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The burden of polyparasitism among primary schoolchildren in rural and farming areas in Zimbabwe
Transactions of the Royal Society of Tropical Medicine and Hygiene (2008) 102, 1039—1045
available at www.sciencedirect.com
journal homepage: www.elsevierhealth.com/journals/trst
The burden of polyparasitism among primary schoolchildren in rural and farming areas in Zimbabwe N. Midzi a, D. Sangweme b, S. Zinyowera c, M.P. Mapingure d, K.C. Brouwer e, A. Munatsi a, F. Mutapi f, J. Mudzori g, N. Kumar b, G. Woelk h, T. Mduluza d,∗ a
National Institute of Health Research, Box CY 573, Causeway, Harare, Zimbabwe Johns Hopkins Bloomberg School of Public Health, Department of Molecular Microbiology and Immunology, Baltimore, MD, USA c College of Health Sciences, Department of Medical Microbiology, P.O. Box A178, Avondale, Harare, Zimbabwe d University of Zimbabwe, Department of Biochemistry, P.O. Box MP167, Mount Pleasant, Harare, Zimbabwe e University of California, San Diego, Division of International Health and Cross Cultural Medicine, Department of Family and Preventive Medicine, San Diego, CA, USA f University of Edinburgh, Institute for Immunology and Infection Research, Edinburgh, UK g National Microbiology Reference Laboratory, P.O. Box ST749, Southerton, Zimbabwe h University of Zimbabwe, Faculty of Medicine, Department of Continuing Health Science, Harare, Zimbabwe b
Received 10 February 2008; received in revised form 28 May 2008; accepted 28 May 2008 Available online 24 July 2008
KEYWORDS Schistosoma; Plasmodium falciparum; Helminths; Polyparasitism; Children; Zimbabwe
∗
Summary A cross-sectional study was conducted in Zimbabwe among 1303 primary schoolchildren from a rural (53.3%) and a commercial farming area (46.7%) to determine the prevalence of co-infection by helminths and Plasmodium falciparum. Urine was examined on three successive days using the filtration method. Two stool specimens were processed using the Kato-Katz method and a third specimen was processed using the sedimentation method. Plasmodium falciparum was diagnosed from thick blood films. The prevalence of Schistosoma haematobium in the rural and farming areas was 66.8% and 52.3%, respectively, and for S. mansoni the prevalence was 12.4% and 22.7%, respectively. Plasmodium falciparum, hookworms, Ascaris lumbricoides and Trichuris trichiura occurred only in the farming area, with a prevalence of 27.9%, 23.7%, 2.1%, 2.3%, respectively. Co-infection and triple infection with schistosomes, P. falciparum and soil-transmitted helminths occurred in the commercial farming area only. Hookworm and S. mansoni infections were associated with P. falciparum malaria (P < 0.001, OR = 2.48, 95% CI 1.56—3.93 and P = 0.005, OR = 1.85, 95% CI 1.20—2.87, respectively). Overlap of helminths with malaria is a concern among primary schoolchildren and incorporating helminth control in programmes aiming to control malaria will improve funding and increase the efficiency of control for neglected tropical diseases in identified co-endemic settings. © 2008 Published by Elsevier Ltd on behalf of Royal Society of Tropical Medicine and Hygiene.
Corresponding author. Tel.: +263 04 334052; fax: +263 04 333407. E-mail address: [email protected] (T. Mduluza).
0035-9203/$ — see front matter © 2008 Published by Elsevier Ltd on behalf of Royal Society of Tropical Medicine and Hygiene. doi:10.1016/j.trstmh.2008.05.024
1040
1. Introduction Malaria is one of the most important global public health threats. It is widely distributed, with 40% of the world’s population at risk of the disease. Three hundred to 500 million persons are infected and more than one million deaths occur annually, 90% of which are in sub-Saharan Africa (WHO, 2000). Schistosomiasis is second only to malaria as a parasitic disease of public health importance in tropical and subtropical countries in Africa, the Middle East and South America (TDR, 2005), and is endemic in 76 countries (Crompton et al., 2003). Six hundred and fifty-two million people are at risk of schistosomiasis infection and 193 million are already infected (Chitsulo et al., 2000). The soil-transmitted helminths (STH): hookworms, Ascaris lumbricoides and Trichuris trichiura are also widely distributed in tropical countries (Mwangi et al., 2006), infecting 1300, 1450 and 1050 million people, respectively (Montresor et al., 2002; WHO, 2002). Among primary school-aged children, infection with schistosomiasis or STH is associated with malnutrition, anaemia, retarded growth and cognitive impairment, and furthermore, sick children are often absent from school (WHO, 2003; WHO and UNICEF, 2004). While parasitic diseases are most commonly studied individually, in reality polyparasitism is common and the high-risk population for both schistosomiasis and STH is primary school-age children. Schistosomiasis, STH and malaria are typically diseases of economically disadvantaged people who have little access to proper care or effective preventive measures (Hotez et al., 2006; Montresor et al., 2002; Mwangi et al., 2006). Schistosomes and STH are similar in that their transmission is through contamination of the environment with faecal matter and urine due to poor or absent sanitary facilities (de Silva, 2003). Overlap of schistosome species, STH and Plasmodium falciparum can be expected in areas where the conditions that favour parasitic survival and transmission are similar. Those conditions are warm temperatures, permanent bodies of water and poverty. Water development schemes for agriculture support the breeding of schistosome vector snails and vector mosquitoes, and sustain the developmental stages of their larvae. Socioeconomic factors such as a lack of insecticide-treated bed nets and shoes are also risk factors associated with polyparasitism (Mwangi et al., 2006). To our knowledge, there has not been a community-based study to investigate the combined overlap of schistosome species and STH with P. falciparum among primary schoolchildren, who still lack advanced immunity against parasitic diseases (WHO, 2004). Such studies may provide useful information to aid the development of vaccines against helminths and malaria (Mwangi et al., 2006), as co-infection may affect the efficacy of such vaccines. Community-based studies may also provide data on foci where schistosome species and STH overlap with P. falciparum. Such information is relevant to the success of the growing global initiatives to reduce the burden of morbidity due to helminth infection (Crompton et al., 2003; WHA, 2001; WHO, 2005). Only when data indicating the geographic overlap of parasitic diseases in endemic communities are available, can programme control managers prepare coordinated plans of action that describe which drugs need to be delivered in integrated control programmes. The data are
N. Midzi et al. also critically important for promoting strategies aimed at incorporating neglected diseases in the ongoing and actively funded global fight against the big three diseases, HIV, malaria and tuberculosis (TB) (Hotez et al., 2006). This study was, therefore, conducted to determine the epidemiological distribution of Schistosoma species, STH and P. falciparum, and any co-infection with helminths and P. falciparum, among primary schoolchildren living in rural and commercial farming areas in Zimbabwe.
