webuye health and demographic surveillance systems

8
Hindawi Publishing Corporation Journal of Tropical Medicine Volume 2013, Article ID 734562, 7 pages http://dx.doi.org/10.1155/2013/734562 Research Article Webuye Health and Demographic Surveillance Systems Baseline Survey of Soil-Transmitted Helminths and Intestinal Protozoa among Children up to Five Years A. A. Obala, 1 C. J. Simiyu, 1 D. O. Odhiambo, 1 V. Nanyu, 1 P. Chege, 1 R. Downing, 1 E. Mwaliko, 1 A. W. Mwangi, 1 D. Menya, 2 D. Chelagat, 3 H. D. N. Nyamogoba, 1 P. O. Ayuo, 1 W. P. O’Meara, 2,4 M. Twagirumukiza, 5 D. Vandenbroek, 5 B. B. O. Otsyula, 1 and J. de Maeseneer 5 1 School of Medicine, Moi University, Kenya 2 School of Public Health, Moi University, Kenya 3 School of Nursing, Moi University, Kenya 4 Duke University, USA 5 Ghent University, Belgium Correspondence should be addressed to A. A. Obala; [email protected] Received 31 October 2012; Accepted 23 January 2013 Academic Editor: Aditya Prasad Dash Copyright © 2013 A. A. Obala et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. e intestinal parasitic infections (IPIs) are globally endemic, and they constitute the greatest cause of illness and disease worldwide. Transmission of IPIs occurs as a result of inadequate sanitation, inaccessibility to potable water, and poor living conditions. Objectives. To determine a baseline prevalence of IPIs among children of five years and below at Webuye Health and Demographic Surveillance (HDSS) area in western Kenya. Methods. Cross-sectional survey was used to collect data. Direct saline and formal-ether-sedimentation techniques were used to process the specimens. Descriptive and inferential statistics such as Chi-square statistics were used to analyze the data. Results. A prevalence of 52.3% (417/797) was obtained with the male child slightly more infected than the female (53.5% versus 51%), but this was not significant ( 2 = 0.482, > 0.05). Giardia lamblia and Entamoeba histolytica were the most common pathogenic IPIs with a prevalence of 26.1% (208/797) and 11.2% (89/797), respectively. Soil-transmitted helminths (STHs) were less common with a prevalence of 4.8% (38/797), 3.8% (30/797), and 0.13% (1/797) for Ascaris lumbricoides, hookworms, and Trichuris trichiura, respectively. Conclusions. Giardia lamblia and E. histolytica were the most prevalent pathogenic intestinal protozoa, while STHs were less common. Community-based health promotion techniques are recommended for controlling these parasites. 1. Introduction It is estimated that approximately a billion people in devel- oping countries of the sub-Saharan Africa, Asia, and the Americas are infected with one or more helminths [1]. About 300 million people are severely ill with intestinal parasitic infections (IPIs), out of which, approximately 50% are school- age children [2]. e IPIs are globally endemic and are responsible for the greatest worldwide cause of illnesses and disease [3, 4]. ese parasites cause high morbidity in school children and women during child-bearing age. e IPIs occur wherever there are poor living conditions, which immensely contribute to economic loss and poor health [1, 3, 4]. Ascaris lumbricoides, Trichuris trichiura, and hookworm species, collectively referred to as soil-transmitted helminths (STHs), are the most common intestinal parasites known to mankind [5]. Bethony et al. [5] have observed that children living in less developed countries are likely to be infected with one or more STH. Infections with these parasites affect the physical and cognitive development of school-age children

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Page 1: Webuye Health and Demographic Surveillance Systems

Hindawi Publishing CorporationJournal of Tropical MedicineVolume 2013 Article ID 734562 7 pageshttpdxdoiorg1011552013734562

Research ArticleWebuye Health and Demographic Surveillance Systems BaselineSurvey of Soil-Transmitted Helminths and Intestinal Protozoaamong Children up to Five Years

A A Obala1 C J Simiyu1 D O Odhiambo1 V Nanyu1 P Chege1 R Downing1

E Mwaliko1 A W Mwangi1 D Menya2 D Chelagat3 H D N Nyamogoba1

P O Ayuo1 W P OrsquoMeara24 M Twagirumukiza5 D Vandenbroek5

B B O Otsyula1 and J de Maeseneer5

1 School of Medicine Moi University Kenya2 School of Public Health Moi University Kenya3 School of Nursing Moi University Kenya4Duke University USA5Ghent University Belgium

Correspondence should be addressed to A A Obala andrewobalagmailcom

Received 31 October 2012 Accepted 23 January 2013

Academic Editor Aditya Prasad Dash

Copyright copy 2013 A A Obala et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Background The intestinal parasitic infections (IPIs) are globally endemic and they constitute the greatest cause of illness anddisease worldwide Transmission of IPIs occurs as a result of inadequate sanitation inaccessibility to potable water and poorliving conditions Objectives To determine a baseline prevalence of IPIs among children of five years and below at Webuye Healthand Demographic Surveillance (HDSS) area in western Kenya Methods Cross-sectional survey was used to collect data Directsaline and formal-ether-sedimentation techniques were used to process the specimens Descriptive and inferential statistics suchas Chi-square statistics were used to analyze the data Results A prevalence of 523 (417797) was obtained with the male childslightly more infected than the female (535 versus 51) but this was not significant (1205942 = 0482 119875 gt 005) Giardia lamblia andEntamoeba histolyticawere themost common pathogenic IPIs with a prevalence of 261 (208797) and 112 (89797) respectivelySoil-transmitted helminths (STHs) were less common with a prevalence of 48 (38797) 38 (30797) and 013 (1797) forAscaris lumbricoides hookworms and Trichuris trichiura respectively Conclusions Giardia lamblia and E histolytica were themost prevalent pathogenic intestinal protozoa while STHs were less common Community-based health promotion techniquesare recommended for controlling these parasites

1 Introduction

It is estimated that approximately a billion people in devel-oping countries of the sub-Saharan Africa Asia and theAmericas are infected with one or more helminths [1] About300 million people are severely ill with intestinal parasiticinfections (IPIs) out of which approximately 50 are school-age children [2] The IPIs are globally endemic and areresponsible for the greatest worldwide cause of illnesses anddisease [3 4] These parasites cause high morbidity in school

children andwomen during child-bearing ageThe IPIs occurwherever there are poor living conditions which immenselycontribute to economic loss and poor health [1 3 4]

Ascaris lumbricoides Trichuris trichiura and hookwormspecies collectively referred to as soil-transmitted helminths(STHs) are the most common intestinal parasites known tomankind [5] Bethony et al [5] have observed that childrenliving in less developed countries are likely to be infectedwithone or more STH Infections with these parasites affect thephysical and cognitive development of school-age children

2 Journal of Tropical Medicine

[5] Similarly Giardia lamblia infects about 200 millionpeople and is themost common parasitic protozoan flagellateworldwide [6 7] Like in other parts of the world [8] it hasbeen documented that in western Kenya [9] the hookwormand other parasitic infections affect the haemoglobin and ironstatus of the children and adults In the Republic of SouthAfrica Appleton et al [10] have cautioned that the rate ofreinfections with STH in urban slums is alarmingly highwhich negates the benefits of treatment alone as a meansof containing the parasitic infections among the endemicpopulations

In a survey that involved 390 participants in other partsof western Kenya 762 had at least one STH and itshowed that hookworm infections were associatedwith lowerhemoglobin resulting in anaemia [11] Nokes et al [12] havealso investigated the impacts ofT trichiura in school childrenof 9ndash12 years and found that expulsion of the worms resultedin a significant improvement in tests of auditory short-termmemory and a highly significant improvement in retrieval oflong-term information

The IPIs are common in rural western Kenya [9] but theprevalence of these parasites among children of five years andbelow has not been documented in the Webuye Health andDemographic Surveillance System (HDSS) area The data wereport was obtained from a community-based survey andthe participants were younger compared to those who haveparticipated inmost studies conducted in western Kenya [11]However based on reports from other studies [5 9 11] weexpected the prevalence of IPIs to be high and documentingthis would help in planning intervention strategies Thisstudy was initiated after our first round data collection at theWebuye HDSS [13] and the Webuye District Hospital annualreport for 2008 [14] which showed intestinal parasites rankedhigh in the health facility records

2 Materials and Methods

21 Study Site This survey was conducted at Webuye HDSSarea (Figure 1) which is located at Webuye Division ofBungoma County at an elevation of 1523m above sea levelThe area has a tropical climate and the land is mainly usedfor subsistence agriculture It lies at a latitude of 06166667∘and a longitude of 347666667∘ During the study periodthe temperatures ranged between 15 and 20∘C to 23 and30∘C forminimumandmaximum temperatures respectivelyThe region receives high rainfall ranging from 1200mm to1800mm annually The first rains come in March to Julyand the second one occurs from September to October[15] The Webuye HDSS area comprises six sublocations inWebuye Division of Bungoma County Kenya The study siteis exhaustively described elsewhere [16]

22 Study Population The Webuye HDSS area has a well-defined population of about 80000 people living in approxi-mately 13478 households in six sublocations within WebuyeDivisionTheparticipantswere selected fromamong childrenbetween 1 and 60 months who were captured in the WebuyeHDSS database

23 Sample Size This being a prevalence study the samplesize was calculated using Fischerrsquos formula as used by O MMugenda and A G Mugenda [17] which is as follows 119899 =1199112

120572119901(1 minus 119901)119889

2 where 119911 is the standard normal deviate = 196for a 95 level of significance 119901 = 50 is the prevalence ratefrom other studies and 119889 = 004 is the degree of accuracyTherefore 119899 = 196205(1 minus 05)0042 = 600 To account forattritionrefusalsinability to produce stool specimen whenrequired we inflated the sample size by 30 and arrived at aminimum sample of size 780 of children who were recruitedin the study

24 Study Design Sampling Frame and Sampling TechniquesCross-sectional design was used to collect the data for thissurvey Seven hundred and ninety seven (797) children wererecruited from about 10000 children of 5 years and belowProportionate sampling was used to determine the numberof children recruited from each sublocation The villageeldersrsquo compounds were used as the reference points in eachvillage and an interval of 16 was used to identify subsequentcompounds The numbers of children recruited from eachsublocation were as follows 104 132 220 122 103 and 99for Malaha Matulo Misikhu Maraka Milo and Kitunirespectively as shown in Table 1 If a child of the required agewas not found in the selected compound the next one wherechildren of this age groupwere found and the head consentedwas recruited

Only children of five years and below who were residentsof Webuye and satisfied the criteria for inclusion in WebuyeHDSS database were recruited Joint Institutional Researchand Ethics Committee (IREC) of the Moi Teaching andReferral Hospital (MTRH) and the School of Medicine MoiUniversity Eldoret approved the proposal of this project viaclearance certificate no IREC2010100 of 1592010

25 Stool Specimen Processing and Examination This surveywas conducted between September andDecember 2010 Onlyone specimen from each participating child was collectedbetween 800 and 1100 hours each day The specimens weretransported for processing and examination at the Schoolof Medicine Eldoret between three to four hours aftercollectionWetmounts were prepared from each specimen todetermine the presence of intestinal protozoan trophozoitesafter which they were further processed using formal-ether-sedimentation technique previously described [18] to identifyhelminths ova and protozoan cysts Briefly a pie-size stoolspecimen was emulsified in 5ml 10 formalin and thepreparation was strained through three layers of wet gauze4ml diethyl ether was added and the mixture was shakenvigorously for about 30 seconds and centrifuged at 2000 rpmfor about 5 minutes The supernatant was decanted and thesediment dislodged using applicator stick A portion of thepreparation was transferred to a clean glass slide containing1-2 drops of 1 Lugolrsquos iodine A cover glass was applied andthe preparation was examined for ova and cysts

26 Data Handling and Analysis The data for this surveywere stored in an Excel spreadsheet after which they were

Journal of Tropical Medicine 3

N

EW

S

0∘459984000998400998400N

0∘409984000998400998400N

0∘359984000998400998400N

0∘309984000998400998400N

4 2 0(Kilometers)

34∘409984000998400998400E 34

∘459984000998400998400E

Compiled by Ochieng Teddy June 2008

Study sites

KituniMalahaMarakaMatuloMiloMisikhu

Roads

bound surfaceAll weather roads

Dry weather roadsMajor tracks (motorable)Railway line

Town centersMarket centerTownshiptownRivers

Health facilities

Schools

Webuye division disease surveillance sites

Figure 1 Webuye Health and Demographic Surveillance System area

imported into SPSS version 125 database for statistical anal-ysis Descriptive statistics such as mean median standarddeviation and ranges were carried out for continuous datawhile frequency listing and percentages were used to explorecategorical data To assess whether there was any associationbetween the categorical variables Pearsonrsquos Chi-square testwas used In all analyses a 119875 value less than 005 wasconsidered significant

3 Results and Discussion

31 Results This cross-sectional survey recruited 797 chil-dren of which 411 (516) and 386 (484) were boysand girls respectively Overall intestinal parasite prevalenceof 523 (417797) was obtained among children of fiveyears and below in the Webuye HDSS The male child wasslightly more infected than the female in all age group

