schindler (T)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.
University of Basel, Basel, Switzerland.
Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, Basel, Switzerland.

Julian Rothen (J)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.
University of Basel, Basel, Switzerland.
Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, Basel, Switzerland.

John Masimba (J)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.

Alisa S Mohammed (A)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.

Fabrice Althaus (F)

Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland.
Health Unit, International Committee of the Red Cross (ICRC), Geneva, Switzerland.

Salim Abdulla (S)

Bagamoyo Research and Training Centre, Ifakara Health Institute, Bagamoyo, United Republic of Tanzania.

Marcel Tanner (M)

Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland.
University of Basel, Basel, Switzerland.

Claudia Daubenberger (C)

University of Basel, Basel, Switzerland.
Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, Basel, Switzerland.

Blaise Genton (B)

Department of Ambulatory Care and Community Medicine, University of Lausanne, Lausanne, Switzerland.

Classifications MeSH