2. Materials and methods 2.1. Study design A cross-sectional study was undertaken to provide baseline data for a longitudinal intervention study, the objective of which is to determine the effect of combined regular schoolbased deworming for schistosomiasis and STH on morbidity and malaria outcome among primary schoolchildren living in rural and commercial farming areas in Zimbabwe.
2.2. Study areas and population The study was carried out in July 2004 among 1302 primary schoolchildren living in rural (Nyamaropa) and commercial farming (Burma Valley) areas. Nyamaropa is a typical rural area located in Shamva district, 160 km north east of the capital city, Harare. The area receives high rainfall, which averages 175 mm/month during the rainy season (November—March), but is dry between May and October. The inhabitants practice subsistence farming. The major source of water is the Eben dam on the perennial River Mupfurudzi. The community has no access to piped water and draws water for domestic purposes from open wells and a few boreholes distributed in the area. During the dry season, the community is heavily involved in vegetable gardening along the rivers and near the dam. Children from this area included in the study attended Nyamaropa Primary School and were drawn from 19 villages that surround the school. Burma Valley, which borders Mozambique, is located in Mutare district, Manicaland province, about 300 km east of Harare. It receives heavy rainfall, which averages 202 mm/month in summer (November—March) and is warm to hot throughout the year. Perennial rivers and streams drain from the mountain ranges to the south. The area is divided into 12 commercial farms and two new resettlement areas. Each farm has a compound where farm labourers live. The communities living in the farm compounds use communal piped water located at strategic points. They also use communal toilets and bathrooms distributed around the compounds. The predominant commercial crops grown in the area include bananas, flowers, butternut squash and tobacco. Abundant irrigation activities keep the soil wet all year round. Three primary schools (Valhalla, Msapa and Kaswa) drawing children from the farming communities were included in our study. Demographic data, including age, gender and the village where participants lived, were recorded by a questionnaire. Ages of participants were obtained from the class registers provided by teachers.
Polyparasitism in children in Zimbabwe
2.3. Parasitological techniques Urine and faecal samples were collected between 10:00 h and 14:00 h in separate wide mouth plastic specimen bottles labelled with the laboratory identification number assigned to each individual. The samples were processed within 2 h of collection. Diagnosis of S. haematobium and intestinal helminths (S. mansoni, hookworms, T. trichiura and A. lumbricoides) was based on the detection of worm eggs in urine and faeces, respectively. Infection with S. haematobium was diagnosed using the urine filtration technique as described by Mott et al. (1982). In brief, 10 ml of urine were filtered through a Nytrel filter membrane. The filter was stained with Lugol’s iodine and examined with a light microscope using the × 10 objective. Schistosoma haematobium egg intensity was expressed as the number of eggs detected per 10 ml of urine. The same procedure was repeated on three consecutive days in order to prevent misdiagnosis due to day-to-day variation in egg excretion (Doehring et al., 1983). The overall intestinal helminth (S. mansoni and STH) infection status of participants was determined based on the combination of results from the formal ether concentration and Kato-Katz techniques in order to improve sensitivity and, hence, accuracy of diagnosis. For the formal ether concentration method, about 1 g of each specimen collected on the first day was preserved in a tube containing 10% formalin (Cheesbrough, 1998). Four qualified laboratory scientists performed microscopic examination of the processed stool specimens in order to detect S. mansoni, hookworm, T. trichiura and A. lumbricoides ova. For the quantitative Kato-Katz technique, stool specimens collected from each individual on the following two consecutive days were processed according to Katz et al. (1972). Thick faecal smears prepared using 41.7 mg plastic templates were examined within 30—60 min using a light microscope in order to detect and quantify hookworm and other STH eggs. The smears were left to clear for at least 24 h and were re-examined to detect S. mansoni eggs. The number of eggs detected from each Kato-Katz thick smear was multiplied by 24 in order to express infection intensities as the number of eggs per gram of stool. Approximately 5 ml of venous blood was drawn from willing participants in blood collection tubes containing EDTA as anticoagulant. Thick films for malaria diagnosis were prepared from fresh blood and the remaining blood was used for plasma separation. Plasmodium falciparum was diagnosed by microscopic examination of thick blood films after Giemsa staining (Cheesbrough, 1998). The presence of either ring forms or gametocytes was a conclusive diagnosis of P. falciparum infection.
2.4. Treatment Children infected with any of the schistosome species or STH were treated with praziquantel at 40 mg/kg and a single 400 mg albendazole tablet. Bread and orange juice (500 ml/child) were given after the tablets in order to reduce the nauseating effect of praziquantel. Children positive for P. falciparum were treated with a combination of
1041 chloroquine, sulfadoxine and pyrimethamine according to local malaria case-management guidelines.
2.5. Ethical considerations Provincial and district medical and education directors, chiefs, councillors and village head-men granted permission. General information regarding the nature of the study and its objectives was explained to the community and study participants. Feedback and consent were sought at schools, farms and village meetings. Inclusion of children into the study took place after free individual, parental and school authority informed written consent. Children joined the study voluntarily and were allowed to drop out at any time they wished without any prejudice.
2.6. Statistical methods Data were analysed using SPSS version 8.0 for Windows (SPSS Inc. Chicago, IL, USA). Description of the study population was done by area of residence. Prevalence of P. falciparum, schistosomes and STH among primary schoolchildren was compared for those living in rural and commercial farming areas using Pearson’s X2 test or Fisher’s exact test, where appropriate. Odds ratios (OR) were calculated for risk estimation. Mixed parasitic infections were compared for those living in rural and farming areas. The association of helminth infection with P. falciparum infection was analyzed using Pearson’s X2 test. In our study, double infection was defined as co-infection with any two parasite species. Triple infection was defined as infection with three parasite species. Statistical significance for all analyses was determined at 5% alpha level.
3. Results Overall, 1303 children were enrolled from a rural (53.3%) and a commercial farming area (46.7%). The age of participants ranged from 5—17 years. Three primary schools in the commercial farming area and one primary school in the rural area were included in the study in order to recruit an equal number of children from each area. At each school, all children from grades 1 to 6 were enrolled on a voluntary basis. The characteristics of the study population are shown in Table 1. Overall, 677 (52%) boys and 626 (48%)
Table 1
Description of the study population by area
Parameter
Overall n (%) Farming n (%) Rural n (%)
Study participants 1303 Gender Male 677 (52.0) Female 626 (48.0) Age group (years) 5—7 8—10 11—13 14—17
186 (14.3) 579 (44.4) 461 (35.4) 77 (5.9)
609 (46.7)
694 (53.3)
307 (45.3) 302 (48.2)
370 (54.7) 324 (51.8)
71 (38.2) 271 (46.8) 221 (47.9) 46 (59.7)
115 (61.8) 308 (53.2) 240 (52.1) 31 (40.3)
1042
N. Midzi et al.
girls were enrolled. Nine hundred and ninety-four children (76.3%) voluntarily gave blood. Among these, malaria testing was performed on 935 (94.1%).
