- Research article
- Open Access
Prevalence and clinical correlates of Schistosoma mansoni co-infection among malaria infected patients, Northwest Ethiopia
BMC Research Notes volume 8, Article number: 480 (2015)
In Ethiopia, where malaria and schistosomiasis are co-endemic, co-infections are expected to be high. However, data about the prevalence of malaria-schistosomiasis co-infection and their clinical correlation is lacking. Therefore, the aim of this study was to assess prevalence of Schistosoma mansoni co-infection and associated clinical correlates in malaria patients.
A cross-sectional study was conducted in 2013 at Chwahit Health Center, in northwest Ethiopia. Blood film positive malaria patients (N = 205) were recruited for the study. Clinical, parasitological, hematological, and biochemical parameters were assessed from every study participant. Stool samples were also collected and processed with Kato-Katz technique to diagnose and classify intensity of Schistosoma mansoni.
The prevalence of Schistosoma mansoni and malaria co-infection was 19.5 %. The age group of 16–20 years old was significantly associated with co-infection. Co-infected patients with a moderate-heavy egg burden of Schistosoma mansoni had significantly high mean Plasmodium parasitemia. On the other hand, age group of 6–10 years old and moderate-heavy Schistosoma mansoni co-infection were significantly associated with severe malaria.
Prevalence of malaria and Schistosoma mansoni co-infection in the study area was considerably high. Severity of malaria and parasitemia of Plasmodium were associated with certain age groups and intensity of concurrent Schistosoma mansoni. Further study is needed to explore the underlying mechanisms of interaction between malaria and Schistosoma mansoni.
Malaria is a complex and deadly parasitic disease caused by genus Plasmodium. Plasmodium falciparum (P. falciparum) and Plasmodium vivax (P. vivax) are the predominant species globally attributing to the majority of disease burden. According to World Malaria Report 2013, there were an estimated 207 million episodes and 627,000 deaths due to malaria in 2012, of which approximately 80 % of the episodes and 90 % of the deaths were in the Africa region. Approximately, 77 % of malaria deaths globally occurred among children under 5 years .
Malaria is a major public health burden in Ethiopia, where its transmission and burden varies with altitude, degree of urbanization, and use of insecticides . A recent malaria trend analysis in northwest Ethiopia revealed 40 % prevalence; the only species to cause the disease, as confirmed microscopically, were P. falciparum (75 %) and P. vivax (25 %) .
In tropical African countries, epidemiological concurrence and co-infection between malaria and helminthiasis is common [4–6]. For example, in Tanzania the prevalence of malaria-schistosomiasis co-infection was reported to be 42 % . In Ethiopia, the prevalence of malaria-schistosomiasis co-infection reported to be 15 % and caused high prevalence of anemia, as compared to those infected only with malaria .
Earlier studies indicated a controversial interaction of helminthic co-infection with malaria [7, 8]. Intestinal schistosomiasis plays an antagonistic role against malaria, but the egg intensity of Schistosoma mansoni (S. mansoni) and the age of infected individuals could determine the type of interaction [9, 10]. Although most studies were conducted on animal models, they reported that S. mansoni co-infection contributes to severe malaria presentation. They revealed that S. mansoni co-infection resulted in high Plasmodium parasitemia and increased susceptibility of infected mouse models to mortality [11–14]. In contrast, others illustrated that S. mansoni co-infection contributed to low Plasmodium parasitemia and inhibited cerebral malaria [15–17]. However, these studies suggested that the type of animal model and Plasmodium parasite used significantly affects the impact of S. mansoni co-infection with malaria.
On the other hand, a study among humans revealed the association between heavy Plasmodium parasitemia and heavy intensity schistosomiasis co-infection . In order to put better clinical management and control of malaria, especially in schistosomiasis co-endemic areas, information on the prevalence and clinical outcomes of schistosomiasis co-infection with malaria is needed. Therefore, this study was aimed to assess the prevalence of intestinal S. mansoni and malaria co-infection and associated clinical correlates among patients in northwest Ethiopia.
The study was conducted at Chwahit Health Center, Northwest Ethiopia. Chwahit is located at 12°20ʹ4ʺN and 37°13ʹ35ʺE and at an elevation of 1837 m above sea level. There was one health center providing health care for about 30,000 people in Chwahit and its surrounding. As reported by the District Health Bureau, malaria (due to P. falciparum and P. vivax) and schistosomiasis (due to S. mansoni) are common in the study area.
Study design, period and participants
A cross-sectional study was conducted from February to May 2013 among microscopically confirmed malaria patients attending Chwahit Health Center.
