Epidemiological and clinical correlates of malaria-helminth co-infections in southern Ethiopia
© Mulu et al.; licensee BioMed Central Ltd. 2013
Received: 4 January 2013
Accepted: 23 June 2013
Published: 3 July 2013
In many areas of the world, including Ethiopia, malaria and helminths are co-endemic, therefore, co-infections are common. However, little is known how concurrent infections affect the epidemiology and/or pathogenesis of each other. Therefore, this study was conducted to assess the effects of intestinal helminth infections on the epidemiology and clinical patterns of malaria in southern Ethiopia where both infections are prevalent.
A cross-sectional study was conducted in 2006 at Wondo Genet Health Center and Bussa Clinic, southern Ethiopia. Consecutive blood film positive malaria patients (N=230) and malaria negative asymptomatic individuals (N=233) were recruited. Malaria parasite detection and quantification was diagnosed using Giemsa-stained thick and thin blood films, respectively. Helminths were detected using direct microscopy and formol-ether concentration techniques. Coarse quantification of helminths ova was made using Kato Katz method.
The over all magnitude of intestinal parasitic infection was high irrespective of malaria infection (67% among malaria positive patients versus 53.1% among malaria non-infected asymptomatic individuals). Trichuris trichiura infection was associated with increased malaria prevalence while increased worm burden of helminths as expressed by egg intensity was associated with increased malaria parasitaemia which could be a potential factor for development of severe malarial infection with the course of the disease. Majority (77%) of the subjects had multiple helminths infection. T. trichiura, Ascaris lumbricoides, Schistosoma mansoni, and hookworm infestation accounted for 64.5, 57.7 %, 28.4%, and 12.2% of the infections, respectively.
Populations in malaria-endemic areas of southern Ethiopia are multi-parasitized with up to four helminths. Mass deworming may be a simple practical approach in endemic areas in reducing the risk of severe malarial attack particularly for those at high risk of both infections.
KeywordsMalaria Helminthic infections Co-infection Ethiopia
Half the world’s population live in malaria-endemic areas, with an estimated 500 million clinical cases and over one million deaths annually . Similarly, malaria is ranked as the leading communicable disease in Ethiopia, accounting for about 30% of the overall disability adjusted life years lost. Approximately 68% of the total population lives in areas at risk of malaria . In Ethiopia, Plasmodium falciparum and Plasmodium vivax are the major parasites accounting for about 70% and 30% of infections, respectively, during peak transmission periods [3, 4].
Soil-transmitted helminths (STH), on the other hand, are a group of common parasites that infect more than a billion people worldwide . In Ethiopia, like other developing countries, infections with the major STH, including Ascaris lumbricoides, Trichuris trichiura, hookworm and Schistosoma mansoni are widely spread with variable prevalences [6–12]. In many areas of the world, malaria and STH are co-endemic, therefore co-infections are common, particularly in Africa [13, 14]. The rate of malaria and STH co-infection in Ethiopia as reported in one study was 9.6%, 6.3% and 2.1% with hookworms, A. lumbricoides and T. trichiura, respectively . In another study a 2.8% prevalence of urinary schistosomiasis and P. falciparum malaria was reported .
However, how concurrent infections affect the epidemiology and/or the pathogenesis of each other remains controversial [17–19] raging from increased severity of malaria to reduced severity and incidence of malaria during helminths co-infection [20–33]. The underlying reason for such different outcomes might be due to numerous factors, including differences in study design and case definition, data analysis and interpretation, the demonstration of antigen cross-reactivity between co-infecting organisms and host factors . Studies on the impact of helminths on incidence, prevalence and severity of malaria in Ethiopia where both infections are hyperendemic is lacking. Therefore, this study was conducted to assess the effects of STH on the epidemiological and clinical patterns of malaria in a hyper-endemic area for both malaria and helminths infections.
This cross-sectional study was conducted at Wondo Genet Health Center and Busssa Clinic, Sidama Administrative Zone, South Ethiopia in a peak transmission season from November to December 2006. These areas are malaria endemic with high prevalence of helminthiasis. All patients presenting with signs and symptoms of malaria during the study period were included (N=230) and asymptomatic individuals with negative result for malaria (N=233). A pretested, structured questionnaire was used to collect socio-demographic and relevant clinical data of the participants.