3.1. Distribution of schistosomes, STH and Plasmodium falciparum The distribution of helminths and P. falciparum among primary schoolchildren living in the rural and commercial farming areas is shown in Table 2. Children living in the rural area were more likely to be infected with S. haematobium (66.8%) compared to those living in the commercial farming area (52.3%) (P < 0.001, OR = 0.54, 95% CI 0.43—0.68). The ORs for being infected with S. mansoni or hookworms for children living in the commercial farming area compared to those living in the rural area were 2.08 and 208.49, respectively. Plasmodium falciparum and STH were absent in the rural area. Hookworm was the predominant STH observed and it was more common in the commercial farming area (23.7%) than the rural area, where only one participant was infected.
3.2. Distribution of parasites by gender More boys (19%) were infected with S. mansoni compared to girls (14%) (P = 0.008). Boys had also a higher prevalence of hookworms (12.7%) compared to girls (9.1%) (P = 0.043). There were no significant differences in distribution of other helminths by gender.
3.3. Distribution of polyparasitism The distribution of mixed infection from schistosomes in the rural and commercial farming areas is shown in Table 3.
Polyparasitism was only observed among primary schoolchildren living in the commercial farming area. However, one child (0.2%) in the rural area was co-infected with schistosomes and STH, compared with 63 (12.8%) in the farming area (OR = 62.81, 95% CI 8.67—454.80, P < 0.001).
3.4. Association of helminths with Plasmodium falciparum malaria The association of helminths with P. falciparum is displayed in Table 4. Children who had hookworm infection were more likely to be infected with P. falciparum malaria (OR = 2.48, 95% CI 1.56—3.93, P < 0.001). There was also a significant association between S. mansoni and P. falciparum malaria (OR = 1.87, 95% CI 1.21—2.90, P = 0.004). There was no relationship between S. haematobium, A. lumbricoides or T. trichiura with P. falciparum malaria.
4. Discussion Our findings corroborate the results of a study undertaken in Senegal by Sokhana et al. (2004), which found a significantly higher incidence of clinical malaria among children infected with S. mansoni. The association of hookworm infection with malaria observed in our study differs with findings made by Shapiro et al. (2005), who found no association of STH with malaria in south western Uganda. In our study, S. haematobium was not associated with P. falciparum infection. Briand et al. (2005) found that children lightly infected with S. haematobium had less parasitaemia than children not infected with S. haematobium, whilst Lyke et al. (2005) reported that S. haematobium was protective against clinical malaria. Table 5 shows the prevalence of STH observed in Burma Valley by different investigators at different time points up
Table 2 Prevalence of schistosomes, soil-transmitted helminths and Plasmodium falciparum among primary schoolchildren living in commercial farming and rural areas in Zimbabwe Farming n (%)
Rural n (%)
X2 test (P-value)
Odds ratio (95% CI)
Schistosoma haematobium Examined 1279 Infected 767 (60.0)
599 313 (52.3)
680 454 (66.8)
28.48 (<0.001)
0.54 (0.43—0.68)
Schistosoma mansoni Examined 1249 Infected 214 (17.1)
577 131 (22.7)
672 83 (12.4)
12.43 (<0.001)
2.08 (1.54—2.82)
Hookworm Examined Infected
575 136 (23.7)
674 1 (0.1)
(<0.001)
208.49 (29.05—1496.27)
Ascaris lumbricoides Examined 1249 Infected 12 (1.0)
575 12 (2.1)
674 0
(<0.001)
Indeterminable
Trichuris trichiura Examined 1249 Infected 13 (1.0)
575 13 (2.3)
674 0
(<0.001)
Indeterminable
Plasmodium falciparum Examined 935 Infected 143 (15.3)
512 143 (27.9)
423 0
(0.001)
Indeterminable
Parasite
Overall n (%)
1249 137 (11.0)
Polyparasitism in children in Zimbabwe Table 3
1043
Distribution of polyparasitism among primary schoolchildren living in farming and rural areas in Zimbabwe
Parasite
Overall n (%)
Farming n (%)
Rural n (%)
Examined
915
493
422
157 (31.8) 29 (5.9) 63 (12.8) 58 (11.8)
289 (64.5) 0 1 (0.2) 0
Schistosomes 444 (48.5) STH only 29 (3.2) Schistosomes + STH 67 (7.3) Schistosomes + Plasmodium 58 (6.3) falciparum STH + Plasmodium 7 (0.8) falciparum Schistosomes + STH + 26 (2.8) Plasmodium falciparum
X2 test (P-value)
Odds ratio (95% CI)
124.91 (<0.001) (<0.001) (<0.001) (<0.001)
0.21 (0.16—0.28) Indeterminable 62.81 (8.67—454.80) Indeterminable
7(1.4)
0
(0.017)
Indeterminable
26 (5.3)
0
(<0.001)
Indeterminable
STH: soil-transmitted helminths.
Table 4 Association of helminths with Plasmodium falciparum infection among primary schoolchildren living in a farming area in Zimbabwe Malaria positive n (%)
Malaria negative n (%)
X2 (P-value)
Odds ratio (95% CI)
Schistosoma haematobium Examined 920 Positive 546 (59.3)
140 85 (60.7)
780 461 (59.1)
0.13 (0.72)
1.07 (0.74—1.55)
Schistosoma mansoni Examined Positive
906 155 (17.1)
132 34 (25.8)
774 121 (15.6)
8.15 (0.004)
1.87 (1.21—2.90)
Hookworm Examined Positive
905 117 (12.9)
131 31 (23.7)
774 86 (11.1)
15.68 (<0.001)
2.48 (1.56—3.93)
Trichuris trichiura Examined Positive
905 11 (1.2)
131 3 (2.3)
774 8 (1.0)
1.47 (0.21a )
2.24 (0.59—8.57)
Ascaris lumbricoides Examined Positive
905 8 (0.9)
131 1 (0.8)
774 7 (0.9)
0.03 (1.000a )
0.84 (0.10—6.91)
Parasite combination
a
Overall n (%)
P-value based on Fisher’s exact test.