Microscopically confirmed malaria patients who provided both blood and stool samples were enrolled in the study.
Patients who attended antiretroviral therapy and antenatal outpatient departments, and patients who had confirmed chronic diseases and concurrent intestinal helminths other than S. mansoni were excluded from participation.
Sample size and sampling techniques
Single population proportion formula was used. Assuming 15 % of malaria and S. mansoni co-infection , 95 % level of significance, 5 % precision and 5 % non response rate, a total of 205 study participants were recruited using a random sampling technique.
Data collection procedures
Demographic and clinical data
An interview-based questionnaire was used to collect demographic data, and clinical data was collected during physical examination at the outpatients’ department of the Health Centre. Severe malaria, in this study, was defined as: P. falciparum positive patients who presented with either circulatory collapse (a systolic pressure of less than 80 mmHg in adults and <50 mmHg in children), severe anemia less than 5 mg/dl, hypoglycemia less than 40 mg/dl, or hyper-parasitemia (≥100,000 parasites/μl of whole blood) .
Microscopic determination of Plasmodium parasitemia
Two drops of venous blood were placed separately on a microscopic glass slide. Thick and thin blood films were prepared and air dried. Thin blood films were fixed with absolute methanol and both films were stained with 10 % Geimsa working solution for 10 min. Then both thin and thick blood films were read by an experienced malaria microscopist with a 100× objective lens and 100 microscopic fields examined to rule out the absence of the malaria parasite. Malaria parasitemia was determined in thick blood films along with 200 white blood cells.
Determination of hematological parameters
Three milliliters venous blood was collected with tris-potassium ethylene diamine tetra acetic acid (EDTA) anti-coagulated tube. Blood was analysed by Cell Dyne 1800 (Abbot Hematology, IL, USA) for the determination of total white blood cells, granulocytes, lymphocytes, mixed cells, red blood cells, platelets, and hemoglobulin level.
Serum biochemical analysis
Three milliliters venous blood was collected with non-anticoagulated tube and allowed to clot at bench top. Then, blood centrifuged at 3000 revolution per minute for 4 min and serum was aliquoted. Then, serum was analysed by HumaStar chemistry analyzer (Human Diagnostics, USA) for serum level of serum glutamate pyruvate transaminase (SGPT), serum glutamate oxaloacetate transaminase (SGOT), total protein, and glucose.
Microscopic diagnosis of Schistosoma mansoni
One gram of fresh stool sample was collected from every study participant. Stool samples were processed with Kato-Katz technique using standardized template measuring 41.75 mg of stool to prepare smear for detection and count of S. mansoni ova. The egg load of S. mansoni from stool was classified as light [1–100 egg/gram (epg)], medium (101–400 epg), or heavy (>400 epg) .
Data entered into computer data base using Epi Info 3.5.3. Cleared data was transferred to SPSS version 20 for statistical analysis using logistic regression, independent samples t test and one way ANOVA. Odds ratio (OR) with 95 % CI was used to determine strength of association between variables. Statistically significance was considered at 95 % level of confidence and P value less than 0.05.
The study protocol was reviewed and approved by School of Biomedical and Laboratory Sciences Research and Ethics Committee, University of Gondar, Gondar, Ethiopia. Permission was obtained from Dembia Health Bureau and Chwahit Health Center to conduct the study. Informed consent and assent were obtained from all participants and/or their guardians after being briefed on the risks and benefits of the study.
Demographic and clinical characteristics of the study participants
A total of 205 malaria positive study participants, 63.4 % (130/205) males and 36.6 % (75/205) females, were included. The mean (SD) age of study participants was 25 (12) years. The prevalence of P. falciparum and P. vivax among the study participants was 71.7 % (147/205) and 25.9 % (53/205), respectively. The remaining 2.4 % (5/205) had mixed infections. Fifty six percent (115/205) of the study participants presented with fever. Hypotension was found only among 2.9 % (6/205) of the participants. Severe malaria was observed in 25 % (38/152) of the study participants, while hyper-parasitemia was identified in only 3.9 % (6/152) of the study participants harboring P. falciparum.
Prevalence of malaria and S. mansoni co-infection
In this study, the prevalence of S. mansoni and malaria co-infection was 19.5 % (40/205). Eighty percent of the S. mansoni co-infections were observed in participants with P. falciparum, while the remaining 20 % were within those with P. vivax infection. A higher percentage of S. mansoni co-infection [32.5 % (13/40)] was observed within the age group of 16–20 years old (p < 0.05) (Table 1).