4 Journal of Tropical Medicine

Table 1 The numbers of households allocated in each sublocationin Webuye HDSS

Sublocation Nos ofhouseholds

Samplingintervals

Targetedhouseholds

Malaha 1802 16 104Matulo 2272 16 132Misikhu 3792 16 220Maraka 2115 16 122Milo 1786 16 103Kituni 1711 16 99Total 13478 mdash 780

categories with greatest difference shown between 25 and48 months age group (Figure 2) However there were nosignificant differences in infections between male and femalechildren (53 versus 51 1205942 = 0482 119875 gt 005)Giardia lamblia was the most common pathogenic intestinalprotozoan flagellate with an overall prevalence of 261(208797) compared to Entamoeba histolytica which was112 (89797) Among nonpathogenic intestinal protozoafound in all age groups Entamoeba coli was the mostprevalent (180 150797) Other nonpathogenic protozoaidentified included Endolimax nana Iodomoeba butschliiand Chilomastix mesnili which are nonpathogenic protozoawere also identified (Table 1) Soil-transmitted helminthswere comparatively less common with a prevalence of 48(38797) 38 (30797) and 013 (1797) for Ascaris lum-bricoides Hookworm species and Trichuris trichiura respec-tivelyTaenia species was only encountered once among theserural children population (Table 2) The children participat-ing in this survey were age stratified and approximately 60(476797) were between the age group 24ndash48 months out ofwhich 744 (354476) had either parasitic helminths (9244476) or protozoan infections (651 310476) Infectionwith any parasites declined considerably after 48 months(Table 2)

Single and double parasitic infections per childweremoreprevalent (252 201797 137 109797 resp) compared toonly 113 (91797) polyparasitisms (ge3 parasitesindividual)obtained among these rural children Similarly polypara-sitisms were found more frequently in protozoa than inhelminthic infections (Figure 3) Dual infections with STHwere less comdmon with only about 05 (4797) childrenwho had both A lumbricoides and hookworm compared to38 (30797) children with E histolytica and G lambliacombination The majority (26 20797) of the childrencoinfected with E histolytica and G lamblia fall between ge25and 48 months age group (Table 3)

32 Discussion The prevalence of intestinal parasites foundat Webuye HDSS area among children of five years andbelow was moderately high and was slightly higher amongstmale children than the female These results concur withthose previously reported [19ndash22] Giardia lamblia was themost common intestinal parasite among our study partici-pants which is also comparable to the results reported by

0

50

100

150

200

250

0

50

100

150

200

250

300

STH

pat

hoge

nic p

roto

zoa

Mal

e and

fem

ale c

hild

ren

Age groups (month)

MalesFemales

STHEhGl

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 2 Soil-transmitted helminths (STHs) and pathogenic proto-zoan parasites among male and female children participants STHssoil-transmitted helminthes EhGl Entamoeba histolyticaGiardialamblia

Mehraj et al [19] who found a similar trend in KarachiPakistan Pillai and Kain [6] andMinenoa and Avery [7] havealso showed that G lamblia is the most prevalent protozoanparasite worldwide with about 200 million people infectedMehraj et al [19] attributed intestinal parasitic infectionspartly to poverty illiteracy poor hygiene inaccessibility topotable water and humid tropical climate These conditionsare somewhat similar to those found in Webuye HDSS areawhere we conducted our study This community has highaccessibility to water however water obtained from thesesources could be contaminated as shown by first-roundWebuye HDSS data [13] Furthermore poverty incidencelevels are high and are estimated between 56 and 60 inBungoma County [15] which could predispose them toparasitic infection

The present survey has shown that mixed infectionswithin STH were less common with only a few childrenfound with both A lumbricoides and hookworms comparedto those coinfected with E histolytica and G lamblia Themajority (26) of those who hadmixed protozoan infectionswere children between ge25 and 48 months These childrenalso had high IPIs infectivity rates This age group fallwithin the period when children are increasingly involvedin outdoor activities including handling fecal contaminatedmaterials which predispose them to parasitic infectionsInfection with any parasites declined considerably after 48months partly because of the deworming program initiatedby the Kenya Governmentrsquos Ministry of Public Health andSanitation which target school-age children between 5ndash12 years old [23] This program also targets the youngerchildren but with a few benefit because they require parentalescort to access these services whenever it is available atthe nearby primary schools However the parents are oftenengaged in other daily cores and would seldom rememberthe deworming schedule In Pakistan Chaudhry et al [24]have also reported a decline in parasitic infection after theage of 2 years but they did not offer any explanation forthis

Journal of Tropical Medicine 5

Table 2 Types and prevalence of intestinal parasites (percentages are in parentheses)

Variables Femalemale Total119875-valueGender distribution 119899 = 386 119899 = 411 119899 = 797

All parasitic infections 197 (510) 220 (535) 417 (523) 0482Ascaris lumbricoides 19 (49) 19 (46) 38 (48) 0843Hookworm spp 10 (26) 20 (49) 30 (38) 0092Trichuris trichiura 0 1 (02) 1 (013) mdashTaenia spp 0 1 (02) 1 (013) mdashEntamoeba histolytica 35 (91) 51 (124) 86 (112) 0129Giardia lamblia 100 (259) 108 (263) 208 (261) 0905Entamoeba coli 76 (197) 74 (192) 150 (188) 0543Endolimax nana 74 (192) 55 (134) 129 (162) 0027Chilomastix mesnili 16 (42) 15 (37) 31 (38) 0718Iodomoeba butschlii 16 (42) 10 (24) 26 (33) 0174

Table 3 Mixed infections of specific soil-transmitted helminths and pathogenic protozoa in each age group

Age group AH AG HG AEH GEH AHEH AGEH TEH HGEH Total1 ge 24months 1 3 0 0 5 0 0 0 0 925 ge 48months 2 2 5 2 20 1 1 1 0 3449 ge 60months 1 1 1 0 4 0 0 0 1 8gt60 months 0 0 0 0 1 0 0 0 1 2Total 4 6 6 2 30 1 1 1 2 53Key A Ascaris spp H Hookworm spp G G lamblia EH E histolytica and T Taenia spp

0

20

40

60

80

100

120

140

F M F M F M F M

Num

ber o

f par

asite

s

Age groups (months)

Five parasitesFour parasitesThree parasites

Two parasitesSingle parasite

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 3 Patterns of single double and polyparasitisms amongchildren participants in each age group

Single and double parasitic infections per child weremore common compared to polyparasitism probably due tothe restricted transmission potential which limited multipleinfections among these rural children Polyparasitism wascommon within the protozoa than in helminthic infectionsbut this was probably the outcome of a more hostile weather

to the mode of transmission of helminths [25] It is debat-able whether polyparasitisms confer any advantage to thoseinfected According to a report by Jardim-Botelho et al [26]children coinfected with A lumbricoides and hookwormsin Brazil had greater odds of poor performance in classthan those infected with A lumbricoides alone Keusch andMigasena [27] have suggested possible synergistic effects ofpolyparasitisms but this is inconclusive due to very fewanalyzed data

Surprisingly it appeared from our data that the preva-lence of soil-transmitted helminths was low compared to thepathogenic protozoa such asE histolytica andG lamblia sug-gesting that there could be factors mitigating low prevalenceof STH at Webuye HDSS area Furthermore a similar surveyinvolving women in a nearby rural western Kenya reported762 infectivity rate with at least one geohelminth comparedto our data (88) [11] This requires further investigationsHowever accessibility of improved hygiene and sanitationand awareness of the diseases associated with lack of access topotable water could be one plausible explanation for low STHprevalence within this community [12 13] Access to shallowwells in Webuye HDSS area is moderately high (461)which minimizes transmission potential of one member ofSTH group hookworm species which is transmitted bylarval penetration of the skin in surface water [12 25]The transmission of the other two members of STH Alumbricoides and T trichiura is feco-oral requiring suitableenvironment for egg maturation survival and transmissionBut this is partly hampered by the climate which has a wet

6 Journal of Tropical Medicine

spell between September andDecember each year during theperiod which temperatures may be conducive but the type ofsoils found in Webuye is mostly clay enriched which mostprobably hold on to the eggs This type of soils also retainsheat for long periods which is inimical to the developmentand dispersion of helminths eggs [28 29] The childreninfected with intestinal parasites were treated at WebuyeDistrict Hospital and other nearby health facilities howeverhelminths egg counts and anthropometric measurementswere not undertaken to provide the baseline informationupon which future studies can be assessed

4 Conclusions and Recommendations

Giardia lamblia and E histolytica were the most prevalentpathogenic intestinal protozoa while STHs were less com-mon among these rural children Further research is requiredto elucidate the factors responsible for low STH prevalenceamong this rural children population The parasites reportedhere are feco-orally transmitted and can easily be containedby the improvement of environmental hygiene Community-based health promotions including regular checkups andtreatment and personal and environmental hygiene arehighly recommended for the control of the intestinal parasitesinfesting children at Webuye HDSS area

Conflict of Interests

The authors declare no conflict of interests The studymethodology execution report and conclusion reflect solelythe authorsrsquo research and scientific work and are not theresponsibility of affiliate institutions or the funding organi-zations

Authorsrsquo Contribution

A A Obala C J Simiyu D O Odhiambo H D NNyamogoba D Menya P O Ayuo R Downing D ChelagatA W Mwangi P Chege and W P Orsquo Meara designed thestudy and took part in data collection processing and analy-sis and paper writing M Twagirumukiza D VandenbroekB B O Otsyula and J de Maeseneer critically reviewed thepaper during preparation

Acknowledgments

The authors acknowledge the assistance received from theProvincial Administration and other stakeholders formakingit possible to access the community They thank Webuyeresidents for their cooperation and for accepting to partic-ipate in this study They acknowledge the assistance of theWebuye HDSS project field supervisors and enumeratorsfor supervision of field activities and specimen collectionrespectively Mr Arthur Aroko Ms Edna Kurgat Mr IsaacMutai and Mr Paul Olang processed and examined thespecimen for which they are very grateful They thank theDeans of Schools of Medicine Public Health and Nursingfor granting them permission to collect data and compile

this report Funds for this project were provided by theMoi University (Kenya)mdashVLIRUOS (Belgium) collaborativeprogramme

References

[1] P J Hotez P J Brindley J M Bethony C H King E J Pearceand J Jacobson ldquoHelminth infections the great neglectedtropical diseasesrdquo Journal of Clinical Investigation vol 118 no4 pp 1311ndash1321 2008

[2] S Waqar H Hussain R Khan et al ldquoIntestinal parasitic infec-tions in children from the Northern Pakistanrdquo Infectious Dis-eases Journal vol 12 pp 73ndash77 2003

[3] R W Steketee ldquoPregnancy nutrition and parasitic diseasesrdquoJournal of Nutrition vol 133 pp 1661Sndash1667S 2003

[4] F Curtale P Pezzotti A L Sharbini et al ldquoKnowledge per-ceptions and behaviour of mothers toward intestinal helminthsin Upper Egypt implications for controlrdquo Health Policy andPlanning vol 13 no 4 pp 423ndash432 1998

[5] J Bethony S Brooker M Albonico et al ldquoSoil-transmittedhelminth infections ascariasis trichuriasis and hookwormrdquoThe Lancet vol 367 no 9521 pp 1521ndash1532 2006

[6] D R Pillai and K C Kain ldquoCommon intestinal parasitesrdquoCurrent Treatment Options in Infectious Diseases vol 5 pp 207ndash217 2003

[7] T Minenoa and M A Avery ldquoGiardiasis recent progress inchemotherapy and drug developmentrdquo Current PharmaceuticalDesign vol 9 pp 841ndash855 2003

[8] R Ndyomugyenyi N Kabatereine A Olsen and PMagnussenldquoMalaria and hookworm infections in relation to haemoglobinand serum ferritin levels in pregnancy in Masindi districtwestern Ugandardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 102 no 2 pp 130ndash136 2008

[9] A Olsen PMagnussen J H Ouma J Andreassen andH FriisldquoThe contribution of hookworm and other parasitic infectionsto haemoglobin and iron status among children and adults inwestern Kenyardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 92 no 6 pp 643ndash649 1998

[10] C C Appleton T I Mosala J Levin and A Olsen ldquoGeo-helminth infection and re-infection after chemotherapy amongslum-dwelling children in Durban South Africardquo Annals ofTropical Medicine and Parasitology vol 103 no 3 pp 249ndash2612009

[11] A M van Eijk K A Lindblade F Odhiambo et al ldquoGeo-helminth infections among pregnant women in rural westernKenya a cross-sectional studyrdquo PLoS Neglected Tropical Dis-eases vol 3 no 1 article e370 2009

[12] C Nokes S M Grantham-McGregor A W Sawyer E SCooper B A Robinson and D A P Bundy ldquoModerate toheavy infections of Trichuris trichiura affect cognitive functionin Jamaican school childrenrdquo Parasitology vol 104 no 3 pp539ndash547 1992

[13] Webuye Health and Demographic Surveillance System FactSheet no 1 2009 Unpublished data

[14] Webuye District Hospital Annual Report 2008 Unpublisheddata

[15] Webuye Climate Pattern 2012 httpenwikipediaorgwikiWebuye

[16] C J Simiyu V Naanyu A Obala et al ldquoEstablishing webuyehealth and demographic surveillance site in rural western

Journal of Tropical Medicine 7

Kenya challenges and lessons learnedrdquo in Population Associ-ation of America Annual Meeting Problem New Orleans LaUSA April 2013

[17] O M Mugenda and A G Mugenda Research MethodsQuantitative and Qualitative Approaches African Centre ofTechnology Studies Nairoibi Kenya 1999

[18] L S Ritchie ldquoAn ether sedimentation technique for rou-tine stool examinationrdquo Bulletin United States Army MedicalDepartment vol 8 article 326 1948

[19] V Mehraj J Hatcher S Akhtar G Rafique and M A BegldquoPrevalence and factors associated with intestinal parasiticinfection among children in an urban slum of Karachirdquo PLoSONE vol 3 no 11 Article ID e3680 2008