to the present study. In all these studies, either the concentration or combined concentration technique and Kato-Katz methods were used. These studies confirm our finding that hookworm is the major geohelminth problem in the commercial farming area compared to other STH. Our results support the findings made by Brooker et al. (2006), based on geographic information systems, that hookworm is the
Table 5
most geographically widespread of the three main types of STH that occur throughout much of the African continent south of the Sahara. Table 5 shows a pattern, in which the prevalence of STH was low in 1973, then increased in 1983 and 1989, and was followed by a decline observed in our study. Chandiwana and Makaza (1983) observed that farm workers
Trends in distribution of soil-transmitted helminths in Burma Valley at different survey times since 1973
Authors
Mcdonald and Goldsmid, 1973 Chandiwana and Makaza, 1983 Chandiwana et al., 1989 Midzi et al. (current paper)
n
1543 200 1635 609
Target population
Children and adults Children and adults Children and adults Children
Prevalence of parasite Hookworm
Ascaris lumbricoides
Trichuris trichiura
26.6% 88.5% 61.7% 21%
2.2% 43.5% 2.7% 1.8%
0.3% 13.5% 2.3% 1.9%
1044 lived in poorly constructed, thatched, mud huts in overcrowded settlements sharing only four unprotected water outlets for domestic purposes. They also observed that sanitary facilities were comprised of a few poorly built and remote pit latrines, mostly unused due to unhygienic conditions, leading to indiscriminate defecation by the population. In our study, we observed that although households still shared toilets in many farm compounds, on average, four families were using a single toilet strategically constructed close to either their huts in some compounds, or to modern houses in other compounds. We also noted that ventilated pit latrines are replacing the old type. The households were also provided with communal sinks and showers for laundry and bathing, respectively. These conditions may have contributed to improved hygiene practices and increased use of latrines compared to bush toilets by the farm workers, probably resulting in reduced STH transmission. However, unlike the earlier studies, our study population did not include adults, who could have a high prevalence of hookworm infection. This could be another explanation for the observed decline in hookworm prevalence. Improvements in accommodation, water and sanitation in the farming communities seem not to have made any impact on the prevalence of schistosomiasis in Burma Valley. Chandiwana and Makaza (1983) observed 16% prevalence of S. mansoni in the Burma Valley area, whereas in our study the prevalence of S. mansoni was 22.7%. The reason could be that children have water contact activities other than bathing in unprotected water bodies (Chandiwana, 1987). Plasmodium falciparum malaria was only observed in the commercial farming area and the prevalence (27.9%) was rather too high for a community where many people are expected to be free from malaria. There were no cases in the rural area, although it is located in a district that has been classified as endemic for malaria (National Health Profile, 2002). This difference could be explained by the different malaria diagnostic methods used. Our results were based on the detection of parasites from thick blood films using a parasitological method which is reliable, whereas results from the National Health Profile reports were based on clinical diagnoses, which may not be specific to malaria, especially in this era when diseases with similar clinical symptoms, like HIV and TB, are common in malaria-endemic areas. Accurate methods, such as microscopy or rapid malaria antigen detection test kits are therefore recommended in the diagnosis of malaria. Microscopy also has an ancillary benefit of testing for drug resistance. Our finding of the occurrence of polyparasitism (Table 3) in the commercial farming area but not the rural area supports that made by Brooker et al. (2006) and the review by Hotez et al. (2006) regarding the geographic congruence of helminths and malaria infection in humans. The existence of triple infection with schistosomes, STH and P. falciparum in the Burma Valley farming area confirms that socioeconomic activities and settlement type, such as clustered and over-crowded settlements, as well as sharing toilets, are risk factors for polyparasitism. On average, four families still shared a single pit latrine in the farming communities (personal observation), a condition that may still not be acceptable to some people, leading to indiscriminate
N. Midzi et al. defaecation (Chandiwana and Makaza, 1983). Irrigation of the banana plantations all year round, except during the rainy season, maintains ponds and small pools of water that become breeding habitats for vector mosquitoes and sustain the adults and larval stages of vector snails (Chimbari et al., 2004; Mwangi et al., 2006). Irrigation activities keep the soils moist all year, making it possible for STH larvae (hookworms) and the ova of A. lumbricoides and T. trichiura, which are transmissible through oral-faecal contamination, to survive. The perennial streams that flow from a range of mountains to the east can also sustain the schistosomiasis vector snail population in the area. During the dry period, May to November, the soils are dry in the rural area, where settlements are dispersed. These conditions are not conducive to transmission of malaria and STH, even though environmental contamination may be occurring. Our study has shown geographical overlap of helminths with P. falciparum, suggesting the need to incorporate helminth control into programmes or funding opportunities for control of the big three diseases (malaria, TB and HIV/AIDS). Regular annual school-based deworming should be initiated in Zimbabwe, targeting children in schools where the prevalence of schistosomiasis is above 50%, in order to reduce the associated morbidity. Authors’ contributions: TM, NM, NK, FM, KCB, AM and GW contributed to the concept and design of the study protocol; NM, DS, AM, SZ, JM and TM carried out the clinical and parasitological assessment; TM, NM, DS and MPM carried out the analysis and interpretation of the data; NM and TM drafted the manuscript. All authors read and approved the final manuscript. TM and NM are guarantors of the paper. Acknowledgements: We thank the schoolchildren from Burma Valley and Shamva, Nyamaropa who participated in the study, and the parents and teachers for permitting their children to take part. We thank the provincial medical and education directors for Manicaland and Mashonaland Central for granting permission to conduct the study in their respective areas. Thanks are addressed to the laboratory technical staff from the National Institute of Health Research. We thank Prof. Anthony Butterworth for all the constructive comments he gave leading to the present state of the manuscript. Acknowledgements also go to the Schistosomiasis Control Initiative (SCI), Imperial College, UK, which supported the programme with anthelminthic drugs (praziquantel). Funding: The UNICEF/UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases Grant A60125, ENHR-Ministry of Health Zimbabwe, Fogarty Grant for field work to NK and DS. International Foundation for Science Grantee: W/4321-1 to TM. Conflicts of interest: None declared.
Polyparasitism in children in Zimbabwe Ethical approval: The Medical Research Council of Zimbabwe gave ethical approval for the study.