Clinical correlates of malaria and S. mansoni co-infection
In this study, there was a higher frequency of fever among S. mansoni co-infected participants than malaria only infected ones (χ2 = 5.43, P < 0.022). A higher frequency of severe anemia was also observed among S. mansoni co-infected participants (35.0 %) than malaria only infected ones (25.5 %) (χ2 = 7.54, P < 0.006).
In addition, mean differences in hematological and biochemical parameters were observed among S. mansoni co-infected and malaria only infected participants. However, a significant difference was observed only in mean red blood cell count (4.42 ± 0.11 vs. 4.64 ± 0.04, p < 0.033) and hemoglobulin level (12.48 ± 0.38 vs. 13.38 ± 0.13, p < 0.006), respectively (Tables 2, 3).
There was a mean difference in malaria parasitemia among malaria only infected, light and moderate-heavy S. mansoni co-infected participants (F = 3.43, p < 0.034). In the Post Hoc analysis, this difference persisted only among light and moderate-heavy S. mansoni co-infected participants (3224 vs. 5537 parasite/μl, p < 0.027).
In this study, severe malaria was identified in 18.5 % (38/205) of the study participants. A higher frequency of severe malaria was observed among males (65.8 %) than females (34.2 %). Patients in the age group of 6–10 years old were 6.8 times more likely to experience severe malaria (p < 0.05). Twenty-six percent of the study participants with severe malaria had S. mansoni co-infection. Moderate-heavy intensity of S. mansoni was associated with severe malaria (p < 0.05) (Table 4).
Malaria and schistosomiasis co-exist in sub-Saharan African countries [4–6, 21]. In the present study, the overall prevalence of S. mansoni co-infection with malaria was 19.5 %. This prevalence was lower compared to a recent study carried out in southern Ethiopia, 22.6 % , and Tanzania 42 % . However, it was higher than another study conducted in southern Ethiopia, 15 % . A cohort study in Senegal also reported a high co-infection between malaria and schistosomiasis . The difference can be explained by differences in water contact and microgeographical areas which could affect the co-infection between malaria and schistosomiasis [23, 24].
In this study, higher S. mansoni co-infection was observed among males and within the age group of 16–20 years old. In an earlier study from Kenya, children were 9.3 times more likely to be co-infected with schistosomiasis and malaria than adults . Additionally, studies from Sudan and Swaziland revealed that socio-cultural factors could lead higher exposure of males for schistosomiasis [25–27].
In the current study, a higher frequency of S. mansoni co-infected participants presented with fever than malaria only infected ones. Although each case of malaria and schistosomiasis could lead to fever presentation [28, 29], schistosomiasis co-infection with malaria suggested to upregulate production of inflammatory markers that aggravate fever .
In this study, although significant association was found only in red blood cell count and hemoglobulin level, hematological parameters were found to be influenced by S. mansoni co-infection. In an earlier animal model study, schistosomiasis co-infection prolonged lower density malaria parasitemia time and caused anemia as compared to the malaria only infected group .
However, P. falciparum and P. vivax were reported to decrease hemoglobulin level, white blood cells, red blood cells and platelet counts . Schistosomiasis could also result in low hemoglobulin level and lymphocyte count, but increased total white blood cell, neutrophils, eosinophiles and monocytes count [33, 34]. Therefore, concurrent schistosomiasis with malaria could lead to high co-morbidity associated with hematological parameters.
In this study, high mean Plasmodium parasitemia was observed more frequently among malaria only infected participants than S. mansoni co-infected participants. In an earlier study, reduced Plasmodium parasitemia was reported to be associated with schistosomiasis co-infection . However, this contradicted a result from southern Ethiopia, where schistosomiasis co-infected malaria patients were 3.65 times more likely to be Plasmodium dense than malaria only positives . The difference could be explained with variation in the intensity of schistosomiasis co-infection, which would affect Plasmodium parasitemia.
Higher mean Plasmodium parasitemia was more frequently observed among moderate-heavy S. mansoni co-infected participants than light co-infected ones. Therefore, schistosomiasis co-infection could affect Plasmodium parasitemia, depending on the intensity of the ova. Previous studies from Mali and Senegal reported that light schistosomiasis intensity is correlated with a decrease in Plasmodium parasitemia [9, 35].
In the current study, the age group of 6–10 years old and moderate-heavy intensity S. mansoni co-infection were identified as the determining factors for severe malaria. In earlier studies, children co-infected with schistosomiasis and heavy intensity of schistosomiasis were at risk of developing severe malaria [24, 30, 35]. This could be explained by the high production of interferon gamma (IFN-γ) in children and resulted in higher malaria parasitemia that could lead to severe malaria . In the present study, 66.7 % of the study participants who presented with hyper-parasitemia were children.