[20] Z Tahir ldquoComparasion of prevalence of intestinal parasites inchildren and adult populationrdquo Biomedica vol 18 pp 74ndash752002

[21] V Srinivasan S Radhakrishna A M Ramanathan and SJabbar ldquoHookworm infection in a rural community in SouthIndia and its association with haemoglobin levelsrdquo Transactionsof the Royal Society of Tropical Medicine andHygiene vol 81 no6 pp 973ndash977 1987

[22] M I Siddiqui F M Bilqees M Iliyas and S PerveenldquoPrevalence of parasitic infections in a rural area of KarachiPakistanrdquo Journal of the Pakistan Medical Association vol 52no 7 pp 315ndash320 2002

[23] Kenya National School-Based Deworming Program httpwwwdewormtheworldorgour-workkenya-national-school-based-deworming-program

[24] Z H Chaudhry M Afzal and M A Malik ldquoEpidemiologicalfactors affecting prevalence of intestinal parasites in children ofMuzaffarabad districtrdquo Pakistan Journal of Zoology vol 36 no4 pp 267ndash271 2004

[25] RMullerWorms andDisease AManual ofMedicalHelminthol-ogy Butler and Tanners 1975

[26] A Jardim-Botelho S Raff R D A Rodrigues et al ldquoHook-worm Ascaris lumbricoides infection and polyparasitism asso-ciated with poor cognitive performance in Brazilian schoolchil-drenrdquo Tropical Medicine and International Health vol 13 no 8pp 994ndash1004 2008

[27] G T Keusch and P Migasena ldquoBiological implications ofpolyparasitismrdquo Reviews of Infectious Diseases vol 4 no 4 pp880ndash882 1982

[28] Webuye economic activities and soil types httpwwwchincicomtravelpaxq178201WebuyeKEKenya0

[29] FAO Corporate Document Repository 1988 ldquoManagement ofVertisols in sub-Saharan Africardquo in Proceedings of a Confer-ence Held at ILCA Addis Ababa Ethiopia September 1987httpwwwfaoorgWairdocsILRIx5493Ex5493e00htm

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Parkinsonrsquos DiseaseHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 2: Webuye Health and Demographic Surveillance Systems

2 Journal of Tropical Medicine

[5] Similarly Giardia lamblia infects about 200 millionpeople and is themost common parasitic protozoan flagellateworldwide [6 7] Like in other parts of the world [8] it hasbeen documented that in western Kenya [9] the hookwormand other parasitic infections affect the haemoglobin and ironstatus of the children and adults In the Republic of SouthAfrica Appleton et al [10] have cautioned that the rate ofreinfections with STH in urban slums is alarmingly highwhich negates the benefits of treatment alone as a meansof containing the parasitic infections among the endemicpopulations

In a survey that involved 390 participants in other partsof western Kenya 762 had at least one STH and itshowed that hookworm infections were associatedwith lowerhemoglobin resulting in anaemia [11] Nokes et al [12] havealso investigated the impacts ofT trichiura in school childrenof 9ndash12 years and found that expulsion of the worms resultedin a significant improvement in tests of auditory short-termmemory and a highly significant improvement in retrieval oflong-term information

The IPIs are common in rural western Kenya [9] but theprevalence of these parasites among children of five years andbelow has not been documented in the Webuye Health andDemographic Surveillance System (HDSS) area The data wereport was obtained from a community-based survey andthe participants were younger compared to those who haveparticipated inmost studies conducted in western Kenya [11]However based on reports from other studies [5 9 11] weexpected the prevalence of IPIs to be high and documentingthis would help in planning intervention strategies Thisstudy was initiated after our first round data collection at theWebuye HDSS [13] and the Webuye District Hospital annualreport for 2008 [14] which showed intestinal parasites rankedhigh in the health facility records

2 Materials and Methods

21 Study Site This survey was conducted at Webuye HDSSarea (Figure 1) which is located at Webuye Division ofBungoma County at an elevation of 1523m above sea levelThe area has a tropical climate and the land is mainly usedfor subsistence agriculture It lies at a latitude of 06166667∘and a longitude of 347666667∘ During the study periodthe temperatures ranged between 15 and 20∘C to 23 and30∘C forminimumandmaximum temperatures respectivelyThe region receives high rainfall ranging from 1200mm to1800mm annually The first rains come in March to Julyand the second one occurs from September to October[15] The Webuye HDSS area comprises six sublocations inWebuye Division of Bungoma County Kenya The study siteis exhaustively described elsewhere [16]

22 Study Population The Webuye HDSS area has a well-defined population of about 80000 people living in approxi-mately 13478 households in six sublocations within WebuyeDivisionTheparticipantswere selected fromamong childrenbetween 1 and 60 months who were captured in the WebuyeHDSS database

23 Sample Size This being a prevalence study the samplesize was calculated using Fischerrsquos formula as used by O MMugenda and A G Mugenda [17] which is as follows 119899 =1199112

120572119901(1 minus 119901)119889

2 where 119911 is the standard normal deviate = 196for a 95 level of significance 119901 = 50 is the prevalence ratefrom other studies and 119889 = 004 is the degree of accuracyTherefore 119899 = 196205(1 minus 05)0042 = 600 To account forattritionrefusalsinability to produce stool specimen whenrequired we inflated the sample size by 30 and arrived at aminimum sample of size 780 of children who were recruitedin the study

24 Study Design Sampling Frame and Sampling TechniquesCross-sectional design was used to collect the data for thissurvey Seven hundred and ninety seven (797) children wererecruited from about 10000 children of 5 years and belowProportionate sampling was used to determine the numberof children recruited from each sublocation The villageeldersrsquo compounds were used as the reference points in eachvillage and an interval of 16 was used to identify subsequentcompounds The numbers of children recruited from eachsublocation were as follows 104 132 220 122 103 and 99for Malaha Matulo Misikhu Maraka Milo and Kitunirespectively as shown in Table 1 If a child of the required agewas not found in the selected compound the next one wherechildren of this age groupwere found and the head consentedwas recruited

Only children of five years and below who were residentsof Webuye and satisfied the criteria for inclusion in WebuyeHDSS database were recruited Joint Institutional Researchand Ethics Committee (IREC) of the Moi Teaching andReferral Hospital (MTRH) and the School of Medicine MoiUniversity Eldoret approved the proposal of this project viaclearance certificate no IREC2010100 of 1592010

25 Stool Specimen Processing and Examination This surveywas conducted between September andDecember 2010 Onlyone specimen from each participating child was collectedbetween 800 and 1100 hours each day The specimens weretransported for processing and examination at the Schoolof Medicine Eldoret between three to four hours aftercollectionWetmounts were prepared from each specimen todetermine the presence of intestinal protozoan trophozoitesafter which they were further processed using formal-ether-sedimentation technique previously described [18] to identifyhelminths ova and protozoan cysts Briefly a pie-size stoolspecimen was emulsified in 5ml 10 formalin and thepreparation was strained through three layers of wet gauze4ml diethyl ether was added and the mixture was shakenvigorously for about 30 seconds and centrifuged at 2000 rpmfor about 5 minutes The supernatant was decanted and thesediment dislodged using applicator stick A portion of thepreparation was transferred to a clean glass slide containing1-2 drops of 1 Lugolrsquos iodine A cover glass was applied andthe preparation was examined for ova and cysts

26 Data Handling and Analysis The data for this surveywere stored in an Excel spreadsheet after which they were

Journal of Tropical Medicine 3

N

EW

S

0∘459984000998400998400N

0∘409984000998400998400N

0∘359984000998400998400N

0∘309984000998400998400N

4 2 0(Kilometers)

34∘409984000998400998400E 34

∘459984000998400998400E

Compiled by Ochieng Teddy June 2008

Study sites

KituniMalahaMarakaMatuloMiloMisikhu

Roads

bound surfaceAll weather roads

Dry weather roadsMajor tracks (motorable)Railway line

Town centersMarket centerTownshiptownRivers

Health facilities

Schools

Webuye division disease surveillance sites

Figure 1 Webuye Health and Demographic Surveillance System area

imported into SPSS version 125 database for statistical anal-ysis Descriptive statistics such as mean median standarddeviation and ranges were carried out for continuous datawhile frequency listing and percentages were used to explorecategorical data To assess whether there was any associationbetween the categorical variables Pearsonrsquos Chi-square testwas used In all analyses a 119875 value less than 005 wasconsidered significant

3 Results and Discussion

31 Results This cross-sectional survey recruited 797 chil-dren of which 411 (516) and 386 (484) were boysand girls respectively Overall intestinal parasite prevalenceof 523 (417797) was obtained among children of fiveyears and below in the Webuye HDSS The male child wasslightly more infected than the female in all age group

4 Journal of Tropical Medicine

Table 1 The numbers of households allocated in each sublocationin Webuye HDSS

Sublocation Nos ofhouseholds

Samplingintervals

Targetedhouseholds

Malaha 1802 16 104Matulo 2272 16 132Misikhu 3792 16 220Maraka 2115 16 122Milo 1786 16 103Kituni 1711 16 99Total 13478 mdash 780

categories with greatest difference shown between 25 and48 months age group (Figure 2) However there were nosignificant differences in infections between male and femalechildren (53 versus 51 1205942 = 0482 119875 gt 005)Giardia lamblia was the most common pathogenic intestinalprotozoan flagellate with an overall prevalence of 261(208797) compared to Entamoeba histolytica which was112 (89797) Among nonpathogenic intestinal protozoafound in all age groups Entamoeba coli was the mostprevalent (180 150797) Other nonpathogenic protozoaidentified included Endolimax nana Iodomoeba butschliiand Chilomastix mesnili which are nonpathogenic protozoawere also identified (Table 1) Soil-transmitted helminthswere comparatively less common with a prevalence of 48(38797) 38 (30797) and 013 (1797) for Ascaris lum-bricoides Hookworm species and Trichuris trichiura respec-tivelyTaenia species was only encountered once among theserural children population (Table 2) The children participat-ing in this survey were age stratified and approximately 60(476797) were between the age group 24ndash48 months out ofwhich 744 (354476) had either parasitic helminths (9244476) or protozoan infections (651 310476) Infectionwith any parasites declined considerably after 48 months(Table 2)

Single and double parasitic infections per childweremoreprevalent (252 201797 137 109797 resp) compared toonly 113 (91797) polyparasitisms (ge3 parasitesindividual)obtained among these rural children Similarly polypara-sitisms were found more frequently in protozoa than inhelminthic infections (Figure 3) Dual infections with STHwere less comdmon with only about 05 (4797) childrenwho had both A lumbricoides and hookworm compared to38 (30797) children with E histolytica and G lambliacombination The majority (26 20797) of the childrencoinfected with E histolytica and G lamblia fall between ge25and 48 months age group (Table 3)

32 Discussion The prevalence of intestinal parasites foundat Webuye HDSS area among children of five years andbelow was moderately high and was slightly higher amongstmale children than the female These results concur withthose previously reported [19ndash22] Giardia lamblia was themost common intestinal parasite among our study partici-pants which is also comparable to the results reported by

0

50

100

150

200

250

0

50

100

150

200

250

300

STH

pat

hoge

nic p

roto

zoa

Mal

e and

fem

ale c

hild

ren

Age groups (month)

MalesFemales

STHEhGl

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 2 Soil-transmitted helminths (STHs) and pathogenic proto-zoan parasites among male and female children participants STHssoil-transmitted helminthes EhGl Entamoeba histolyticaGiardialamblia

Mehraj et al [19] who found a similar trend in KarachiPakistan Pillai and Kain [6] andMinenoa and Avery [7] havealso showed that G lamblia is the most prevalent protozoanparasite worldwide with about 200 million people infectedMehraj et al [19] attributed intestinal parasitic infectionspartly to poverty illiteracy poor hygiene inaccessibility topotable water and humid tropical climate These conditionsare somewhat similar to those found in Webuye HDSS areawhere we conducted our study This community has highaccessibility to water however water obtained from thesesources could be contaminated as shown by first-roundWebuye HDSS data [13] Furthermore poverty incidencelevels are high and are estimated between 56 and 60 inBungoma County [15] which could predispose them toparasitic infection

The present survey has shown that mixed infectionswithin STH were less common with only a few childrenfound with both A lumbricoides and hookworms comparedto those coinfected with E histolytica and G lamblia Themajority (26) of those who hadmixed protozoan infectionswere children between ge25 and 48 months These childrenalso had high IPIs infectivity rates This age group fallwithin the period when children are increasingly involvedin outdoor activities including handling fecal contaminatedmaterials which predispose them to parasitic infectionsInfection with any parasites declined considerably after 48months partly because of the deworming program initiatedby the Kenya Governmentrsquos Ministry of Public Health andSanitation which target school-age children between 5ndash12 years old [23] This program also targets the youngerchildren but with a few benefit because they require parentalescort to access these services whenever it is available atthe nearby primary schools However the parents are oftenengaged in other daily cores and would seldom rememberthe deworming schedule In Pakistan Chaudhry et al [24]have also reported a decline in parasitic infection after theage of 2 years but they did not offer any explanation forthis

Journal of Tropical Medicine 5

Table 2 Types and prevalence of intestinal parasites (percentages are in parentheses)

Variables Femalemale Total119875-valueGender distribution 119899 = 386 119899 = 411 119899 = 797