Diagnosis of malaria
Both thick and thin blood films were made in a single slide and were stained with Giemsa staining solution for detection and quantification of malaria parasites. To detect malaria infections, 200 fields (the equivalent of 0.5μl of thick blood film) were examined. The parasite density was expressed per μl of blood assuming 8,000 leucocytes per μl of blood. In brief, a thick fill was selected where the white blood cells were evenly distributed. Using the oil immersion objective, 200 white blood cells were counted systematically, by counting at the same time the number of parasites (asexual form only) in each field covered. Then the number of parasite per μl of blood was calculated by multiplying the number of parasite (asexual stages) counted against 200 leucocytes and 8,000 leucocytes and dividing the product by 200 . After clinical examination and laboratory findings, patients were categorized in to different clinical forms of malaria (uncomplicated, severe and complicated cerebral malaria) following the national protocol [MOH, Standard Malaria Diagnosis and Treatment Guideline, 2004].
Malaria patients and their counter part controls were requested to deliver stool specimen. Those who volunteered to deliver the specimen were given a clean, dry, leak-proof plastic. Stool samples were then examined by direct stool examination method using normal saline. The portion of stool was processed by using the Kato Katz technique; about 3 g stool was preserved by 10% formalin for formol-ether sedimentation techniques. Coarse quantification of eggs was obtained by counting the number of eggs on a smear of 41.7 mg faeces, and a quantitative variable scoring (light infection/low worm burden, moderate infection/medium worm burden and heavy infection/massive worm burden) was created for each helminths following the standard procedure used by World Health Organization (WHO) [34, 35]. Packed red cell volume was determined using the conventional methods following the standard protocol.
The data were analysed using to SPSS version 13 statistical packages software. Intestinal parasite densities were transformed to log for analysis and geometric mean was used. Baseline characteristics and malaria parasites densities of groups with and without intestinal parasitic infections was compared by Student’s t test and ANOVA. Two-tailed P values was determined and considered significant when found <0.05. Logistic regression analysis was also used to determined association between variables.
This study was conducted after institutional (Aklilu Lemma Institute of Pathobiology, Addis Ababa University) and regional (Southern Nation and Nationalist Regional State Health Department) ethical clearance was obtained and after written and/or verbal informed consent was obtained from the study participants. Participants who were found to be positive for any of the parasites were linked to the health institutions for treatment.
A total of 230 patients with malaria infection and 233 malaria negative individuals were included. The mean (±SD, range) age of the subjects was not similar in both groups [17.8 (±14.15) versus 19 + 12.23. The majority (34.5%) of the participants were under nine years of age, and 54% of the subjects were males.
Prevalence and intensity of helminths infection
Prevalence and intensity of Trichuris trichiura, Ascaris lumbricoides, Schistosoma mansoni and hookworm in different age groups
No positive for parasites (%)
EPG † (corresponding 95 % CI)
Intensity of infection for T. trichiura, A. lumbricoides and S. mansoni by age group and sex
Status of Helminths infection §
Distribution of malaria parasite by age and sex
P. falciparum and P. vivax
Plasmodium falciparum parasitaemia (per μl of blood) in relation helminths infection status
Prevalence of intestinal helminths among malaria positive and negative individuals
Type of helminth infection
OR (95% CI) #
Approximately 68% of the total population of Ethiopia lives in areas at risk of malaria . According to the World Malaria Report in 2011, Ethiopia was categorized among the four countries with a 25 to 50% reduction in new malaria cases . However, despite the continuous efforts made to control malaria during the past decade, infections with malaria remained high in many parts of the country . The current study in Wendo Genet reflected the same notion, with a very high prevalence rate of malaria. Most of the malaria infections were caused by P. falciparum (58.3%) while P. vivax and mixed infections accounted for 35.2% and 6.5% of the infections, respectively. The persistently high prevalence of malaria urges a need for evaluation of the malaria control programme in the study area. In Ethiopia, A. lumbricoides, T. trichiura, hookworm, and S. mansoni infections are widespread with variable prevalence that may reach up to 90% in some places among the general population [6–12]. Likewise, the most predominant intestinal helminths diagnosed were T. trichiura, A. lumbricoides, S. mansoni and hookworm, with a prevalence of 64.5%, 57.7%, 28.4% and 12.2%, respectively. The high prevalence of helminthiasis in general and the predominance of specific parasites in the area were in agreement with previous reports in the region [8, 37].
