Malaria severity status in patients with soil-transmitted helminth infections

doi:10.1016/j.actatropica.2009.05.019

Acta Tropica

Volume 112, Issue 1, October 2009, Pages 8-11

https://doi.org/10.1016/j.actatropica.2009.05.019 Get rights and content

Abstract

Objective

To investigate the possible impact of soil-transmitted helminth (STH) infection on malaria severity, level of parasitaemia and clearance/reduction of Plasmodium parasites following treatment with anti-malarial drugs.

Methods

458 voluntary malaria patients who visited the Alaba Kulito Health Center, southern Ethiopia, for medical treatment in November and December 2007 were included in this study. Giemsa-stained thick and thin blood films were used for the determination of parasitaemia and identification of Plasmodium species, respectively. Stool sample was collected from these patients and diagnosed for intestinal helminths using Kato-Katz technique. Haemoglobin concentration was measured using a portable spectrophotometer (HemoCue HB 201). Malaria parasite clearance was checked on day 3 post-treatment.

Findings

The prevalence of co-infection of malaria with the major soil-transmitted helminths (STHs), i.e., with hookworm species, Ascaris lumbricoides and Trichuris trichiura was 9.6%, 6.3% and 2.1%, respectively. About 8.1% of the study subjects had severe malaria. Intensity of hookworm infection showed positive association with malaria parasite densities (F = 3.510, P = 0.033). STHs infection in general was negatively correlated with the symptoms of severe malaria (OR = 0.317, 95% CI = 0.315–0.86, P = 0.01), but a small proportion (4.5%) of malaria patients who were concurrently harboring one or more intestinal helminths had severe malaria. Only few malaria patients (2.3%) co-infected with STHs were found positive for Plasmodium parasites on day 3 post-treatment.

Conclusion

The present findings indicate that soil-transmitted helminths have very little contribution to malaria severity in co-infected individuals. The findings also indicate that STHs do not have significant impact on clearance rate of Plasmodium falciparum and Plasmodium vivax when treated with anti-malarial drugs.

Introduction

Malaria is widely co-endemic with intestinal helminth infections such as hookworm infections, ascariasis, trichuriasis and schistosomiasis, resulting in a high rate of co-infection (Adrienne et al., 2005, Brooker et al., 2006). Studies on malaria and helminth co-infections have shown contradictory results regarding severity of malaria. Infection with Ascaris lumbricoides was reported to suppress malaria symptoms including cerebral malaria (Nacher et al., 2000). The association was reported to hold true for all helminths in protecting from cerebral malaria, renal failure, jaundice and higher body temperature (Nacher et al., 2001a, Nacher et al., 2001b, Nacher et al., 2002a). Furthermore, the treatment of ascariasis has been shown to be accompanied by recrudescence of malaria attacks (Murray et al., 1978).

On the other hand, soil-transmitted helminths and Schistosoma mansoni are reported to increase the incidence of clinical malaria in children (Spigel et al., 2003, Hartgers and Yazdanbakhsh, 2006). LeHesran et al. (2004) have also shown the association between severe malaria attack and high prevalence of A. lumbricoides infection in children. Children infected either with intestinal helminths or S. haematobium are said to be more susceptible to acute malaria attacks (Jambou et al., 1998, Sokhna et al., 2004). An increased likelihood of falciparum malaria was also observed in patients with helminths in a low-transmission area (Nacher et al., 2002b). The present study was, therefore, undertaken to look at the possible impact of helminth infection on malaria severity, level of parasitaemia and clearance/reduction of Plasmodium parasites following treatment with anti-malarial drugs in Alaba Kulito, one of the malarious areas in Ethiopia.

Section snippets

Study area and population

The study was conducted at Alaba Kulito Health Center in Alaba Woreda (administrative unit), south Ethiopia, located 313 km to the south of Addis Ababa. The Woreda is semi-arid with annual temperature ranging from 18 to 23 °C and mean annual rainfall from 100 to 120 mm. Malaria and intestinal parasites are the most prevalent public health problems in the area.