All parasitic infections 197 (510) 220 (535) 417 (523) 0482Ascaris lumbricoides 19 (49) 19 (46) 38 (48) 0843Hookworm spp 10 (26) 20 (49) 30 (38) 0092Trichuris trichiura 0 1 (02) 1 (013) mdashTaenia spp 0 1 (02) 1 (013) mdashEntamoeba histolytica 35 (91) 51 (124) 86 (112) 0129Giardia lamblia 100 (259) 108 (263) 208 (261) 0905Entamoeba coli 76 (197) 74 (192) 150 (188) 0543Endolimax nana 74 (192) 55 (134) 129 (162) 0027Chilomastix mesnili 16 (42) 15 (37) 31 (38) 0718Iodomoeba butschlii 16 (42) 10 (24) 26 (33) 0174

Table 3 Mixed infections of specific soil-transmitted helminths and pathogenic protozoa in each age group

Age group AH AG HG AEH GEH AHEH AGEH TEH HGEH Total1 ge 24months 1 3 0 0 5 0 0 0 0 925 ge 48months 2 2 5 2 20 1 1 1 0 3449 ge 60months 1 1 1 0 4 0 0 0 1 8gt60 months 0 0 0 0 1 0 0 0 1 2Total 4 6 6 2 30 1 1 1 2 53Key A Ascaris spp H Hookworm spp G G lamblia EH E histolytica and T Taenia spp

0

20

40

60

80

100

120

140

F M F M F M F M

Num

ber o

f par

asite

s

Age groups (months)

Five parasitesFour parasitesThree parasites

Two parasitesSingle parasite

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 3 Patterns of single double and polyparasitisms amongchildren participants in each age group

Single and double parasitic infections per child weremore common compared to polyparasitism probably due tothe restricted transmission potential which limited multipleinfections among these rural children Polyparasitism wascommon within the protozoa than in helminthic infectionsbut this was probably the outcome of a more hostile weather

to the mode of transmission of helminths [25] It is debat-able whether polyparasitisms confer any advantage to thoseinfected According to a report by Jardim-Botelho et al [26]children coinfected with A lumbricoides and hookwormsin Brazil had greater odds of poor performance in classthan those infected with A lumbricoides alone Keusch andMigasena [27] have suggested possible synergistic effects ofpolyparasitisms but this is inconclusive due to very fewanalyzed data

Surprisingly it appeared from our data that the preva-lence of soil-transmitted helminths was low compared to thepathogenic protozoa such asE histolytica andG lamblia sug-gesting that there could be factors mitigating low prevalenceof STH at Webuye HDSS area Furthermore a similar surveyinvolving women in a nearby rural western Kenya reported762 infectivity rate with at least one geohelminth comparedto our data (88) [11] This requires further investigationsHowever accessibility of improved hygiene and sanitationand awareness of the diseases associated with lack of access topotable water could be one plausible explanation for low STHprevalence within this community [12 13] Access to shallowwells in Webuye HDSS area is moderately high (461)which minimizes transmission potential of one member ofSTH group hookworm species which is transmitted bylarval penetration of the skin in surface water [12 25]The transmission of the other two members of STH Alumbricoides and T trichiura is feco-oral requiring suitableenvironment for egg maturation survival and transmissionBut this is partly hampered by the climate which has a wet

6 Journal of Tropical Medicine

spell between September andDecember each year during theperiod which temperatures may be conducive but the type ofsoils found in Webuye is mostly clay enriched which mostprobably hold on to the eggs This type of soils also retainsheat for long periods which is inimical to the developmentand dispersion of helminths eggs [28 29] The childreninfected with intestinal parasites were treated at WebuyeDistrict Hospital and other nearby health facilities howeverhelminths egg counts and anthropometric measurementswere not undertaken to provide the baseline informationupon which future studies can be assessed

4 Conclusions and Recommendations

Giardia lamblia and E histolytica were the most prevalentpathogenic intestinal protozoa while STHs were less com-mon among these rural children Further research is requiredto elucidate the factors responsible for low STH prevalenceamong this rural children population The parasites reportedhere are feco-orally transmitted and can easily be containedby the improvement of environmental hygiene Community-based health promotions including regular checkups andtreatment and personal and environmental hygiene arehighly recommended for the control of the intestinal parasitesinfesting children at Webuye HDSS area

Conflict of Interests

The authors declare no conflict of interests The studymethodology execution report and conclusion reflect solelythe authorsrsquo research and scientific work and are not theresponsibility of affiliate institutions or the funding organi-zations

Authorsrsquo Contribution

A A Obala C J Simiyu D O Odhiambo H D NNyamogoba D Menya P O Ayuo R Downing D ChelagatA W Mwangi P Chege and W P Orsquo Meara designed thestudy and took part in data collection processing and analy-sis and paper writing M Twagirumukiza D VandenbroekB B O Otsyula and J de Maeseneer critically reviewed thepaper during preparation

Acknowledgments

The authors acknowledge the assistance received from theProvincial Administration and other stakeholders formakingit possible to access the community They thank Webuyeresidents for their cooperation and for accepting to partic-ipate in this study They acknowledge the assistance of theWebuye HDSS project field supervisors and enumeratorsfor supervision of field activities and specimen collectionrespectively Mr Arthur Aroko Ms Edna Kurgat Mr IsaacMutai and Mr Paul Olang processed and examined thespecimen for which they are very grateful They thank theDeans of Schools of Medicine Public Health and Nursingfor granting them permission to collect data and compile

this report Funds for this project were provided by theMoi University (Kenya)mdashVLIRUOS (Belgium) collaborativeprogramme

References

[1] P J Hotez P J Brindley J M Bethony C H King E J Pearceand J Jacobson ldquoHelminth infections the great neglectedtropical diseasesrdquo Journal of Clinical Investigation vol 118 no4 pp 1311ndash1321 2008

[2] S Waqar H Hussain R Khan et al ldquoIntestinal parasitic infec-tions in children from the Northern Pakistanrdquo Infectious Dis-eases Journal vol 12 pp 73ndash77 2003

[3] R W Steketee ldquoPregnancy nutrition and parasitic diseasesrdquoJournal of Nutrition vol 133 pp 1661Sndash1667S 2003

[4] F Curtale P Pezzotti A L Sharbini et al ldquoKnowledge per-ceptions and behaviour of mothers toward intestinal helminthsin Upper Egypt implications for controlrdquo Health Policy andPlanning vol 13 no 4 pp 423ndash432 1998

[5] J Bethony S Brooker M Albonico et al ldquoSoil-transmittedhelminth infections ascariasis trichuriasis and hookwormrdquoThe Lancet vol 367 no 9521 pp 1521ndash1532 2006

[6] D R Pillai and K C Kain ldquoCommon intestinal parasitesrdquoCurrent Treatment Options in Infectious Diseases vol 5 pp 207ndash217 2003

[7] T Minenoa and M A Avery ldquoGiardiasis recent progress inchemotherapy and drug developmentrdquo Current PharmaceuticalDesign vol 9 pp 841ndash855 2003

[8] R Ndyomugyenyi N Kabatereine A Olsen and PMagnussenldquoMalaria and hookworm infections in relation to haemoglobinand serum ferritin levels in pregnancy in Masindi districtwestern Ugandardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 102 no 2 pp 130ndash136 2008

[9] A Olsen PMagnussen J H Ouma J Andreassen andH FriisldquoThe contribution of hookworm and other parasitic infectionsto haemoglobin and iron status among children and adults inwestern Kenyardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 92 no 6 pp 643ndash649 1998

[10] C C Appleton T I Mosala J Levin and A Olsen ldquoGeo-helminth infection and re-infection after chemotherapy amongslum-dwelling children in Durban South Africardquo Annals ofTropical Medicine and Parasitology vol 103 no 3 pp 249ndash2612009

[11] A M van Eijk K A Lindblade F Odhiambo et al ldquoGeo-helminth infections among pregnant women in rural westernKenya a cross-sectional studyrdquo PLoS Neglected Tropical Dis-eases vol 3 no 1 article e370 2009

[12] C Nokes S M Grantham-McGregor A W Sawyer E SCooper B A Robinson and D A P Bundy ldquoModerate toheavy infections of Trichuris trichiura affect cognitive functionin Jamaican school childrenrdquo Parasitology vol 104 no 3 pp539ndash547 1992

[13] Webuye Health and Demographic Surveillance System FactSheet no 1 2009 Unpublished data

[14] Webuye District Hospital Annual Report 2008 Unpublisheddata

[15] Webuye Climate Pattern 2012 httpenwikipediaorgwikiWebuye

[16] C J Simiyu V Naanyu A Obala et al ldquoEstablishing webuyehealth and demographic surveillance site in rural western

Journal of Tropical Medicine 7

Kenya challenges and lessons learnedrdquo in Population Associ-ation of America Annual Meeting Problem New Orleans LaUSA April 2013

[17] O M Mugenda and A G Mugenda Research MethodsQuantitative and Qualitative Approaches African Centre ofTechnology Studies Nairoibi Kenya 1999

[18] L S Ritchie ldquoAn ether sedimentation technique for rou-tine stool examinationrdquo Bulletin United States Army MedicalDepartment vol 8 article 326 1948

[19] V Mehraj J Hatcher S Akhtar G Rafique and M A BegldquoPrevalence and factors associated with intestinal parasiticinfection among children in an urban slum of Karachirdquo PLoSONE vol 3 no 11 Article ID e3680 2008

[20] Z Tahir ldquoComparasion of prevalence of intestinal parasites inchildren and adult populationrdquo Biomedica vol 18 pp 74ndash752002

[21] V Srinivasan S Radhakrishna A M Ramanathan and SJabbar ldquoHookworm infection in a rural community in SouthIndia and its association with haemoglobin levelsrdquo Transactionsof the Royal Society of Tropical Medicine andHygiene vol 81 no6 pp 973ndash977 1987

[22] M I Siddiqui F M Bilqees M Iliyas and S PerveenldquoPrevalence of parasitic infections in a rural area of KarachiPakistanrdquo Journal of the Pakistan Medical Association vol 52no 7 pp 315ndash320 2002

[23] Kenya National School-Based Deworming Program httpwwwdewormtheworldorgour-workkenya-national-school-based-deworming-program

[24] Z H Chaudhry M Afzal and M A Malik ldquoEpidemiologicalfactors affecting prevalence of intestinal parasites in children ofMuzaffarabad districtrdquo Pakistan Journal of Zoology vol 36 no4 pp 267ndash271 2004

[25] RMullerWorms andDisease AManual ofMedicalHelminthol-ogy Butler and Tanners 1975

[26] A Jardim-Botelho S Raff R D A Rodrigues et al ldquoHook-worm Ascaris lumbricoides infection and polyparasitism asso-ciated with poor cognitive performance in Brazilian schoolchil-drenrdquo Tropical Medicine and International Health vol 13 no 8pp 994ndash1004 2008

[27] G T Keusch and P Migasena ldquoBiological implications ofpolyparasitismrdquo Reviews of Infectious Diseases vol 4 no 4 pp880ndash882 1982

[28] Webuye economic activities and soil types httpwwwchincicomtravelpaxq178201WebuyeKEKenya0

[29] FAO Corporate Document Repository 1988 ldquoManagement ofVertisols in sub-Saharan Africardquo in Proceedings of a Confer-ence Held at ILCA Addis Ababa Ethiopia September 1987httpwwwfaoorgWairdocsILRIx5493Ex5493e00htm

Submit your manuscripts athttpwwwhindawicom

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MEDIATORSINFLAMMATION

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

International Journal of

EndocrinologyHindawi Publishing Corporationhttpwwwhindawicom

Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

BioMed Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

PPARRe sea rch

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

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Diabetes ResearchJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

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Gastroenterology Research and Practice

Parkinsonrsquos DiseaseHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 3: Webuye Health and Demographic Surveillance Systems

Journal of Tropical Medicine 3

N

EW

S

0∘459984000998400998400N

0∘409984000998400998400N

0∘359984000998400998400N

0∘309984000998400998400N

4 2 0(Kilometers)

34∘409984000998400998400E 34

∘459984000998400998400E

Compiled by Ochieng Teddy June 2008

Study sites

KituniMalahaMarakaMatuloMiloMisikhu

Roads

bound surfaceAll weather roads

Dry weather roadsMajor tracks (motorable)Railway line

Town centersMarket centerTownshiptownRivers

Health facilities

Schools

Webuye division disease surveillance sites

Figure 1 Webuye Health and Demographic Surveillance System area

imported into SPSS version 125 database for statistical anal-ysis Descriptive statistics such as mean median standarddeviation and ranges were carried out for continuous datawhile frequency listing and percentages were used to explorecategorical data To assess whether there was any associationbetween the categorical variables Pearsonrsquos Chi-square testwas used In all analyses a 119875 value less than 005 wasconsidered significant

3 Results and Discussion

31 Results This cross-sectional survey recruited 797 chil-dren of which 411 (516) and 386 (484) were boysand girls respectively Overall intestinal parasite prevalenceof 523 (417797) was obtained among children of fiveyears and below in the Webuye HDSS The male child wasslightly more infected than the female in all age group

4 Journal of Tropical Medicine

Table 1 The numbers of households allocated in each sublocationin Webuye HDSS

Sublocation Nos ofhouseholds

Samplingintervals

Targetedhouseholds

Malaha 1802 16 104Matulo 2272 16 132Misikhu 3792 16 220Maraka 2115 16 122Milo 1786 16 103Kituni 1711 16 99Total 13478 mdash 780

categories with greatest difference shown between 25 and48 months age group (Figure 2) However there were nosignificant differences in infections between male and femalechildren (53 versus 51 1205942 = 0482 119875 gt 005)Giardia lamblia was the most common pathogenic intestinalprotozoan flagellate with an overall prevalence of 261(208797) compared to Entamoeba histolytica which was112 (89797) Among nonpathogenic intestinal protozoafound in all age groups Entamoeba coli was the mostprevalent (180 150797) Other nonpathogenic protozoaidentified included Endolimax nana Iodomoeba butschliiand Chilomastix mesnili which are nonpathogenic protozoawere also identified (Table 1) Soil-transmitted helminthswere comparatively less common with a prevalence of 48(38797) 38 (30797) and 013 (1797) for Ascaris lum-bricoides Hookworm species and Trichuris trichiura respec-tivelyTaenia species was only encountered once among theserural children population (Table 2) The children participat-ing in this survey were age stratified and approximately 60(476797) were between the age group 24ndash48 months out ofwhich 744 (354476) had either parasitic helminths (9244476) or protozoan infections (651 310476) Infectionwith any parasites declined considerably after 48 months(Table 2)