Prevalence of malaria and S. mansoni in the study area was considerably high. Severity of malaria and parasitemia of Plasmodium were associated with certain age groups and intensity of concurrent intestinal schistosomiasis. Further study is needed to explore the underlying mechanisms of interaction between malaria and S. mansoni.
tris-potassium ethylene diamine tetra acetic acid
egg per gram
Serum glutamate oxaloacetate transaminase
serum glutamate pyruvate transaminase
World Health Organization. World malaria report. Geneva: WHO; 2013.
Jima D, Getachew A, Bilak H, Steketee RW, Emerson PM, Graves PM, et al. Malaria indicator survey 2007, Ethiopia: coverage and use of major malaria prevention and control interventions. Malaria J. 2010;9:58.
Alemu A, Muluye D, Mihret M, Adugna M, Gebeyaw M. Ten year trend analysis of malaria prevalence in Kola Diba, North Gondar, Northwest Ethiopia. Parasites Vectors. 2012;5:173–8.
Mazigo HD, Waihenya R, Lwambo NJS, Mnyone LL, Mahande AM, Seni J, et al. Co-infections with Plasmodium falciparum, Schistosoma mansoni and intestinal helminths among schoolchildren in endemic areas of Northwestern Tanzania. Parasites Vectors. 2010;3:44.
Sousa-Figueiredo JC, Gamboa D, Pedro JM, Fancony C, Langa AJ, Magalhaes RJS, et al. Epidemiology of malaria, schistosomiasis, geohelminths, anemia and malnutrition in the context of a demographic surveillance system in Northern Angola. PLoS One. 2012;7(4):e33189. doi:10.1371/journal.pone.0033189.
Degarege A, Legesse M, Medhin G, Animut A, Erko B. Malaria and related outcomes in patients with intestinal helminths: a cross-sectional study. BioMed Cent Infect Dis. 2012;12:291.
Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Krudsood S, Gay F, et al. Association of helminth infections with increased gametocyte carriage during mild falciparum malaria in Thailand. Am J Trop Med Hyg. 2001;65(5):644–7.
Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Vannaphan S, Traore B, et al. Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. Am J Trop Med Hyg. 2001;65(6):834–6.
Briand V, Watier L, Hesran JVL, 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(6):702–7.
Sangweme DT, Midzi N, Zinyowera-Mutapuri S, Mduluza T, Diener-West M, Kumar N. Impact of Schistosome infection on Plasmodium falciparum malariometric indices and immune correlates in school age children in Burma Valley, Zimbabwe. PLoS Negl Trop Dis. 2010;4(11):e882. doi:10.1371/journal.pntd.0000882.
Yoshida A, Maruyama H, Kumagai T, Amano T, Kobayashi F, Zhang M, et al. Schistosoma mansoni infection cancels the susceptibility to Plasmodium chabaudi through induction of type 1 immune responses in A/Jmice. Int Immunol. 2000;12(8):1117–25.
Sangweme D, Shiff C, Kumar N. Plasmodium yoelii: adverse outcome of non-lethal P. yoelii malaria during co-infection with Schistosoma mansoni in BALB/c mouse model. Exp Parasitol. 2009;122(3):254–9.
Legesse M, Erko B, Balcha F. Increased parasitaemia and delayed parasite clearance in Schistosoma mansoni and Plasmodium berghei co-infected mice. Acta Trop. 2004;91(2):161–6.
Laranjeiras RF, Brant LCC, Lima ACL, Coelho PMZ, Braga EM. Reduced protective effect of Plasmodium berghei immunization by concurrent Schistosoma mansoni infection. Mem Inst Oswaldo Cruz. 2008;103(7):674–7.
Lwin M, Last C, Targett GAT, Doenhoff MJ. Infection of mice concurrently with Schistosoma mansoni and rodent malarias: contrasting effects of patent S. mansoni infections on Plasmodium chabaudi, P. yoelii and P. berghei. Ann Trop Med Parasitol. 1982;76(3):265–73.
Waknine-Grinberg JH, Gold D, Ohayon A, Flescher E, Heyfets A, Doenhoff MJ, et al. Schistosoma mansoni infection reduces the incidence of murine cerebral malaria. Malaria J. 2010;9:5.
Bucher K, Dietz K, Lackner P, Pasche B, Fendel R, Mordmuller B, et al. Schistosoma co-infection protects against brain pathology but does not prevent severe disease and death in a murine model of cerebral malaria. Int J Parasitol. 2011;41(1):21–31.