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1045 tobium infection with protection against acute Plasmodium falciparum malaria in Malian Children. Am. J. Trop. Med. Hyg. 73, 1124—1130. Mcdonald, F., Goldsmid, J.M., 1973. Intestinal helminth infections in the Burma Valley area of Rhodesia. Cent. Afr. J. Med. 19, 113—115. Montresor, A., Crompton, D.W.T., Gyorkos, T.W., Savioli, L., 2002. Helminth control in school-age children: a guide for managers of control programmes. http://www.who.int/wormcontrol/ documents/helminth control/en/ [accessed 28 April 2008]. Mott, K.E., Baltes, R., Bambagha, J., Baldassini, B., 1982. Field studies of a reusable polyamide filter for detection of Schistosoma haematobium eggs by urine filtration. Tropenmed. Parasitol. 3, 227—228. Mwangi, T.W., Bethony, J., Brooker, S., 2006. Malaria and helminth interactions in humans: an epidemiological viewpoint. Ann. Trop. Med. Parasitol. 100, 551—570. National Health Profile, 2002. Zimbabwe Ministry of Health and Child Welfare, Harare. Shapiro, A.E., Tukulembwa, E.M., Kasten, J., Clarke, S.E., Magnussen, P., Olsen, A., Kabarateine, N.B., Ndyomugyenyi, R., Brooker, S., 2005. Epidemiology of helminth infections and their relationship to clinical malaria in south west Uganda. Trans. R. Soc. Trop. Med. Hyg. 99, 18—24. Sokhana, C., Le Hesran, J.Y., Mbaye, P.A., Akiana, J., Camara, P., Diop, M., Ly, A., Druilhe, P., 2004. Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malar. J. 3, 43. TDR, 2005. Schistosomiasis disease information. Special Programme for Research and Training in Tropical Diseases (TDR). http://www.who.int/tdr/diseases/schisto/diseaseinfo.htm [accessed 28 April 2008]. WHA, 2001. Communicable diseases. 54th World Health Assembly, Resolution WHA54.19. WHO, 2000. Severe falciparum malaria. Trans. R. Soc. Trop. Med. Hyg. 94 (Suppl. 1). WHO, 2002. The prevention and control of schistosomiasis and soil transmitted helminthiasis. World Health Organization, Geneva, Technical Report Series No. 912. WHO, 2003. Partners for Parasite Control Newsletter, issue 1. http://www.who.int/wormcontrol/en/action against worms. pdf [accessed 28 April 2008]. WHO, 2005. Deworming for health and development. Report of the 3rd Global Meeting of the Partners for Parasite Control, Geneva, 29 November 2004. World Health Organization, Geneva, p. 51. WHO and UNICEF, 2004. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. WHO/CDS/CPE/PVC/ 2004.9. http://www.who.int/wormcontrol/documents/joint statements/en/ppc unicef finalreport.pdf [accessed 28 April 2008].
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The burden of polyparasitism among primary schoolchildren in rural and farming areas in Zimbabwe N. Midzi a, D. Sangweme b, S. Zinyowera c, M.P. Mapingure d, K.C. Brouwer e, A. Munatsi a, F. Mutapi f, J. Mudzori g, N. Kumar b, G. Woelk h, T. Mduluza d,∗ a
National Institute of Health Research, Box CY 573, Causeway, Harare, Zimbabwe Johns Hopkins Bloomberg School of Public Health, Department of Molecular Microbiology and Immunology, Baltimore, MD, USA c College of Health Sciences, Department of Medical Microbiology, P.O. Box A178, Avondale, Harare, Zimbabwe d University of Zimbabwe, Department of Biochemistry, P.O. Box MP167, Mount Pleasant, Harare, Zimbabwe e University of California, San Diego, Division of International Health and Cross Cultural Medicine, Department of Family and Preventive Medicine, San Diego, CA, USA f University of Edinburgh, Institute for Immunology and Infection Research, Edinburgh, UK g National Microbiology Reference Laboratory, P.O. Box ST749, Southerton, Zimbabwe h University of Zimbabwe, Faculty of Medicine, Department of Continuing Health Science, Harare, Zimbabwe b
Received 10 February 2008; received in revised form 28 May 2008; accepted 28 May 2008 Available online 24 July 2008
KEYWORDS Schistosoma; Plasmodium falciparum; Helminths; Polyparasitism; Children; Zimbabwe
∗
Summary A cross-sectional study was conducted in Zimbabwe among 1303 primary schoolchildren from a rural (53.3%) and a commercial farming area (46.7%) to determine the prevalence of co-infection by helminths and Plasmodium falciparum. Urine was examined on three successive days using the filtration method. Two stool specimens were processed using the Kato-Katz method and a third specimen was processed using the sedimentation method. Plasmodium falciparum was diagnosed from thick blood films. The prevalence of Schistosoma haematobium in the rural and farming areas was 66.8% and 52.3%, respectively, and for S. mansoni the prevalence was 12.4% and 22.7%, respectively. Plasmodium falciparum, hookworms, Ascaris lumbricoides and Trichuris trichiura occurred only in the farming area, with a prevalence of 27.9%, 23.7%, 2.1%, 2.3%, respectively. Co-infection and triple infection with schistosomes, P. falciparum and soil-transmitted helminths occurred in the commercial farming area only. Hookworm and S. mansoni infections were associated with P. falciparum malaria (P < 0.001, OR = 2.48, 95% CI 1.56—3.93 and P = 0.005, OR = 1.85, 95% CI 1.20—2.87, respectively). Overlap of helminths with malaria is a concern among primary schoolchildren and incorporating helminth control in programmes aiming to control malaria will improve funding and increase the efficiency of control for neglected tropical diseases in identified co-endemic settings. © 2008 Published by Elsevier Ltd on behalf of Royal Society of Tropical Medicine and Hygiene.
Corresponding author. Tel.: +263 04 334052; fax: +263 04 333407. E-mail address: [email protected] (T. Mduluza).
0035-9203/$ — see front matter © 2008 Published by Elsevier Ltd on behalf of Royal Society of Tropical Medicine and Hygiene. doi:10.1016/j.trstmh.2008.05.024
1040
1. Introduction Malaria is one of the most important global public health threats. It is widely distributed, with 40% of the world’s population at risk of the disease. Three hundred to 500 million persons are infected and more than one million deaths occur annually, 90% of which are in sub-Saharan Africa (WHO, 2000). Schistosomiasis is second only to malaria as a parasitic disease of public health importance in tropical and subtropical countries in Africa, the Middle East and South America (TDR, 2005), and is endemic in 76 countries (Crompton et al., 2003). Six hundred and fifty-two million people are at risk of schistosomiasis infection and 193 million are already infected (Chitsulo et al., 2000). The soil-transmitted helminths (STH): hookworms, Ascaris lumbricoides and Trichuris trichiura are also widely distributed in tropical countries (Mwangi et al., 2006), infecting 1300, 1450 and 1050 million people, respectively (Montresor et al., 2002; WHO, 2002). Among primary school-aged children, infection with schistosomiasis or STH is associated with malnutrition, anaemia, retarded growth and cognitive impairment, and furthermore, sick children are often absent from school (WHO, 2003; WHO and UNICEF, 2004). While parasitic diseases are most commonly studied individually, in reality polyparasitism is common and the high-risk population for both schistosomiasis and STH is primary school-age children. Schistosomiasis, STH and malaria are typically diseases of economically disadvantaged people who have little access to proper care or effective preventive measures (Hotez et al., 2006; Montresor et al., 2002; Mwangi et al., 2006). Schistosomes and STH are similar in that their transmission is through contamination of the environment with faecal matter and urine due to poor or absent sanitary facilities (de Silva, 2003). Overlap of schistosome species, STH and Plasmodium falciparum can be expected in areas where the conditions that favour parasitic survival and transmission are similar. Those conditions are warm temperatures, permanent bodies of water and poverty. Water development schemes for agriculture support the breeding of schistosome vector snails and vector mosquitoes, and sustain the developmental stages of their larvae. Socioeconomic factors such as a lack of insecticide-treated bed nets and shoes are also risk factors associated with polyparasitism (Mwangi et al., 2006). To our knowledge, there has not been a community-based study to investigate the combined overlap of schistosome species and STH with P. falciparum among primary schoolchildren, who still lack advanced immunity against parasitic diseases (WHO, 2004). Such studies may provide useful information to aid the development of vaccines against helminths and malaria (Mwangi et al., 2006), as co-infection may affect the efficacy of such vaccines. Community-based studies may also provide data on foci where schistosome species and STH overlap with P. falciparum. Such information is relevant to the success of the growing global initiatives to reduce the burden of morbidity due to helminth infection (Crompton et al., 2003; WHA, 2001; WHO, 2005). Only when data indicating the geographic overlap of parasitic diseases in endemic communities are available, can programme control managers prepare coordinated plans of action that describe which drugs need to be delivered in integrated control programmes. The data are
N. Midzi et al. also critically important for promoting strategies aimed at incorporating neglected diseases in the ongoing and actively funded global fight against the big three diseases, HIV, malaria and tuberculosis (TB) (Hotez et al., 2006). This study was, therefore, conducted to determine the epidemiological distribution of Schistosoma species, STH and P. falciparum, and any co-infection with helminths and P. falciparum, among primary schoolchildren living in rural and commercial farming areas in Zimbabwe.