Single and double parasitic infections per childweremoreprevalent (252 201797 137 109797 resp) compared toonly 113 (91797) polyparasitisms (ge3 parasitesindividual)obtained among these rural children Similarly polypara-sitisms were found more frequently in protozoa than inhelminthic infections (Figure 3) Dual infections with STHwere less comdmon with only about 05 (4797) childrenwho had both A lumbricoides and hookworm compared to38 (30797) children with E histolytica and G lambliacombination The majority (26 20797) of the childrencoinfected with E histolytica and G lamblia fall between ge25and 48 months age group (Table 3)

32 Discussion The prevalence of intestinal parasites foundat Webuye HDSS area among children of five years andbelow was moderately high and was slightly higher amongstmale children than the female These results concur withthose previously reported [19ndash22] Giardia lamblia was themost common intestinal parasite among our study partici-pants which is also comparable to the results reported by

0

50

100

150

200

250

0

50

100

150

200

250

300

STH

pat

hoge

nic p

roto

zoa

Mal

e and

fem

ale c

hild

ren

Age groups (month)

MalesFemales

STHEhGl

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 2 Soil-transmitted helminths (STHs) and pathogenic proto-zoan parasites among male and female children participants STHssoil-transmitted helminthes EhGl Entamoeba histolyticaGiardialamblia

Mehraj et al [19] who found a similar trend in KarachiPakistan Pillai and Kain [6] andMinenoa and Avery [7] havealso showed that G lamblia is the most prevalent protozoanparasite worldwide with about 200 million people infectedMehraj et al [19] attributed intestinal parasitic infectionspartly to poverty illiteracy poor hygiene inaccessibility topotable water and humid tropical climate These conditionsare somewhat similar to those found in Webuye HDSS areawhere we conducted our study This community has highaccessibility to water however water obtained from thesesources could be contaminated as shown by first-roundWebuye HDSS data [13] Furthermore poverty incidencelevels are high and are estimated between 56 and 60 inBungoma County [15] which could predispose them toparasitic infection

The present survey has shown that mixed infectionswithin STH were less common with only a few childrenfound with both A lumbricoides and hookworms comparedto those coinfected with E histolytica and G lamblia Themajority (26) of those who hadmixed protozoan infectionswere children between ge25 and 48 months These childrenalso had high IPIs infectivity rates This age group fallwithin the period when children are increasingly involvedin outdoor activities including handling fecal contaminatedmaterials which predispose them to parasitic infectionsInfection with any parasites declined considerably after 48months partly because of the deworming program initiatedby the Kenya Governmentrsquos Ministry of Public Health andSanitation which target school-age children between 5ndash12 years old [23] This program also targets the youngerchildren but with a few benefit because they require parentalescort to access these services whenever it is available atthe nearby primary schools However the parents are oftenengaged in other daily cores and would seldom rememberthe deworming schedule In Pakistan Chaudhry et al [24]have also reported a decline in parasitic infection after theage of 2 years but they did not offer any explanation forthis

Journal of Tropical Medicine 5

Table 2 Types and prevalence of intestinal parasites (percentages are in parentheses)

Variables Femalemale Total119875-valueGender distribution 119899 = 386 119899 = 411 119899 = 797

All parasitic infections 197 (510) 220 (535) 417 (523) 0482Ascaris lumbricoides 19 (49) 19 (46) 38 (48) 0843Hookworm spp 10 (26) 20 (49) 30 (38) 0092Trichuris trichiura 0 1 (02) 1 (013) mdashTaenia spp 0 1 (02) 1 (013) mdashEntamoeba histolytica 35 (91) 51 (124) 86 (112) 0129Giardia lamblia 100 (259) 108 (263) 208 (261) 0905Entamoeba coli 76 (197) 74 (192) 150 (188) 0543Endolimax nana 74 (192) 55 (134) 129 (162) 0027Chilomastix mesnili 16 (42) 15 (37) 31 (38) 0718Iodomoeba butschlii 16 (42) 10 (24) 26 (33) 0174

Table 3 Mixed infections of specific soil-transmitted helminths and pathogenic protozoa in each age group

Age group AH AG HG AEH GEH AHEH AGEH TEH HGEH Total1 ge 24months 1 3 0 0 5 0 0 0 0 925 ge 48months 2 2 5 2 20 1 1 1 0 3449 ge 60months 1 1 1 0 4 0 0 0 1 8gt60 months 0 0 0 0 1 0 0 0 1 2Total 4 6 6 2 30 1 1 1 2 53Key A Ascaris spp H Hookworm spp G G lamblia EH E histolytica and T Taenia spp

0

20

40

60

80

100

120

140

F M F M F M F M

Num

ber o

f par

asite

s

Age groups (months)

Five parasitesFour parasitesThree parasites

Two parasitesSingle parasite

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 3 Patterns of single double and polyparasitisms amongchildren participants in each age group

Single and double parasitic infections per child weremore common compared to polyparasitism probably due tothe restricted transmission potential which limited multipleinfections among these rural children Polyparasitism wascommon within the protozoa than in helminthic infectionsbut this was probably the outcome of a more hostile weather

to the mode of transmission of helminths [25] It is debat-able whether polyparasitisms confer any advantage to thoseinfected According to a report by Jardim-Botelho et al [26]children coinfected with A lumbricoides and hookwormsin Brazil had greater odds of poor performance in classthan those infected with A lumbricoides alone Keusch andMigasena [27] have suggested possible synergistic effects ofpolyparasitisms but this is inconclusive due to very fewanalyzed data

Surprisingly it appeared from our data that the preva-lence of soil-transmitted helminths was low compared to thepathogenic protozoa such asE histolytica andG lamblia sug-gesting that there could be factors mitigating low prevalenceof STH at Webuye HDSS area Furthermore a similar surveyinvolving women in a nearby rural western Kenya reported762 infectivity rate with at least one geohelminth comparedto our data (88) [11] This requires further investigationsHowever accessibility of improved hygiene and sanitationand awareness of the diseases associated with lack of access topotable water could be one plausible explanation for low STHprevalence within this community [12 13] Access to shallowwells in Webuye HDSS area is moderately high (461)which minimizes transmission potential of one member ofSTH group hookworm species which is transmitted bylarval penetration of the skin in surface water [12 25]The transmission of the other two members of STH Alumbricoides and T trichiura is feco-oral requiring suitableenvironment for egg maturation survival and transmissionBut this is partly hampered by the climate which has a wet

6 Journal of Tropical Medicine

spell between September andDecember each year during theperiod which temperatures may be conducive but the type ofsoils found in Webuye is mostly clay enriched which mostprobably hold on to the eggs This type of soils also retainsheat for long periods which is inimical to the developmentand dispersion of helminths eggs [28 29] The childreninfected with intestinal parasites were treated at WebuyeDistrict Hospital and other nearby health facilities howeverhelminths egg counts and anthropometric measurementswere not undertaken to provide the baseline informationupon which future studies can be assessed

4 Conclusions and Recommendations

Giardia lamblia and E histolytica were the most prevalentpathogenic intestinal protozoa while STHs were less com-mon among these rural children Further research is requiredto elucidate the factors responsible for low STH prevalenceamong this rural children population The parasites reportedhere are feco-orally transmitted and can easily be containedby the improvement of environmental hygiene Community-based health promotions including regular checkups andtreatment and personal and environmental hygiene arehighly recommended for the control of the intestinal parasitesinfesting children at Webuye HDSS area

Conflict of Interests

The authors declare no conflict of interests The studymethodology execution report and conclusion reflect solelythe authorsrsquo research and scientific work and are not theresponsibility of affiliate institutions or the funding organi-zations

Authorsrsquo Contribution

A A Obala C J Simiyu D O Odhiambo H D NNyamogoba D Menya P O Ayuo R Downing D ChelagatA W Mwangi P Chege and W P Orsquo Meara designed thestudy and took part in data collection processing and analy-sis and paper writing M Twagirumukiza D VandenbroekB B O Otsyula and J de Maeseneer critically reviewed thepaper during preparation

Acknowledgments

The authors acknowledge the assistance received from theProvincial Administration and other stakeholders formakingit possible to access the community They thank Webuyeresidents for their cooperation and for accepting to partic-ipate in this study They acknowledge the assistance of theWebuye HDSS project field supervisors and enumeratorsfor supervision of field activities and specimen collectionrespectively Mr Arthur Aroko Ms Edna Kurgat Mr IsaacMutai and Mr Paul Olang processed and examined thespecimen for which they are very grateful They thank theDeans of Schools of Medicine Public Health and Nursingfor granting them permission to collect data and compile

this report Funds for this project were provided by theMoi University (Kenya)mdashVLIRUOS (Belgium) collaborativeprogramme

References

[1] P J Hotez P J Brindley J M Bethony C H King E J Pearceand J Jacobson ldquoHelminth infections the great neglectedtropical diseasesrdquo Journal of Clinical Investigation vol 118 no4 pp 1311ndash1321 2008

[2] S Waqar H Hussain R Khan et al ldquoIntestinal parasitic infec-tions in children from the Northern Pakistanrdquo Infectious Dis-eases Journal vol 12 pp 73ndash77 2003

[3] R W Steketee ldquoPregnancy nutrition and parasitic diseasesrdquoJournal of Nutrition vol 133 pp 1661Sndash1667S 2003

[4] F Curtale P Pezzotti A L Sharbini et al ldquoKnowledge per-ceptions and behaviour of mothers toward intestinal helminthsin Upper Egypt implications for controlrdquo Health Policy andPlanning vol 13 no 4 pp 423ndash432 1998

[5] J Bethony S Brooker M Albonico et al ldquoSoil-transmittedhelminth infections ascariasis trichuriasis and hookwormrdquoThe Lancet vol 367 no 9521 pp 1521ndash1532 2006

[6] D R Pillai and K C Kain ldquoCommon intestinal parasitesrdquoCurrent Treatment Options in Infectious Diseases vol 5 pp 207ndash217 2003

[7] T Minenoa and M A Avery ldquoGiardiasis recent progress inchemotherapy and drug developmentrdquo Current PharmaceuticalDesign vol 9 pp 841ndash855 2003

[8] R Ndyomugyenyi N Kabatereine A Olsen and PMagnussenldquoMalaria and hookworm infections in relation to haemoglobinand serum ferritin levels in pregnancy in Masindi districtwestern Ugandardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 102 no 2 pp 130ndash136 2008

[9] A Olsen PMagnussen J H Ouma J Andreassen andH FriisldquoThe contribution of hookworm and other parasitic infectionsto haemoglobin and iron status among children and adults inwestern Kenyardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 92 no 6 pp 643ndash649 1998

[10] C C Appleton T I Mosala J Levin and A Olsen ldquoGeo-helminth infection and re-infection after chemotherapy amongslum-dwelling children in Durban South Africardquo Annals ofTropical Medicine and Parasitology vol 103 no 3 pp 249ndash2612009

[11] A M van Eijk K A Lindblade F Odhiambo et al ldquoGeo-helminth infections among pregnant women in rural westernKenya a cross-sectional studyrdquo PLoS Neglected Tropical Dis-eases vol 3 no 1 article e370 2009

[12] C Nokes S M Grantham-McGregor A W Sawyer E SCooper B A Robinson and D A P Bundy ldquoModerate toheavy infections of Trichuris trichiura affect cognitive functionin Jamaican school childrenrdquo Parasitology vol 104 no 3 pp539ndash547 1992

[13] Webuye Health and Demographic Surveillance System FactSheet no 1 2009 Unpublished data

[14] Webuye District Hospital Annual Report 2008 Unpublisheddata

[15] Webuye Climate Pattern 2012 httpenwikipediaorgwikiWebuye

[16] C J Simiyu V Naanyu A Obala et al ldquoEstablishing webuyehealth and demographic surveillance site in rural western

Journal of Tropical Medicine 7

Kenya challenges and lessons learnedrdquo in Population Associ-ation of America Annual Meeting Problem New Orleans LaUSA April 2013

[17] O M Mugenda and A G Mugenda Research MethodsQuantitative and Qualitative Approaches African Centre ofTechnology Studies Nairoibi Kenya 1999

[18] L S Ritchie ldquoAn ether sedimentation technique for rou-tine stool examinationrdquo Bulletin United States Army MedicalDepartment vol 8 article 326 1948

[19] V Mehraj J Hatcher S Akhtar G Rafique and M A BegldquoPrevalence and factors associated with intestinal parasiticinfection among children in an urban slum of Karachirdquo PLoSONE vol 3 no 11 Article ID e3680 2008

[20] Z Tahir ldquoComparasion of prevalence of intestinal parasites inchildren and adult populationrdquo Biomedica vol 18 pp 74ndash752002

[21] V Srinivasan S Radhakrishna A M Ramanathan and SJabbar ldquoHookworm infection in a rural community in SouthIndia and its association with haemoglobin levelsrdquo Transactionsof the Royal Society of Tropical Medicine andHygiene vol 81 no6 pp 973ndash977 1987