In many tropical areas of the world, malaria and STH co-exist with significant co-infection rates [13, 14]. This was reflected by the high co-infection rates observed in the current study (67%) which is consistent with studies from other tropical countries from Africa and Asia [29, 31]. Higher rate of severe malaria attack among individuals co-infected with helminths as compared with those free from helminths was the reported from Thailand . However, African study from Uganda failed to show such association even in heavily infected individuals . In this study, trichuriasis that was found to be significantly associated with increased malaria infection. Schistosoma mansoni was not associated with increased malaria infection in the current study. This, however, contradicts the report from Senegal where the incidence rate of malaria attacks was significantly higher among S. mansoni-infected individuals . On the other hand, a study in Nigeria reported that periodic deworming of children with A. lumbricoides has protective effect from malaria infection . This implies prior infection with A. lumbricoides is a risk factor for malaria infection. In line with this, although it did not reach to a statistical significance level, there was a high A. lumbricoides- malaria co-infection rate in the current study. However, it is difficult to strongly conclude the epidemiological interaction of helminths and malaria infection with such cross-sectional study. Hence, it would be useful to check the incidence of malaria in a longitudinal study among cohorts of people having/not having different helminthiasis with and without treatment. Conducting further studies on the co-epidemiology of malaria and helminths in Ethiopia could be of paramount importance to a potential public health value of synergistic opportunities for control.
The current study however, tried to determine the effect of helminths co-infection on the clinical manifestation of the malaria cases with only three cases presenting with sign and symptoms of severe malaria. The absence of severe malaria cases in highly ‘wormy’ malaria patients in the current study was, however, consistent with a study conducted by Nacher et al.  where helminths infection was associated with protection from cerebral malaria. However, a strong association between worm burden as expressed by egg intensity and malaria parasite density was observed which suggest that with the time course of the infection, such patients with high density of both helminths and malaria will tend to develop severe form of clinical malaria by influencing the immune response during co-infection [27, 39]. Studies have reported a positive correlation between egg load of helminth infection and Plasmodium density [13, 18]. In line with this, the current study found that individuals with light T. trichiura and A. lumbricoides infections had lower Plasmodium densities than those with moderate or heavy infection. Contrary to this, heavy S. mansoni infection was associated with lower Plasmodium densities . However, the effect of specific helminths on the severity of malaria and the mechanisms leading to this needs to be determined in longitudinal studies in a larger pool of clinical cases of malaria.
The majority of malaria patients in the current study were found to be multi-parasitized with up to four helminths. A strong association between worm burden as expressed by helminths egg intensity and malaria parasite density was observed which could be a dose-dependent risk factor for severe malaria attack with the course of the infection. Mass deworming may be simple practical approaches in endemic areas in reducing the risk of severe malarial attack particularly for those at high risk of both infections.
We thank the Institute of Pathobiology, Addis Ababa University and University of Gondar for funding the project. Our special thanks and appreciation also goes to all the study participants who voluntarily participate in this study.
- WHO: World Malaria Report 2008. 2008, Geneva: World Health OrganizationGoogle Scholar
- Malaria Operational Plan Ethiopia FY2011.Google Scholar
- Tulu NA: Malaria. The Ecology of Health and Disease in Ethiopia. Edited by: Kloos H, Zein AZ. 1993, Boulder, USA: Westview Press Inc, 341-352. 2Google Scholar