The study subjects included acute febrile patients who visited the Health Center in November and December 2007 and who presented with

Malaria infection and severity

Among 1802 patients who visited Alaba Kulito Health Center, south Ethiopia, in November and December 2007, 502 (27.9%) were found positive for Plasmodium parasites and 458 subjects (233 males and 225 females) fulfilled the inclusion criteria and enrolled in the study (Table 1). The highest malaria cases were due to P. vivax (79.9%) followed by P. falciparum (15.7%). Mixed infections with P. falciparum and P. vivax were detected in 4.4% of the cases. Highest prevalence of malaria (39.2%) was

Discussion

The present study showed that only few cases of helminth and malaria co-infected patients showed signs and symptoms of severe malaria as compared with severe manifestation in patients infected with malaria parasite alone. This indicates that helminth infection provides some degree of protection against the development of severe malaria which is also in agreement with the previous reports (Nacher et al., 2000, Nacher et al., 2001a, Nacher et al., 2002a)

Light infection with A. lumbricoides was

Acknowledgements

We thank the Global Fund Programme for Malaria and Aklilu Lemma Institute of Pathobiology for financial support of the work. We are also very much indebted to Ms Kokebe Gebere-Michael, Mr Sisay Dessie and all staff of the Alaba Kulito Health Center for their technical support and laboratory facilities. We also express our gratitude to the patients who voluntarily participated in the study.

References (24)

M. Legesse et al.
Increased parasitaemia and delayed parasite clearance in Schistosoma mansoni and Plasmodium berghei co-infected mice
Acta Trop.
(2004)
J. Murray et al.
The biological suppression of malaria: an ecological and nutritional interrelationship of a host and two parasites
Am. J. Clin. Nutr.
(1978)
E. Adrienne et al.
Epidemiology of helminth infection and their relationship to clinical malaria in southwest Uganda
Trans. R. Soc. Trop. Med. Hyg.
(2005)
V. Briand et al.
Co infection with Plasmodium falciparum and Schistososma heamatobium: protective effect of Schistosomiasis on malaria in Senegalese children?
Am. J. Trop. Med. Hyg.
(2005)
S. Brooker et al.
Global epidemiology, ecology and control of soil-transmitted helminth infections
Adv. Parasitol.
(2006)
M. Cheesbrough
Parasitological Tests, District Laboratory Practices in Tropical Countries, Part I
(1998)
F.C. Hartgers et al.
Co-infection of helminths and malaria: modulation of the immune responses to malaria
Parasite Immunol.
(2006)
R. Jambou et al.
Change in response to malaria induced by repeated treatment of children with Levamisole
J.Y. LeHesran et al.
Severe malaria attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal
Trans. R. Soc. Trop. Med. Hyg.
(2004)
MOH
Malaria Diagnosis and Treatment Guide Lines for Health Workers in Ethiopia
(2004)

T.W. Mwangi et al.

Malaria and helminth interactions in humans: an epidemiological viewpoint

Ann. Trop. Med. Parasitol.

(2006)

M. Nacher et al.

Ascaris lumbricoides infection is associated with protection from cerebral malaria

Parasite Immunol.

(2000)

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Malaria severity status in patients with soil-transmitted helminth infections

Abstract

Objective

Methods

Findings

Conclusion

Introduction

Section snippets

Study area and population

Malaria infection and severity

Discussion

Acknowledgements

Acta Trop.

Am. J. Clin. Nutr.

Epidemiology of helminth infection and their relationship to clinical malaria in southwest Uganda

Trans. R. Soc. Trop. Med. Hyg.

Co infection with Plasmodium falciparum and Schistososma heamatobium: protective effect of Schistosomiasis on malaria in Senegalese children?

Am. J. Trop. Med. Hyg.

Global epidemiology, ecology and control of soil-transmitted helminth infections

Adv. Parasitol.

Parasitological Tests, District Laboratory Practices in Tropical Countries, Part I

Co-infection of helminths and malaria: modulation of the immune responses to malaria

Parasite Immunol.

Change in response to malaria induced by repeated treatment of children with Levamisole

Severe malaria attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal

Trans. R. Soc. Trop. Med. Hyg.

Malaria Diagnosis and Treatment Guide Lines for Health Workers in Ethiopia

Malaria and helminth interactions in humans: an epidemiological viewpoint

Ann. Trop. Med. Parasitol.

Ascaris lumbricoides infection is associated with protection from cerebral malaria

Parasite Immunol.