[22] M I Siddiqui F M Bilqees M Iliyas and S PerveenldquoPrevalence of parasitic infections in a rural area of KarachiPakistanrdquo Journal of the Pakistan Medical Association vol 52no 7 pp 315ndash320 2002

[23] Kenya National School-Based Deworming Program httpwwwdewormtheworldorgour-workkenya-national-school-based-deworming-program

[24] Z H Chaudhry M Afzal and M A Malik ldquoEpidemiologicalfactors affecting prevalence of intestinal parasites in children ofMuzaffarabad districtrdquo Pakistan Journal of Zoology vol 36 no4 pp 267ndash271 2004

[25] RMullerWorms andDisease AManual ofMedicalHelminthol-ogy Butler and Tanners 1975

[26] A Jardim-Botelho S Raff R D A Rodrigues et al ldquoHook-worm Ascaris lumbricoides infection and polyparasitism asso-ciated with poor cognitive performance in Brazilian schoolchil-drenrdquo Tropical Medicine and International Health vol 13 no 8pp 994ndash1004 2008

[27] G T Keusch and P Migasena ldquoBiological implications ofpolyparasitismrdquo Reviews of Infectious Diseases vol 4 no 4 pp880ndash882 1982

[28] Webuye economic activities and soil types httpwwwchincicomtravelpaxq178201WebuyeKEKenya0

[29] FAO Corporate Document Repository 1988 ldquoManagement ofVertisols in sub-Saharan Africardquo in Proceedings of a Confer-ence Held at ILCA Addis Ababa Ethiopia September 1987httpwwwfaoorgWairdocsILRIx5493Ex5493e00htm

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

International Journal of

EndocrinologyHindawi Publishing Corporationhttpwwwhindawicom

Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

BioMed Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

PPARRe sea rch

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Parkinsonrsquos DiseaseHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 4: Webuye Health and Demographic Surveillance Systems

4 Journal of Tropical Medicine

Table 1 The numbers of households allocated in each sublocationin Webuye HDSS

Sublocation Nos ofhouseholds

Samplingintervals

Targetedhouseholds

Malaha 1802 16 104Matulo 2272 16 132Misikhu 3792 16 220Maraka 2115 16 122Milo 1786 16 103Kituni 1711 16 99Total 13478 mdash 780

categories with greatest difference shown between 25 and48 months age group (Figure 2) However there were nosignificant differences in infections between male and femalechildren (53 versus 51 1205942 = 0482 119875 gt 005)Giardia lamblia was the most common pathogenic intestinalprotozoan flagellate with an overall prevalence of 261(208797) compared to Entamoeba histolytica which was112 (89797) Among nonpathogenic intestinal protozoafound in all age groups Entamoeba coli was the mostprevalent (180 150797) Other nonpathogenic protozoaidentified included Endolimax nana Iodomoeba butschliiand Chilomastix mesnili which are nonpathogenic protozoawere also identified (Table 1) Soil-transmitted helminthswere comparatively less common with a prevalence of 48(38797) 38 (30797) and 013 (1797) for Ascaris lum-bricoides Hookworm species and Trichuris trichiura respec-tivelyTaenia species was only encountered once among theserural children population (Table 2) The children participat-ing in this survey were age stratified and approximately 60(476797) were between the age group 24ndash48 months out ofwhich 744 (354476) had either parasitic helminths (9244476) or protozoan infections (651 310476) Infectionwith any parasites declined considerably after 48 months(Table 2)

Single and double parasitic infections per childweremoreprevalent (252 201797 137 109797 resp) compared toonly 113 (91797) polyparasitisms (ge3 parasitesindividual)obtained among these rural children Similarly polypara-sitisms were found more frequently in protozoa than inhelminthic infections (Figure 3) Dual infections with STHwere less comdmon with only about 05 (4797) childrenwho had both A lumbricoides and hookworm compared to38 (30797) children with E histolytica and G lambliacombination The majority (26 20797) of the childrencoinfected with E histolytica and G lamblia fall between ge25and 48 months age group (Table 3)

32 Discussion The prevalence of intestinal parasites foundat Webuye HDSS area among children of five years andbelow was moderately high and was slightly higher amongstmale children than the female These results concur withthose previously reported [19ndash22] Giardia lamblia was themost common intestinal parasite among our study partici-pants which is also comparable to the results reported by

0

50

100

150

200

250

0

50

100

150

200

250

300

STH

pat

hoge

nic p

roto

zoa

Mal

e and

fem

ale c

hild

ren

Age groups (month)

MalesFemales

STHEhGl

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 2 Soil-transmitted helminths (STHs) and pathogenic proto-zoan parasites among male and female children participants STHssoil-transmitted helminthes EhGl Entamoeba histolyticaGiardialamblia

Mehraj et al [19] who found a similar trend in KarachiPakistan Pillai and Kain [6] andMinenoa and Avery [7] havealso showed that G lamblia is the most prevalent protozoanparasite worldwide with about 200 million people infectedMehraj et al [19] attributed intestinal parasitic infectionspartly to poverty illiteracy poor hygiene inaccessibility topotable water and humid tropical climate These conditionsare somewhat similar to those found in Webuye HDSS areawhere we conducted our study This community has highaccessibility to water however water obtained from thesesources could be contaminated as shown by first-roundWebuye HDSS data [13] Furthermore poverty incidencelevels are high and are estimated between 56 and 60 inBungoma County [15] which could predispose them toparasitic infection

The present survey has shown that mixed infectionswithin STH were less common with only a few childrenfound with both A lumbricoides and hookworms comparedto those coinfected with E histolytica and G lamblia Themajority (26) of those who hadmixed protozoan infectionswere children between ge25 and 48 months These childrenalso had high IPIs infectivity rates This age group fallwithin the period when children are increasingly involvedin outdoor activities including handling fecal contaminatedmaterials which predispose them to parasitic infectionsInfection with any parasites declined considerably after 48months partly because of the deworming program initiatedby the Kenya Governmentrsquos Ministry of Public Health andSanitation which target school-age children between 5ndash12 years old [23] This program also targets the youngerchildren but with a few benefit because they require parentalescort to access these services whenever it is available atthe nearby primary schools However the parents are oftenengaged in other daily cores and would seldom rememberthe deworming schedule In Pakistan Chaudhry et al [24]have also reported a decline in parasitic infection after theage of 2 years but they did not offer any explanation forthis

Journal of Tropical Medicine 5

Table 2 Types and prevalence of intestinal parasites (percentages are in parentheses)

Variables Femalemale Total119875-valueGender distribution 119899 = 386 119899 = 411 119899 = 797

All parasitic infections 197 (510) 220 (535) 417 (523) 0482Ascaris lumbricoides 19 (49) 19 (46) 38 (48) 0843Hookworm spp 10 (26) 20 (49) 30 (38) 0092Trichuris trichiura 0 1 (02) 1 (013) mdashTaenia spp 0 1 (02) 1 (013) mdashEntamoeba histolytica 35 (91) 51 (124) 86 (112) 0129Giardia lamblia 100 (259) 108 (263) 208 (261) 0905Entamoeba coli 76 (197) 74 (192) 150 (188) 0543Endolimax nana 74 (192) 55 (134) 129 (162) 0027Chilomastix mesnili 16 (42) 15 (37) 31 (38) 0718Iodomoeba butschlii 16 (42) 10 (24) 26 (33) 0174

Table 3 Mixed infections of specific soil-transmitted helminths and pathogenic protozoa in each age group

Age group AH AG HG AEH GEH AHEH AGEH TEH HGEH Total1 ge 24months 1 3 0 0 5 0 0 0 0 925 ge 48months 2 2 5 2 20 1 1 1 0 3449 ge 60months 1 1 1 0 4 0 0 0 1 8gt60 months 0 0 0 0 1 0 0 0 1 2Total 4 6 6 2 30 1 1 1 2 53Key A Ascaris spp H Hookworm spp G G lamblia EH E histolytica and T Taenia spp

0

20

40

60

80

100

120

140

F M F M F M F M

Num

ber o

f par

asite

s

Age groups (months)

Five parasitesFour parasitesThree parasites

Two parasitesSingle parasite

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 3 Patterns of single double and polyparasitisms amongchildren participants in each age group

Single and double parasitic infections per child weremore common compared to polyparasitism probably due tothe restricted transmission potential which limited multipleinfections among these rural children Polyparasitism wascommon within the protozoa than in helminthic infectionsbut this was probably the outcome of a more hostile weather

to the mode of transmission of helminths [25] It is debat-able whether polyparasitisms confer any advantage to thoseinfected According to a report by Jardim-Botelho et al [26]children coinfected with A lumbricoides and hookwormsin Brazil had greater odds of poor performance in classthan those infected with A lumbricoides alone Keusch andMigasena [27] have suggested possible synergistic effects ofpolyparasitisms but this is inconclusive due to very fewanalyzed data

Surprisingly it appeared from our data that the preva-lence of soil-transmitted helminths was low compared to thepathogenic protozoa such asE histolytica andG lamblia sug-gesting that there could be factors mitigating low prevalenceof STH at Webuye HDSS area Furthermore a similar surveyinvolving women in a nearby rural western Kenya reported762 infectivity rate with at least one geohelminth comparedto our data (88) [11] This requires further investigationsHowever accessibility of improved hygiene and sanitationand awareness of the diseases associated with lack of access topotable water could be one plausible explanation for low STHprevalence within this community [12 13] Access to shallowwells in Webuye HDSS area is moderately high (461)which minimizes transmission potential of one member ofSTH group hookworm species which is transmitted bylarval penetration of the skin in surface water [12 25]The transmission of the other two members of STH Alumbricoides and T trichiura is feco-oral requiring suitableenvironment for egg maturation survival and transmissionBut this is partly hampered by the climate which has a wet

6 Journal of Tropical Medicine

spell between September andDecember each year during theperiod which temperatures may be conducive but the type ofsoils found in Webuye is mostly clay enriched which mostprobably hold on to the eggs This type of soils also retainsheat for long periods which is inimical to the developmentand dispersion of helminths eggs [28 29] The childreninfected with intestinal parasites were treated at WebuyeDistrict Hospital and other nearby health facilities howeverhelminths egg counts and anthropometric measurementswere not undertaken to provide the baseline informationupon which future studies can be assessed

4 Conclusions and Recommendations

Giardia lamblia and E histolytica were the most prevalentpathogenic intestinal protozoa while STHs were less com-mon among these rural children Further research is requiredto elucidate the factors responsible for low STH prevalenceamong this rural children population The parasites reportedhere are feco-orally transmitted and can easily be containedby the improvement of environmental hygiene Community-based health promotions including regular checkups andtreatment and personal and environmental hygiene arehighly recommended for the control of the intestinal parasitesinfesting children at Webuye HDSS area

Conflict of Interests

The authors declare no conflict of interests The studymethodology execution report and conclusion reflect solelythe authorsrsquo research and scientific work and are not theresponsibility of affiliate institutions or the funding organi-zations

Authorsrsquo Contribution

A A Obala C J Simiyu D O Odhiambo H D NNyamogoba D Menya P O Ayuo R Downing D ChelagatA W Mwangi P Chege and W P Orsquo Meara designed thestudy and took part in data collection processing and analy-sis and paper writing M Twagirumukiza D VandenbroekB B O Otsyula and J de Maeseneer critically reviewed thepaper during preparation

Acknowledgments

The authors acknowledge the assistance received from theProvincial Administration and other stakeholders formakingit possible to access the community They thank Webuyeresidents for their cooperation and for accepting to partic-ipate in this study They acknowledge the assistance of theWebuye HDSS project field supervisors and enumeratorsfor supervision of field activities and specimen collectionrespectively Mr Arthur Aroko Ms Edna Kurgat Mr IsaacMutai and Mr Paul Olang processed and examined thespecimen for which they are very grateful They thank theDeans of Schools of Medicine Public Health and Nursingfor granting them permission to collect data and compile

this report Funds for this project were provided by theMoi University (Kenya)mdashVLIRUOS (Belgium) collaborativeprogramme

References

[1] P J Hotez P J Brindley J M Bethony C H King E J Pearceand J Jacobson ldquoHelminth infections the great neglectedtropical diseasesrdquo Journal of Clinical Investigation vol 118 no4 pp 1311ndash1321 2008

[2] S Waqar H Hussain R Khan et al ldquoIntestinal parasitic infec-tions in children from the Northern Pakistanrdquo Infectious Dis-eases Journal vol 12 pp 73ndash77 2003

[3] R W Steketee ldquoPregnancy nutrition and parasitic diseasesrdquoJournal of Nutrition vol 133 pp 1661Sndash1667S 2003

[4] F Curtale P Pezzotti A L Sharbini et al ldquoKnowledge per-ceptions and behaviour of mothers toward intestinal helminthsin Upper Egypt implications for controlrdquo Health Policy andPlanning vol 13 no 4 pp 423ndash432 1998

[5] J Bethony S Brooker M Albonico et al ldquoSoil-transmittedhelminth infections ascariasis trichuriasis and hookwormrdquoThe Lancet vol 367 no 9521 pp 1521ndash1532 2006

[6] D R Pillai and K C Kain ldquoCommon intestinal parasitesrdquoCurrent Treatment Options in Infectious Diseases vol 5 pp 207ndash217 2003

[7] T Minenoa and M A Avery ldquoGiardiasis recent progress inchemotherapy and drug developmentrdquo Current PharmaceuticalDesign vol 9 pp 841ndash855 2003

[8] R Ndyomugyenyi N Kabatereine A Olsen and PMagnussenldquoMalaria and hookworm infections in relation to haemoglobinand serum ferritin levels in pregnancy in Masindi districtwestern Ugandardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 102 no 2 pp 130ndash136 2008