Florey LS, King CH, Dyke MKV, Muchiri EM, Mungai PL, Zimmerman PA, et al. Partnering parasites: evidence of synergism between heavy schistosoma haematobium and Plasmodium species infections in Kenyan children. PLoS Negl Trop Dis. 2012;6(7):e1723. doi:10.1371/journal.pntd.0001723.
World Health Organization (WHO). Management of severee malaria: a practical hand book. 3rd ed. Geneva: WHO; 2012.
World Health Organization. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Geneva: WHO; 2002.
Mulu A, Legesse M, Erko B, Belyhun Y, Nugussie D, Shimelis T, et al. Epidemiological and clinical correlates of malaria-helminth co-infections in southern Ethiopia. Malaria J. 2013;12:227.
Sokhna C, Hesran JVL, Mbaye PA, Akiana J, Camara P, Diop M, et al. Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malaria J. 2004;3:43.
Essa T, Birhane Y, Endris M, Moges A, Moges F. Current status of Schistosoma mansoni infections and associated risk factors among students in Gorgora town, Northwest Ethiopia. ISRN Infect Dis. 2013. doi:10.5402/2013/636103.
Booth M, Vennervald BJ, Kenty LC, Butterworth AE, Kariuki HC, Kadzo H, et al. Micro-geographical variation in exposure to Schistosoma mansoni and malaria, and exacerbation of splenomegaly in Kenyan school-aged children. BioMed Cent Infect Dis. 2004;4:13.
Dahab TO, El-Bingawi HM. Epidemiological survey: Schistosoma haematobium in school children of White Nile areas, Khartoum. Sudan Med J. 2012;48(2):1–6.
Liao CW, Sukati H, Nara T, Tsubouchi A, Chou CM, Jian JY, et al. Prevalence of Schistosoma haematobium infection among schoolchildren in remote areas devoid of sanitation in northwestern Swaziland, Southern Africa. Jpn J Infect Dis. 2011;64(4):322–6.
Abou-Zeid AH, Abkar TA, Mohamed RO. Schistosomiasis infection among primary school students in a war zone, Southern Kordofan State, Sudan: a cross-sectional study. BMC Public Health. 2013;13:643.
Ahsan T, Ali H, Bkaht SF, Ahmad N, Farooq MU, Shaheer A, et al. Jaundice in falciparum malaria; changing trends in clinical presentation-a need for awareness. J Pak Med Assoc. 2008;58(11):616–21.
de Jesus AR, Silva A, Santana LB, Magalhaes A, de Jesus AA, de Almeida RP, et al. Clinical and immunologic evaluation of 31 patients with acute Schistosomiasis mansoni. J Infect Dis. 2002;185:98–105.
Diallo TO, Remoue F, Schacht AM, Charrier N, Dompnier JP, Pillet S, et al. Schistosomiasis co-infection in humans influences inflammatory markers in uncomplicated Plasmodium falciparum malaria. Parasite Immunol. 2004;26:365–9.
Sangweme D, Shiff C, Kumar N. Plasmodium yoelii: adverse outcome of non-lethal P. yoelii malaria during co-infection with Schistosoma mansoni in BALB/c mouse model. Exp Parasitol. 2009;122(3):254–9.
Erhart LM, Yingyuen K, Chuanak N, Buathong N, Laoboonchai A, Miller RS, et al. Hematologic and clinical indices of malaria in a semi-immune population of western Thailand. Am J Trop Med Hyg. 2004;70(1):8–14.
Mohammed EHA, Eltayeb M, Ibrahim H. Haematological and biochemical morbidity of Schistosoma haematobium in school children in Sudan. Sultan Qaboos Univ Med J. 2006;6(2):59–64.
Al-hroob A. Haematological and biochemical study on Albino rats infected with 70 ± 10 cercariae Schistosoma mansoni. Adv Environ Biol. 2010;4(2):220–3.
Lyke KE, Dicko A, Dabo A, Sangare L, Kone A, Coulibaly D, et al. Association of Schistosoma haematobium infection with protection against acute Plasmodium falciparum malaria in Malian children. Am J Trop Med Hyg. 2005;73(6):1124–30.
SG and BM conceived the study. SG, GG, LW and MW participated in the data collection. BM, YW and AK supervised the data collection. SG analysed the data and prepared the first manuscript draft. BM and YW reviewed the draft. All authors contributed to the writing of the paper. All authors read and approved the final manuscript.
The authors would like to thank University of Gondar for funding this study. We would also thank the Health Center staff and study participants for their kind cooperation during the data collection.
Compliance with ethical guidelines
Competing interests The authors declare that they have no competing interests.