- WHO: World Malaria Report 2010. 2011, Geneva: World Health OrganizationGoogle Scholar
- Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ: Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006, 67: 1521-1532.View ArticleGoogle Scholar
- Tadesse G: The prevalence of intestinal helminthic infections and associated risk factors among school children in Babile town, Eastern Ethiopia. Ethiopian J Health Dev. 2005, 19: 140-147.View ArticleGoogle Scholar
- Legesse M, Erko B: Prevalence of intestinal parasites among school children in a rural area close to south east of Lake Langano, Ethiopia. Ethiopian J Health Dev. 2004, 18: 116-120.Google Scholar
- Erko B, Medhin G: Human helminthiasis in wendo genet, southern Ethiopia with emphasis on geohelminthiasis. Ethiopian Med J. 2003, 41: 333-344.Google Scholar
- Jemaneh L: Comparative prevalence of some common intestinal helminths infections in different altitudinal regions in Ethiopia. Ethiopian Med J. 1998, 36: 1-8.Google Scholar
- Roma B, Worku S: Magnitude of S. mansoni and intestinal helminthic infections among school children in Wondo Genet Zuria, Southern Ethiopia. Ethiopian J Health Dev. 1997, 11: 125-129.Google Scholar
- Tadesse Z, Hailemariam A, Kolaczinski JH: Potential for integrated control of neglected tropical diseases in Ethiopia. Trans R Soc Trop Med Hyg. 2008, 102: 213-214. 10.1016/j.trstmh.2007.09.005.View ArticlePubMedGoogle Scholar
- Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, Mathewos B, Birhan W, Gebretsadik S, Gelaw B: Soil transmitted helminths and schistosoma mansoni infections among school children in zarima town, northwest Ethiopia. BMC Infect Dis. 2011, 11: 189-10.1186/1471-2334-11-189.PubMed CentralView ArticlePubMedGoogle Scholar
- Briand V, Watier L, Le Hesran J, Garcia A, Cot M: Coinfection with Plasmodium falciparum and Schistosoma haematobium: protective effect of schistosomiasis on malaria in Senegalese children. Am J Trop Med Hyg. 2005, 72: 702-707.PubMedGoogle Scholar
- Helmby H, Kullberg M, Troye Blomberg M: Altered immune response in mice with concomitant Schistosoma mansoni and Plasmodium chabaudi infections. Infect Immun. 1998, 66: 5167-5174.PubMed CentralPubMedGoogle Scholar
- Degarege A, Animut A, Legesse M, Erko B: Malaria severity status in patients with soil-transmitted helminth infections. Acta Trop. 2009, 112: 8-11. 10.1016/j.actatropica.2009.05.019.View ArticlePubMedGoogle Scholar
- Zinaye T, Ketema D, Beyene P: Urinary schistosomiasis and malaria associated anemia in Ethiopia. Asian Pacific J Trop Biomed. 2013, 3: 307-310. 10.1016/S2221-1691(13)60068-4.View ArticleGoogle Scholar
- Sokhna C, Le Hesran JY, Mbaye PA, Akiana J, Camara P, Diop M, Ly A, Druilhe P: Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malar J. 2004, 3: 43-10.1186/1475-2875-3-43.PubMed CentralView ArticlePubMedGoogle Scholar
- Nacher M, Gay F, Singhasivanon P, Krudsood S, Treeprasertsuk S, Mazier D, Vouldoukis I, Looareesuwan S: Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunol. 2000, 22: 107-113. 10.1046/j.1365-3024.2000.00284.x.View ArticlePubMedGoogle Scholar
- Mitchell AJ, Hansen AM, Hee L, Ball HJ, Potter SM, Walker JC, Hunt NH: Early cytokine production is associated with protection from murine cerebral malaria. Infect Immun. 2005, 73: 5645-5653. 10.1128/IAI.73.9.5645-5653.2005.PubMed CentralView ArticlePubMedGoogle Scholar
- Helmby H, Bickle Q: Immune modulation by helminth infections. Parasite Immunol. 2006, 28: 479-481. 10.1111/j.1365-3024.2006.00912.x.View ArticlePubMedGoogle Scholar
- Turner JD, Faulkner H, Kamgno J, Cormont F, Van Snick J, Else KJ, Grencis RK, Behnke JM, Boussinesq M, Bradley JE: Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J Infect Dis. 2003, 188: 1768-1775. 10.1086/379370.View ArticlePubMedGoogle Scholar
- Pierrot C, Adam E, Hot D, Lafitte S, Capron M, George JD, Khalife J: Contribution of T cells and neutrophils in protection of young susceptible rats from fatal experimental malaria. J Immunol. 2007, 178 (3): 1713-1722.View ArticlePubMedGoogle Scholar
- Nacher M, Singhasivanon P, Traoe B, Vannaphan S, Gay F, Chindanond D, Francois J, Mazier D, Looareesuwan S: Helminths infection are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand. Am J Trop Med Hyg. 2002, 66: 304-309.PubMedGoogle Scholar