[9] A Olsen PMagnussen J H Ouma J Andreassen andH FriisldquoThe contribution of hookworm and other parasitic infectionsto haemoglobin and iron status among children and adults inwestern Kenyardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 92 no 6 pp 643ndash649 1998

[10] C C Appleton T I Mosala J Levin and A Olsen ldquoGeo-helminth infection and re-infection after chemotherapy amongslum-dwelling children in Durban South Africardquo Annals ofTropical Medicine and Parasitology vol 103 no 3 pp 249ndash2612009

[11] A M van Eijk K A Lindblade F Odhiambo et al ldquoGeo-helminth infections among pregnant women in rural westernKenya a cross-sectional studyrdquo PLoS Neglected Tropical Dis-eases vol 3 no 1 article e370 2009

[12] C Nokes S M Grantham-McGregor A W Sawyer E SCooper B A Robinson and D A P Bundy ldquoModerate toheavy infections of Trichuris trichiura affect cognitive functionin Jamaican school childrenrdquo Parasitology vol 104 no 3 pp539ndash547 1992

[13] Webuye Health and Demographic Surveillance System FactSheet no 1 2009 Unpublished data

[14] Webuye District Hospital Annual Report 2008 Unpublisheddata

[15] Webuye Climate Pattern 2012 httpenwikipediaorgwikiWebuye

[16] C J Simiyu V Naanyu A Obala et al ldquoEstablishing webuyehealth and demographic surveillance site in rural western

Journal of Tropical Medicine 7

Kenya challenges and lessons learnedrdquo in Population Associ-ation of America Annual Meeting Problem New Orleans LaUSA April 2013

[17] O M Mugenda and A G Mugenda Research MethodsQuantitative and Qualitative Approaches African Centre ofTechnology Studies Nairoibi Kenya 1999

[18] L S Ritchie ldquoAn ether sedimentation technique for rou-tine stool examinationrdquo Bulletin United States Army MedicalDepartment vol 8 article 326 1948

[19] V Mehraj J Hatcher S Akhtar G Rafique and M A BegldquoPrevalence and factors associated with intestinal parasiticinfection among children in an urban slum of Karachirdquo PLoSONE vol 3 no 11 Article ID e3680 2008

[20] Z Tahir ldquoComparasion of prevalence of intestinal parasites inchildren and adult populationrdquo Biomedica vol 18 pp 74ndash752002

[21] V Srinivasan S Radhakrishna A M Ramanathan and SJabbar ldquoHookworm infection in a rural community in SouthIndia and its association with haemoglobin levelsrdquo Transactionsof the Royal Society of Tropical Medicine andHygiene vol 81 no6 pp 973ndash977 1987

[22] M I Siddiqui F M Bilqees M Iliyas and S PerveenldquoPrevalence of parasitic infections in a rural area of KarachiPakistanrdquo Journal of the Pakistan Medical Association vol 52no 7 pp 315ndash320 2002

[23] Kenya National School-Based Deworming Program httpwwwdewormtheworldorgour-workkenya-national-school-based-deworming-program

[24] Z H Chaudhry M Afzal and M A Malik ldquoEpidemiologicalfactors affecting prevalence of intestinal parasites in children ofMuzaffarabad districtrdquo Pakistan Journal of Zoology vol 36 no4 pp 267ndash271 2004

[25] RMullerWorms andDisease AManual ofMedicalHelminthol-ogy Butler and Tanners 1975

[26] A Jardim-Botelho S Raff R D A Rodrigues et al ldquoHook-worm Ascaris lumbricoides infection and polyparasitism asso-ciated with poor cognitive performance in Brazilian schoolchil-drenrdquo Tropical Medicine and International Health vol 13 no 8pp 994ndash1004 2008

[27] G T Keusch and P Migasena ldquoBiological implications ofpolyparasitismrdquo Reviews of Infectious Diseases vol 4 no 4 pp880ndash882 1982

[28] Webuye economic activities and soil types httpwwwchincicomtravelpaxq178201WebuyeKEKenya0

[29] FAO Corporate Document Repository 1988 ldquoManagement ofVertisols in sub-Saharan Africardquo in Proceedings of a Confer-ence Held at ILCA Addis Ababa Ethiopia September 1987httpwwwfaoorgWairdocsILRIx5493Ex5493e00htm

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

International Journal of

EndocrinologyHindawi Publishing Corporationhttpwwwhindawicom

Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

BioMed Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

PPARRe sea rch

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Parkinsonrsquos DiseaseHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 5: Webuye Health and Demographic Surveillance Systems

Journal of Tropical Medicine 5

Table 2 Types and prevalence of intestinal parasites (percentages are in parentheses)

Variables Femalemale Total119875-valueGender distribution 119899 = 386 119899 = 411 119899 = 797

All parasitic infections 197 (510) 220 (535) 417 (523) 0482Ascaris lumbricoides 19 (49) 19 (46) 38 (48) 0843Hookworm spp 10 (26) 20 (49) 30 (38) 0092Trichuris trichiura 0 1 (02) 1 (013) mdashTaenia spp 0 1 (02) 1 (013) mdashEntamoeba histolytica 35 (91) 51 (124) 86 (112) 0129Giardia lamblia 100 (259) 108 (263) 208 (261) 0905Entamoeba coli 76 (197) 74 (192) 150 (188) 0543Endolimax nana 74 (192) 55 (134) 129 (162) 0027Chilomastix mesnili 16 (42) 15 (37) 31 (38) 0718Iodomoeba butschlii 16 (42) 10 (24) 26 (33) 0174

Table 3 Mixed infections of specific soil-transmitted helminths and pathogenic protozoa in each age group

Age group AH AG HG AEH GEH AHEH AGEH TEH HGEH Total1 ge 24months 1 3 0 0 5 0 0 0 0 925 ge 48months 2 2 5 2 20 1 1 1 0 3449 ge 60months 1 1 1 0 4 0 0 0 1 8gt60 months 0 0 0 0 1 0 0 0 1 2Total 4 6 6 2 30 1 1 1 2 53Key A Ascaris spp H Hookworm spp G G lamblia EH E histolytica and T Taenia spp

0

20

40

60

80

100

120

140

F M F M F M F M

Num

ber o

f par

asite

s

Age groups (months)

Five parasitesFour parasitesThree parasites

Two parasitesSingle parasite

1 ge 24 25 ge 48 49 ge 60 gt60

Figure 3 Patterns of single double and polyparasitisms amongchildren participants in each age group

Single and double parasitic infections per child weremore common compared to polyparasitism probably due tothe restricted transmission potential which limited multipleinfections among these rural children Polyparasitism wascommon within the protozoa than in helminthic infectionsbut this was probably the outcome of a more hostile weather

to the mode of transmission of helminths [25] It is debat-able whether polyparasitisms confer any advantage to thoseinfected According to a report by Jardim-Botelho et al [26]children coinfected with A lumbricoides and hookwormsin Brazil had greater odds of poor performance in classthan those infected with A lumbricoides alone Keusch andMigasena [27] have suggested possible synergistic effects ofpolyparasitisms but this is inconclusive due to very fewanalyzed data

Surprisingly it appeared from our data that the preva-lence of soil-transmitted helminths was low compared to thepathogenic protozoa such asE histolytica andG lamblia sug-gesting that there could be factors mitigating low prevalenceof STH at Webuye HDSS area Furthermore a similar surveyinvolving women in a nearby rural western Kenya reported762 infectivity rate with at least one geohelminth comparedto our data (88) [11] This requires further investigationsHowever accessibility of improved hygiene and sanitationand awareness of the diseases associated with lack of access topotable water could be one plausible explanation for low STHprevalence within this community [12 13] Access to shallowwells in Webuye HDSS area is moderately high (461)which minimizes transmission potential of one member ofSTH group hookworm species which is transmitted bylarval penetration of the skin in surface water [12 25]The transmission of the other two members of STH Alumbricoides and T trichiura is feco-oral requiring suitableenvironment for egg maturation survival and transmissionBut this is partly hampered by the climate which has a wet

6 Journal of Tropical Medicine

spell between September andDecember each year during theperiod which temperatures may be conducive but the type ofsoils found in Webuye is mostly clay enriched which mostprobably hold on to the eggs This type of soils also retainsheat for long periods which is inimical to the developmentand dispersion of helminths eggs [28 29] The childreninfected with intestinal parasites were treated at WebuyeDistrict Hospital and other nearby health facilities howeverhelminths egg counts and anthropometric measurementswere not undertaken to provide the baseline informationupon which future studies can be assessed

4 Conclusions and Recommendations

Giardia lamblia and E histolytica were the most prevalentpathogenic intestinal protozoa while STHs were less com-mon among these rural children Further research is requiredto elucidate the factors responsible for low STH prevalenceamong this rural children population The parasites reportedhere are feco-orally transmitted and can easily be containedby the improvement of environmental hygiene Community-based health promotions including regular checkups andtreatment and personal and environmental hygiene arehighly recommended for the control of the intestinal parasitesinfesting children at Webuye HDSS area

Conflict of Interests

The authors declare no conflict of interests The studymethodology execution report and conclusion reflect solelythe authorsrsquo research and scientific work and are not theresponsibility of affiliate institutions or the funding organi-zations

Authorsrsquo Contribution

A A Obala C J Simiyu D O Odhiambo H D NNyamogoba D Menya P O Ayuo R Downing D ChelagatA W Mwangi P Chege and W P Orsquo Meara designed thestudy and took part in data collection processing and analy-sis and paper writing M Twagirumukiza D VandenbroekB B O Otsyula and J de Maeseneer critically reviewed thepaper during preparation

Acknowledgments

The authors acknowledge the assistance received from theProvincial Administration and other stakeholders formakingit possible to access the community They thank Webuyeresidents for their cooperation and for accepting to partic-ipate in this study They acknowledge the assistance of theWebuye HDSS project field supervisors and enumeratorsfor supervision of field activities and specimen collectionrespectively Mr Arthur Aroko Ms Edna Kurgat Mr IsaacMutai and Mr Paul Olang processed and examined thespecimen for which they are very grateful They thank theDeans of Schools of Medicine Public Health and Nursingfor granting them permission to collect data and compile

this report Funds for this project were provided by theMoi University (Kenya)mdashVLIRUOS (Belgium) collaborativeprogramme

References

[1] P J Hotez P J Brindley J M Bethony C H King E J Pearceand J Jacobson ldquoHelminth infections the great neglectedtropical diseasesrdquo Journal of Clinical Investigation vol 118 no4 pp 1311ndash1321 2008

[2] S Waqar H Hussain R Khan et al ldquoIntestinal parasitic infec-tions in children from the Northern Pakistanrdquo Infectious Dis-eases Journal vol 12 pp 73ndash77 2003

[3] R W Steketee ldquoPregnancy nutrition and parasitic diseasesrdquoJournal of Nutrition vol 133 pp 1661Sndash1667S 2003

[4] F Curtale P Pezzotti A L Sharbini et al ldquoKnowledge per-ceptions and behaviour of mothers toward intestinal helminthsin Upper Egypt implications for controlrdquo Health Policy andPlanning vol 13 no 4 pp 423ndash432 1998

[5] J Bethony S Brooker M Albonico et al ldquoSoil-transmittedhelminth infections ascariasis trichuriasis and hookwormrdquoThe Lancet vol 367 no 9521 pp 1521ndash1532 2006

[6] D R Pillai and K C Kain ldquoCommon intestinal parasitesrdquoCurrent Treatment Options in Infectious Diseases vol 5 pp 207ndash217 2003

[7] T Minenoa and M A Avery ldquoGiardiasis recent progress inchemotherapy and drug developmentrdquo Current PharmaceuticalDesign vol 9 pp 841ndash855 2003

[8] R Ndyomugyenyi N Kabatereine A Olsen and PMagnussenldquoMalaria and hookworm infections in relation to haemoglobinand serum ferritin levels in pregnancy in Masindi districtwestern Ugandardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 102 no 2 pp 130ndash136 2008

[9] A Olsen PMagnussen J H Ouma J Andreassen andH FriisldquoThe contribution of hookworm and other parasitic infectionsto haemoglobin and iron status among children and adults inwestern Kenyardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 92 no 6 pp 643ndash649 1998

[10] C C Appleton T I Mosala J Levin and A Olsen ldquoGeo-helminth infection and re-infection after chemotherapy amongslum-dwelling children in Durban South Africardquo Annals ofTropical Medicine and Parasitology vol 103 no 3 pp 249ndash2612009

[11] A M van Eijk K A Lindblade F Odhiambo et al ldquoGeo-helminth infections among pregnant women in rural westernKenya a cross-sectional studyrdquo PLoS Neglected Tropical Dis-eases vol 3 no 1 article e370 2009

[12] C Nokes S M Grantham-McGregor A W Sawyer E SCooper B A Robinson and D A P Bundy ldquoModerate toheavy infections of Trichuris trichiura affect cognitive functionin Jamaican school childrenrdquo Parasitology vol 104 no 3 pp539ndash547 1992

[13] Webuye Health and Demographic Surveillance System FactSheet no 1 2009 Unpublished data

[14] Webuye District Hospital Annual Report 2008 Unpublisheddata

[15] Webuye Climate Pattern 2012 httpenwikipediaorgwikiWebuye

[16] C J Simiyu V Naanyu A Obala et al ldquoEstablishing webuyehealth and demographic surveillance site in rural western

Journal of Tropical Medicine 7

Kenya challenges and lessons learnedrdquo in Population Associ-ation of America Annual Meeting Problem New Orleans LaUSA April 2013