2. Materials and methods 2.1. Study design A cross-sectional study was undertaken to provide baseline data for a longitudinal intervention study, the objective of which is to determine the effect of combined regular schoolbased deworming for schistosomiasis and STH on morbidity and malaria outcome among primary schoolchildren living in rural and commercial farming areas in Zimbabwe.
2.2. Study areas and population The study was carried out in July 2004 among 1302 primary schoolchildren living in rural (Nyamaropa) and commercial farming (Burma Valley) areas. Nyamaropa is a typical rural area located in Shamva district, 160 km north east of the capital city, Harare. The area receives high rainfall, which averages 175 mm/month during the rainy season (November—March), but is dry between May and October. The inhabitants practice subsistence farming. The major source of water is the Eben dam on the perennial River Mupfurudzi. The community has no access to piped water and draws water for domestic purposes from open wells and a few boreholes distributed in the area. During the dry season, the community is heavily involved in vegetable gardening along the rivers and near the dam. Children from this area included in the study attended Nyamaropa Primary School and were drawn from 19 villages that surround the school. Burma Valley, which borders Mozambique, is located in Mutare district, Manicaland province, about 300 km east of Harare. It receives heavy rainfall, which averages 202 mm/month in summer (November—March) and is warm to hot throughout the year. Perennial rivers and streams drain from the mountain ranges to the south. The area is divided into 12 commercial farms and two new resettlement areas. Each farm has a compound where farm labourers live. The communities living in the farm compounds use communal piped water located at strategic points. They also use communal toilets and bathrooms distributed around the compounds. The predominant commercial crops grown in the area include bananas, flowers, butternut squash and tobacco. Abundant irrigation activities keep the soil wet all year round. Three primary schools (Valhalla, Msapa and Kaswa) drawing children from the farming communities were included in our study. Demographic data, including age, gender and the village where participants lived, were recorded by a questionnaire. Ages of participants were obtained from the class registers provided by teachers.
Polyparasitism in children in Zimbabwe
2.3. Parasitological techniques Urine and faecal samples were collected between 10:00 h and 14:00 h in separate wide mouth plastic specimen bottles labelled with the laboratory identification number assigned to each individual. The samples were processed within 2 h of collection. Diagnosis of S. haematobium and intestinal helminths (S. mansoni, hookworms, T. trichiura and A. lumbricoides) was based on the detection of worm eggs in urine and faeces, respectively. Infection with S. haematobium was diagnosed using the urine filtration technique as described by Mott et al. (1982). In brief, 10 ml of urine were filtered through a Nytrel filter membrane. The filter was stained with Lugol’s iodine and examined with a light microscope using the × 10 objective. Schistosoma haematobium egg intensity was expressed as the number of eggs detected per 10 ml of urine. The same procedure was repeated on three consecutive days in order to prevent misdiagnosis due to day-to-day variation in egg excretion (Doehring et al., 1983). The overall intestinal helminth (S. mansoni and STH) infection status of participants was determined based on the combination of results from the formal ether concentration and Kato-Katz techniques in order to improve sensitivity and, hence, accuracy of diagnosis. For the formal ether concentration method, about 1 g of each specimen collected on the first day was preserved in a tube containing 10% formalin (Cheesbrough, 1998). Four qualified laboratory scientists performed microscopic examination of the processed stool specimens in order to detect S. mansoni, hookworm, T. trichiura and A. lumbricoides ova. For the quantitative Kato-Katz technique, stool specimens collected from each individual on the following two consecutive days were processed according to Katz et al. (1972). Thick faecal smears prepared using 41.7 mg plastic templates were examined within 30—60 min using a light microscope in order to detect and quantify hookworm and other STH eggs. The smears were left to clear for at least 24 h and were re-examined to detect S. mansoni eggs. The number of eggs detected from each Kato-Katz thick smear was multiplied by 24 in order to express infection intensities as the number of eggs per gram of stool. Approximately 5 ml of venous blood was drawn from willing participants in blood collection tubes containing EDTA as anticoagulant. Thick films for malaria diagnosis were prepared from fresh blood and the remaining blood was used for plasma separation. Plasmodium falciparum was diagnosed by microscopic examination of thick blood films after Giemsa staining (Cheesbrough, 1998). The presence of either ring forms or gametocytes was a conclusive diagnosis of P. falciparum infection.
2.4. Treatment Children infected with any of the schistosome species or STH were treated with praziquantel at 40 mg/kg and a single 400 mg albendazole tablet. Bread and orange juice (500 ml/child) were given after the tablets in order to reduce the nauseating effect of praziquantel. Children positive for P. falciparum were treated with a combination of
1041 chloroquine, sulfadoxine and pyrimethamine according to local malaria case-management guidelines.
2.5. Ethical considerations Provincial and district medical and education directors, chiefs, councillors and village head-men granted permission. General information regarding the nature of the study and its objectives was explained to the community and study participants. Feedback and consent were sought at schools, farms and village meetings. Inclusion of children into the study took place after free individual, parental and school authority informed written consent. Children joined the study voluntarily and were allowed to drop out at any time they wished without any prejudice.
2.6. Statistical methods Data were analysed using SPSS version 8.0 for Windows (SPSS Inc. Chicago, IL, USA). Description of the study population was done by area of residence. Prevalence of P. falciparum, schistosomes and STH among primary schoolchildren was compared for those living in rural and commercial farming areas using Pearson’s X2 test or Fisher’s exact test, where appropriate. Odds ratios (OR) were calculated for risk estimation. Mixed parasitic infections were compared for those living in rural and farming areas. The association of helminth infection with P. falciparum infection was analyzed using Pearson’s X2 test. In our study, double infection was defined as co-infection with any two parasite species. Triple infection was defined as infection with three parasite species. Statistical significance for all analyses was determined at 5% alpha level.