- Yaman FM, Mokela D, Genton B, Rockett KA, Alpers MP, Clark IA: Association between serum levels of reactive nitrogen intermediates and coma in children with cerebral malaria in Papua New Guinea. Trans R Soc Trop Med Hyg. 1996, 90: 270-273. 10.1016/S0035-9203(96)90243-6.View ArticlePubMedGoogle Scholar
- Murray MJ, Murray AB, Murray MB, Murray CJ: Parotid enlargement, forehead edema and suppression of malaria as nutritional consequences of ascariasis. Am J Clin Nutrition. 1977, 30: 2117-2121.Google Scholar
- Murray J, Murray A, Murray M, Murray C: The biological suppression of malaria: an ecological and nutritional interrelationship of a host and two parasites. Am J Clin Nutrition. 1978, 31: 1363-1366.Google Scholar
- Nacher M, Singhasivanon P, Traore B, Dejvorakul S, Phumartanaprapin W, Looareesuwan S, Gay F: Hookworm infection is associated with decreased body temperature during mild Plasmodium falciparum malaria. Am J Trop Med Hyg. 2001, 65: 131-137.Google Scholar
- Hesran J, Akiana J, Ndiaye EI, Dia M, Senghor P, Konate L: Severe malarial attack is associated with high prevalence of Ascaris lumbricoides infection among children in rural Senegal. Trans R Soc Trop Med Hyg. 2004, 98: 397-399. 10.1016/j.trstmh.2003.10.009.View ArticlePubMedGoogle Scholar
- Shapiro AE, Tukahebwa EM, Kasten J, Clarke SE, Magnussen P, Olsen A, Kabatereine NB, Ndyomugyenyi R, Brooker S: Epidemiology of helminths infections and their relationship to clinical malaria in southwest Uganda. Trans R Soc Trop Med Hyg. 2005, 99: 18-24. 10.1016/j.trstmh.2004.02.006.View ArticlePubMedGoogle Scholar
- Kelly-Hope LA, Diggle PJ, Rowlingson BS, Gyapong JO, Kyelem D, Coleman M, Thomson MC, Obsomer V, Lindsay SW, Hemingway J, Molyneux DH: Negative spatial association between lymphatic filariasis and malaria in West Africa. Trop Med Int Health. 2006, 11: 129-135. 10.1111/j.1365-3156.2005.01558.x.View ArticlePubMedGoogle Scholar
- Nacher M, Sighasivanon P, Yimsamran S, Manibunyong W, Thanyavanich N, Wuthisen P, Looareesuwan S: Intestinal helminths infection are associated with increased incidence of Plasmodium falciparum malaria in Thailand. J Parasitol. 2002, 88: 55-58.View ArticlePubMedGoogle Scholar
- Mutapi F, Ndhlovn PD, Hagan P, Woolhouse ME: Anti Schistosome antibody responses in children coinfected with malaria. Parasite Immunol. 2000, 22: 207-208. 10.1046/j.1365-3024.2000.00288.x.View ArticlePubMedGoogle Scholar
- Diallon TO, Remoue F, Schacht AM, Charrier N, Dompnier JP, Pillet S, Garraud O, N’ Diaye AA, Capron M, Riveau G: Schistosomiasis coinfection in humans influences inflammatory markers in uncomplicated Plasmodium falciparum malaria. Parasite Immunol. 2004, 26: 365-369. 10.1111/j.0141-9838.2004.00719.x.View ArticleGoogle Scholar
- Cheesbrough M: District laboratory practice in tropical countries. 1998, Cambridge: Part I. Cambridge University Press, 191-239.Google Scholar
- WHO Expert Committee: Prevention and control of Schistosomiasis and soil transmitted helminthiasis. World Health Org Tech Rep Ser. 2002, 912: 1-57.Google Scholar
- Sharew B, Legesse M, Animut A, Jima D, Medhin G, Erko B: Evaluation of the performance of CareStart malaria Pf/Pv combo and paracheck Pf tests for the diagnosis of malaria in wondo genet, southern Ethiopia. Acta Trop. 2009, 111: 321-324. 10.1016/j.actatropica.2009.05.014.View ArticlePubMedGoogle Scholar
- Terefe A, Shimelis T, Mengistu M, Hailu A, Erko B: Schistosomiasis mansoni and soil-transmitted helminthiasis in Bushulo village, southern Ethiopia. Ethiopian Journal of Health Development. 2011, 25: 46-50.View ArticleGoogle Scholar
- Kirwan P, Jackson AL, Asaolu SO, Molloy SF, Abiona TC, Bruce MC, Ranford-Cartwright L, O’ Neill SM, Holland CV: Impact of repeated four-monthly anthelmintic treatment on Plasmodium infection in preschool children: a double-blind placebo-controlled randomized trial. BMC Infect Dis. 2010, 10: 277-10.1186/1471-2334-10-277.PubMed CentralView ArticlePubMedGoogle Scholar
- Elliott AM, Mawa PA, Joseph S, Namujju PB, Kizza M, Nakiyingi JS, Watera C, Dunne DW, Whitworth JA: Association between helimnth infection and CD4+ T cells count, viral load and cytokine response in HIV infected Ugandan adults. Trans R Soc Trop Med Hyg. 2003, 97: 103-108. 10.1016/S0035-9203(03)90040-X.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.