3. Results Overall, 1303 children were enrolled from a rural (53.3%) and a commercial farming area (46.7%). The age of participants ranged from 5—17 years. Three primary schools in the commercial farming area and one primary school in the rural area were included in the study in order to recruit an equal number of children from each area. At each school, all children from grades 1 to 6 were enrolled on a voluntary basis. The characteristics of the study population are shown in Table 1. Overall, 677 (52%) boys and 626 (48%)
Table 1
Description of the study population by area
Parameter
Overall n (%) Farming n (%) Rural n (%)
Study participants 1303 Gender Male 677 (52.0) Female 626 (48.0) Age group (years) 5—7 8—10 11—13 14—17
186 (14.3) 579 (44.4) 461 (35.4) 77 (5.9)
609 (46.7)
694 (53.3)
307 (45.3) 302 (48.2)
370 (54.7) 324 (51.8)
71 (38.2) 271 (46.8) 221 (47.9) 46 (59.7)
115 (61.8) 308 (53.2) 240 (52.1) 31 (40.3)
1042
N. Midzi et al.
girls were enrolled. Nine hundred and ninety-four children (76.3%) voluntarily gave blood. Among these, malaria testing was performed on 935 (94.1%).
3.1. Distribution of schistosomes, STH and Plasmodium falciparum The distribution of helminths and P. falciparum among primary schoolchildren living in the rural and commercial farming areas is shown in Table 2. Children living in the rural area were more likely to be infected with S. haematobium (66.8%) compared to those living in the commercial farming area (52.3%) (P < 0.001, OR = 0.54, 95% CI 0.43—0.68). The ORs for being infected with S. mansoni or hookworms for children living in the commercial farming area compared to those living in the rural area were 2.08 and 208.49, respectively. Plasmodium falciparum and STH were absent in the rural area. Hookworm was the predominant STH observed and it was more common in the commercial farming area (23.7%) than the rural area, where only one participant was infected.
3.2. Distribution of parasites by gender More boys (19%) were infected with S. mansoni compared to girls (14%) (P = 0.008). Boys had also a higher prevalence of hookworms (12.7%) compared to girls (9.1%) (P = 0.043). There were no significant differences in distribution of other helminths by gender.
3.3. Distribution of polyparasitism The distribution of mixed infection from schistosomes in the rural and commercial farming areas is shown in Table 3.
Polyparasitism was only observed among primary schoolchildren living in the commercial farming area. However, one child (0.2%) in the rural area was co-infected with schistosomes and STH, compared with 63 (12.8%) in the farming area (OR = 62.81, 95% CI 8.67—454.80, P < 0.001).
3.4. Association of helminths with Plasmodium falciparum malaria The association of helminths with P. falciparum is displayed in Table 4. Children who had hookworm infection were more likely to be infected with P. falciparum malaria (OR = 2.48, 95% CI 1.56—3.93, P < 0.001). There was also a significant association between S. mansoni and P. falciparum malaria (OR = 1.87, 95% CI 1.21—2.90, P = 0.004). There was no relationship between S. haematobium, A. lumbricoides or T. trichiura with P. falciparum malaria.
4. Discussion Our findings corroborate the results of a study undertaken in Senegal by Sokhana et al. (2004), which found a significantly higher incidence of clinical malaria among children infected with S. mansoni. The association of hookworm infection with malaria observed in our study differs with findings made by Shapiro et al. (2005), who found no association of STH with malaria in south western Uganda. In our study, S. haematobium was not associated with P. falciparum infection. Briand et al. (2005) found that children lightly infected with S. haematobium had less parasitaemia than children not infected with S. haematobium, whilst Lyke et al. (2005) reported that S. haematobium was protective against clinical malaria. Table 5 shows the prevalence of STH observed in Burma Valley by different investigators at different time points up
Table 2 Prevalence of schistosomes, soil-transmitted helminths and Plasmodium falciparum among primary schoolchildren living in commercial farming and rural areas in Zimbabwe Farming n (%)
Rural n (%)
X2 test (P-value)
Odds ratio (95% CI)
Schistosoma haematobium Examined 1279 Infected 767 (60.0)
599 313 (52.3)
680 454 (66.8)
28.48 (<0.001)
0.54 (0.43—0.68)
Schistosoma mansoni Examined 1249 Infected 214 (17.1)
577 131 (22.7)
672 83 (12.4)
12.43 (<0.001)
2.08 (1.54—2.82)
Hookworm Examined Infected
575 136 (23.7)
674 1 (0.1)
(<0.001)
208.49 (29.05—1496.27)
Ascaris lumbricoides Examined 1249 Infected 12 (1.0)
575 12 (2.1)
674 0
(<0.001)
Indeterminable
Trichuris trichiura Examined 1249 Infected 13 (1.0)
575 13 (2.3)
674 0
(<0.001)
Indeterminable
Plasmodium falciparum Examined 935 Infected 143 (15.3)
512 143 (27.9)
423 0
(0.001)
Indeterminable
Parasite
Overall n (%)
1249 137 (11.0)
Polyparasitism in children in Zimbabwe Table 3
1043
Distribution of polyparasitism among primary schoolchildren living in farming and rural areas in Zimbabwe
Parasite
Overall n (%)
Farming n (%)
Rural n (%)
Examined
915
493
422
157 (31.8) 29 (5.9) 63 (12.8) 58 (11.8)
289 (64.5) 0 1 (0.2) 0
Schistosomes 444 (48.5) STH only 29 (3.2) Schistosomes + STH 67 (7.3) Schistosomes + Plasmodium 58 (6.3) falciparum STH + Plasmodium 7 (0.8) falciparum Schistosomes + STH + 26 (2.8) Plasmodium falciparum
X2 test (P-value)
Odds ratio (95% CI)
124.91 (<0.001) (<0.001) (<0.001) (<0.001)
0.21 (0.16—0.28) Indeterminable 62.81 (8.67—454.80) Indeterminable
7(1.4)
0
(0.017)
Indeterminable
26 (5.3)
0
(<0.001)
Indeterminable
STH: soil-transmitted helminths.
Table 4 Association of helminths with Plasmodium falciparum infection among primary schoolchildren living in a farming area in Zimbabwe Malaria positive n (%)
Malaria negative n (%)
X2 (P-value)
Odds ratio (95% CI)
Schistosoma haematobium Examined 920 Positive 546 (59.3)
140 85 (60.7)
780 461 (59.1)
0.13 (0.72)
1.07 (0.74—1.55)
Schistosoma mansoni Examined Positive
906 155 (17.1)
132 34 (25.8)
774 121 (15.6)
8.15 (0.004)
1.87 (1.21—2.90)
Hookworm Examined Positive
905 117 (12.9)
131 31 (23.7)
774 86 (11.1)
15.68 (<0.001)
2.48 (1.56—3.93)
Trichuris trichiura Examined Positive
905 11 (1.2)
131 3 (2.3)
774 8 (1.0)
1.47 (0.21a )
2.24 (0.59—8.57)
Ascaris lumbricoides Examined Positive
905 8 (0.9)
131 1 (0.8)
774 7 (0.9)
0.03 (1.000a )
0.84 (0.10—6.91)
Parasite combination
a
Overall n (%)
P-value based on Fisher’s exact test.
to the present study. In all these studies, either the concentration or combined concentration technique and Kato-Katz methods were used. These studies confirm our finding that hookworm is the major geohelminth problem in the commercial farming area compared to other STH. Our results support the findings made by Brooker et al. (2006), based on geographic information systems, that hookworm is the
Table 5
most geographically widespread of the three main types of STH that occur throughout much of the African continent south of the Sahara. Table 5 shows a pattern, in which the prevalence of STH was low in 1973, then increased in 1983 and 1989, and was followed by a decline observed in our study. Chandiwana and Makaza (1983) observed that farm workers
Trends in distribution of soil-transmitted helminths in Burma Valley at different survey times since 1973
Authors
Mcdonald and Goldsmid, 1973 Chandiwana and Makaza, 1983 Chandiwana et al., 1989 Midzi et al. (current paper)
n
1543 200 1635 609
Target population
Children and adults Children and adults Children and adults Children
Prevalence of parasite Hookworm
Ascaris lumbricoides
Trichuris trichiura
26.6% 88.5% 61.7% 21%
2.2% 43.5% 2.7% 1.8%
0.3% 13.5% 2.3% 1.9%
1044 lived in poorly constructed, thatched, mud huts in overcrowded settlements sharing only four unprotected water outlets for domestic purposes. They also observed that sanitary facilities were comprised of a few poorly built and remote pit latrines, mostly unused due to unhygienic conditions, leading to indiscriminate defecation by the population. In our study, we observed that although households still shared toilets in many farm compounds, on average, four families were using a single toilet strategically constructed close to either their huts in some compounds, or to modern houses in other compounds. We also noted that ventilated pit latrines are replacing the old type. The households were also provided with communal sinks and showers for laundry and bathing, respectively. These conditions may have contributed to improved hygiene practices and increased use of latrines compared to bush toilets by the farm workers, probably resulting in reduced STH transmission. However, unlike the earlier studies, our study population did not include adults, who could have a high prevalence of hookworm infection. This could be another explanation for the observed decline in hookworm prevalence. Improvements in accommodation, water and sanitation in the farming communities seem not to have made any impact on the prevalence of schistosomiasis in Burma Valley. Chandiwana and Makaza (1983) observed 16% prevalence of S. mansoni in the Burma Valley area, whereas in our study the prevalence of S. mansoni was 22.7%. The reason could be that children have water contact activities other than bathing in unprotected water bodies (Chandiwana, 1987). Plasmodium falciparum malaria was only observed in the commercial farming area and the prevalence (27.9%) was rather too high for a community where many people are expected to be free from malaria. There were no cases in the rural area, although it is located in a district that has been classified as endemic for malaria (National Health Profile, 2002). This difference could be explained by the different malaria diagnostic methods used. Our results were based on the detection of parasites from thick blood films using a parasitological method which is reliable, whereas results from the National Health Profile reports were based on clinical diagnoses, which may not be specific to malaria, especially in this era when diseases with similar clinical symptoms, like HIV and TB, are common in malaria-endemic areas. Accurate methods, such as microscopy or rapid malaria antigen detection test kits are therefore recommended in the diagnosis of malaria. Microscopy also has an ancillary benefit of testing for drug resistance. Our finding of the occurrence of polyparasitism (Table 3) in the commercial farming area but not the rural area supports that made by Brooker et al. (2006) and the review by Hotez et al. (2006) regarding the geographic congruence of helminths and malaria infection in humans. The existence of triple infection with schistosomes, STH and P. falciparum in the Burma Valley farming area confirms that socioeconomic activities and settlement type, such as clustered and over-crowded settlements, as well as sharing toilets, are risk factors for polyparasitism. On average, four families still shared a single pit latrine in the farming communities (personal observation), a condition that may still not be acceptable to some people, leading to indiscriminate
N. Midzi et al. defaecation (Chandiwana and Makaza, 1983). Irrigation of the banana plantations all year round, except during the rainy season, maintains ponds and small pools of water that become breeding habitats for vector mosquitoes and sustain the adults and larval stages of vector snails (Chimbari et al., 2004; Mwangi et al., 2006). Irrigation activities keep the soils moist all year, making it possible for STH larvae (hookworms) and the ova of A. lumbricoides and T. trichiura, which are transmissible through oral-faecal contamination, to survive. The perennial streams that flow from a range of mountains to the east can also sustain the schistosomiasis vector snail population in the area. During the dry period, May to November, the soils are dry in the rural area, where settlements are dispersed. These conditions are not conducive to transmission of malaria and STH, even though environmental contamination may be occurring. Our study has shown geographical overlap of helminths with P. falciparum, suggesting the need to incorporate helminth control into programmes or funding opportunities for control of the big three diseases (malaria, TB and HIV/AIDS). Regular annual school-based deworming should be initiated in Zimbabwe, targeting children in schools where the prevalence of schistosomiasis is above 50%, in order to reduce the associated morbidity. Authors’ contributions: TM, NM, NK, FM, KCB, AM and GW contributed to the concept and design of the study protocol; NM, DS, AM, SZ, JM and TM carried out the clinical and parasitological assessment; TM, NM, DS and MPM carried out the analysis and interpretation of the data; NM and TM drafted the manuscript. All authors read and approved the final manuscript. TM and NM are guarantors of the paper. Acknowledgements: We thank the schoolchildren from Burma Valley and Shamva, Nyamaropa who participated in the study, and the parents and teachers for permitting their children to take part. We thank the provincial medical and education directors for Manicaland and Mashonaland Central for granting permission to conduct the study in their respective areas. Thanks are addressed to the laboratory technical staff from the National Institute of Health Research. We thank Prof. Anthony Butterworth for all the constructive comments he gave leading to the present state of the manuscript. Acknowledgements also go to the Schistosomiasis Control Initiative (SCI), Imperial College, UK, which supported the programme with anthelminthic drugs (praziquantel). Funding: The UNICEF/UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases Grant A60125, ENHR-Ministry of Health Zimbabwe, Fogarty Grant for field work to NK and DS. International Foundation for Science Grantee: W/4321-1 to TM. Conflicts of interest: None declared.
Polyparasitism in children in Zimbabwe Ethical approval: The Medical Research Council of Zimbabwe gave ethical approval for the study.
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