[17] O M Mugenda and A G Mugenda Research MethodsQuantitative and Qualitative Approaches African Centre ofTechnology Studies Nairoibi Kenya 1999

[18] L S Ritchie ldquoAn ether sedimentation technique for rou-tine stool examinationrdquo Bulletin United States Army MedicalDepartment vol 8 article 326 1948

[19] V Mehraj J Hatcher S Akhtar G Rafique and M A BegldquoPrevalence and factors associated with intestinal parasiticinfection among children in an urban slum of Karachirdquo PLoSONE vol 3 no 11 Article ID e3680 2008

[20] Z Tahir ldquoComparasion of prevalence of intestinal parasites inchildren and adult populationrdquo Biomedica vol 18 pp 74ndash752002

[21] V Srinivasan S Radhakrishna A M Ramanathan and SJabbar ldquoHookworm infection in a rural community in SouthIndia and its association with haemoglobin levelsrdquo Transactionsof the Royal Society of Tropical Medicine andHygiene vol 81 no6 pp 973ndash977 1987

[22] M I Siddiqui F M Bilqees M Iliyas and S PerveenldquoPrevalence of parasitic infections in a rural area of KarachiPakistanrdquo Journal of the Pakistan Medical Association vol 52no 7 pp 315ndash320 2002

[23] Kenya National School-Based Deworming Program httpwwwdewormtheworldorgour-workkenya-national-school-based-deworming-program

[24] Z H Chaudhry M Afzal and M A Malik ldquoEpidemiologicalfactors affecting prevalence of intestinal parasites in children ofMuzaffarabad districtrdquo Pakistan Journal of Zoology vol 36 no4 pp 267ndash271 2004

[25] RMullerWorms andDisease AManual ofMedicalHelminthol-ogy Butler and Tanners 1975

[26] A Jardim-Botelho S Raff R D A Rodrigues et al ldquoHook-worm Ascaris lumbricoides infection and polyparasitism asso-ciated with poor cognitive performance in Brazilian schoolchil-drenrdquo Tropical Medicine and International Health vol 13 no 8pp 994ndash1004 2008

[27] G T Keusch and P Migasena ldquoBiological implications ofpolyparasitismrdquo Reviews of Infectious Diseases vol 4 no 4 pp880ndash882 1982

[28] Webuye economic activities and soil types httpwwwchincicomtravelpaxq178201WebuyeKEKenya0

[29] FAO Corporate Document Repository 1988 ldquoManagement ofVertisols in sub-Saharan Africardquo in Proceedings of a Confer-ence Held at ILCA Addis Ababa Ethiopia September 1987httpwwwfaoorgWairdocsILRIx5493Ex5493e00htm

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

International Journal of

EndocrinologyHindawi Publishing Corporationhttpwwwhindawicom

Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

BioMed Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

PPARRe sea rch

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Parkinsonrsquos DiseaseHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 6: Webuye Health and Demographic Surveillance Systems

6 Journal of Tropical Medicine

spell between September andDecember each year during theperiod which temperatures may be conducive but the type ofsoils found in Webuye is mostly clay enriched which mostprobably hold on to the eggs This type of soils also retainsheat for long periods which is inimical to the developmentand dispersion of helminths eggs [28 29] The childreninfected with intestinal parasites were treated at WebuyeDistrict Hospital and other nearby health facilities howeverhelminths egg counts and anthropometric measurementswere not undertaken to provide the baseline informationupon which future studies can be assessed

4 Conclusions and Recommendations

Giardia lamblia and E histolytica were the most prevalentpathogenic intestinal protozoa while STHs were less com-mon among these rural children Further research is requiredto elucidate the factors responsible for low STH prevalenceamong this rural children population The parasites reportedhere are feco-orally transmitted and can easily be containedby the improvement of environmental hygiene Community-based health promotions including regular checkups andtreatment and personal and environmental hygiene arehighly recommended for the control of the intestinal parasitesinfesting children at Webuye HDSS area

Conflict of Interests

The authors declare no conflict of interests The studymethodology execution report and conclusion reflect solelythe authorsrsquo research and scientific work and are not theresponsibility of affiliate institutions or the funding organi-zations

Authorsrsquo Contribution

A A Obala C J Simiyu D O Odhiambo H D NNyamogoba D Menya P O Ayuo R Downing D ChelagatA W Mwangi P Chege and W P Orsquo Meara designed thestudy and took part in data collection processing and analy-sis and paper writing M Twagirumukiza D VandenbroekB B O Otsyula and J de Maeseneer critically reviewed thepaper during preparation

Acknowledgments

The authors acknowledge the assistance received from theProvincial Administration and other stakeholders formakingit possible to access the community They thank Webuyeresidents for their cooperation and for accepting to partic-ipate in this study They acknowledge the assistance of theWebuye HDSS project field supervisors and enumeratorsfor supervision of field activities and specimen collectionrespectively Mr Arthur Aroko Ms Edna Kurgat Mr IsaacMutai and Mr Paul Olang processed and examined thespecimen for which they are very grateful They thank theDeans of Schools of Medicine Public Health and Nursingfor granting them permission to collect data and compile

this report Funds for this project were provided by theMoi University (Kenya)mdashVLIRUOS (Belgium) collaborativeprogramme

References

[1] P J Hotez P J Brindley J M Bethony C H King E J Pearceand J Jacobson ldquoHelminth infections the great neglectedtropical diseasesrdquo Journal of Clinical Investigation vol 118 no4 pp 1311ndash1321 2008

[2] S Waqar H Hussain R Khan et al ldquoIntestinal parasitic infec-tions in children from the Northern Pakistanrdquo Infectious Dis-eases Journal vol 12 pp 73ndash77 2003

[3] R W Steketee ldquoPregnancy nutrition and parasitic diseasesrdquoJournal of Nutrition vol 133 pp 1661Sndash1667S 2003

[4] F Curtale P Pezzotti A L Sharbini et al ldquoKnowledge per-ceptions and behaviour of mothers toward intestinal helminthsin Upper Egypt implications for controlrdquo Health Policy andPlanning vol 13 no 4 pp 423ndash432 1998

[5] J Bethony S Brooker M Albonico et al ldquoSoil-transmittedhelminth infections ascariasis trichuriasis and hookwormrdquoThe Lancet vol 367 no 9521 pp 1521ndash1532 2006

[6] D R Pillai and K C Kain ldquoCommon intestinal parasitesrdquoCurrent Treatment Options in Infectious Diseases vol 5 pp 207ndash217 2003

[7] T Minenoa and M A Avery ldquoGiardiasis recent progress inchemotherapy and drug developmentrdquo Current PharmaceuticalDesign vol 9 pp 841ndash855 2003

[8] R Ndyomugyenyi N Kabatereine A Olsen and PMagnussenldquoMalaria and hookworm infections in relation to haemoglobinand serum ferritin levels in pregnancy in Masindi districtwestern Ugandardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 102 no 2 pp 130ndash136 2008

[9] A Olsen PMagnussen J H Ouma J Andreassen andH FriisldquoThe contribution of hookworm and other parasitic infectionsto haemoglobin and iron status among children and adults inwestern Kenyardquo Transactions of the Royal Society of TropicalMedicine and Hygiene vol 92 no 6 pp 643ndash649 1998

[10] C C Appleton T I Mosala J Levin and A Olsen ldquoGeo-helminth infection and re-infection after chemotherapy amongslum-dwelling children in Durban South Africardquo Annals ofTropical Medicine and Parasitology vol 103 no 3 pp 249ndash2612009

[11] A M van Eijk K A Lindblade F Odhiambo et al ldquoGeo-helminth infections among pregnant women in rural westernKenya a cross-sectional studyrdquo PLoS Neglected Tropical Dis-eases vol 3 no 1 article e370 2009

[12] C Nokes S M Grantham-McGregor A W Sawyer E SCooper B A Robinson and D A P Bundy ldquoModerate toheavy infections of Trichuris trichiura affect cognitive functionin Jamaican school childrenrdquo Parasitology vol 104 no 3 pp539ndash547 1992

[13] Webuye Health and Demographic Surveillance System FactSheet no 1 2009 Unpublished data

[14] Webuye District Hospital Annual Report 2008 Unpublisheddata

[15] Webuye Climate Pattern 2012 httpenwikipediaorgwikiWebuye

[16] C J Simiyu V Naanyu A Obala et al ldquoEstablishing webuyehealth and demographic surveillance site in rural western

Journal of Tropical Medicine 7

Kenya challenges and lessons learnedrdquo in Population Associ-ation of America Annual Meeting Problem New Orleans LaUSA April 2013

[17] O M Mugenda and A G Mugenda Research MethodsQuantitative and Qualitative Approaches African Centre ofTechnology Studies Nairoibi Kenya 1999

[18] L S Ritchie ldquoAn ether sedimentation technique for rou-tine stool examinationrdquo Bulletin United States Army MedicalDepartment vol 8 article 326 1948

[19] V Mehraj J Hatcher S Akhtar G Rafique and M A BegldquoPrevalence and factors associated with intestinal parasiticinfection among children in an urban slum of Karachirdquo PLoSONE vol 3 no 11 Article ID e3680 2008

[20] Z Tahir ldquoComparasion of prevalence of intestinal parasites inchildren and adult populationrdquo Biomedica vol 18 pp 74ndash752002

[21] V Srinivasan S Radhakrishna A M Ramanathan and SJabbar ldquoHookworm infection in a rural community in SouthIndia and its association with haemoglobin levelsrdquo Transactionsof the Royal Society of Tropical Medicine andHygiene vol 81 no6 pp 973ndash977 1987

[22] M I Siddiqui F M Bilqees M Iliyas and S PerveenldquoPrevalence of parasitic infections in a rural area of KarachiPakistanrdquo Journal of the Pakistan Medical Association vol 52no 7 pp 315ndash320 2002

[23] Kenya National School-Based Deworming Program httpwwwdewormtheworldorgour-workkenya-national-school-based-deworming-program

[24] Z H Chaudhry M Afzal and M A Malik ldquoEpidemiologicalfactors affecting prevalence of intestinal parasites in children ofMuzaffarabad districtrdquo Pakistan Journal of Zoology vol 36 no4 pp 267ndash271 2004

[25] RMullerWorms andDisease AManual ofMedicalHelminthol-ogy Butler and Tanners 1975

[26] A Jardim-Botelho S Raff R D A Rodrigues et al ldquoHook-worm Ascaris lumbricoides infection and polyparasitism asso-ciated with poor cognitive performance in Brazilian schoolchil-drenrdquo Tropical Medicine and International Health vol 13 no 8pp 994ndash1004 2008

[27] G T Keusch and P Migasena ldquoBiological implications ofpolyparasitismrdquo Reviews of Infectious Diseases vol 4 no 4 pp880ndash882 1982

[28] Webuye economic activities and soil types httpwwwchincicomtravelpaxq178201WebuyeKEKenya0

[29] FAO Corporate Document Repository 1988 ldquoManagement ofVertisols in sub-Saharan Africardquo in Proceedings of a Confer-ence Held at ILCA Addis Ababa Ethiopia September 1987httpwwwfaoorgWairdocsILRIx5493Ex5493e00htm

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

International Journal of

EndocrinologyHindawi Publishing Corporationhttpwwwhindawicom

Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

BioMed Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

PPARRe sea rch

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Parkinsonrsquos DiseaseHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 7: Webuye Health and Demographic Surveillance Systems

Journal of Tropical Medicine 7

Kenya challenges and lessons learnedrdquo in Population Associ-ation of America Annual Meeting Problem New Orleans LaUSA April 2013

[17] O M Mugenda and A G Mugenda Research MethodsQuantitative and Qualitative Approaches African Centre ofTechnology Studies Nairoibi Kenya 1999

[18] L S Ritchie ldquoAn ether sedimentation technique for rou-tine stool examinationrdquo Bulletin United States Army MedicalDepartment vol 8 article 326 1948

[19] V Mehraj J Hatcher S Akhtar G Rafique and M A BegldquoPrevalence and factors associated with intestinal parasiticinfection among children in an urban slum of Karachirdquo PLoSONE vol 3 no 11 Article ID e3680 2008

[20] Z Tahir ldquoComparasion of prevalence of intestinal parasites inchildren and adult populationrdquo Biomedica vol 18 pp 74ndash752002

[21] V Srinivasan S Radhakrishna A M Ramanathan and SJabbar ldquoHookworm infection in a rural community in SouthIndia and its association with haemoglobin levelsrdquo Transactionsof the Royal Society of Tropical Medicine andHygiene vol 81 no6 pp 973ndash977 1987

[22] M I Siddiqui F M Bilqees M Iliyas and S PerveenldquoPrevalence of parasitic infections in a rural area of KarachiPakistanrdquo Journal of the Pakistan Medical Association vol 52no 7 pp 315ndash320 2002

[23] Kenya National School-Based Deworming Program httpwwwdewormtheworldorgour-workkenya-national-school-based-deworming-program

[24] Z H Chaudhry M Afzal and M A Malik ldquoEpidemiologicalfactors affecting prevalence of intestinal parasites in children ofMuzaffarabad districtrdquo Pakistan Journal of Zoology vol 36 no4 pp 267ndash271 2004

[25] RMullerWorms andDisease AManual ofMedicalHelminthol-ogy Butler and Tanners 1975

[26] A Jardim-Botelho S Raff R D A Rodrigues et al ldquoHook-worm Ascaris lumbricoides infection and polyparasitism asso-ciated with poor cognitive performance in Brazilian schoolchil-drenrdquo Tropical Medicine and International Health vol 13 no 8pp 994ndash1004 2008

[27] G T Keusch and P Migasena ldquoBiological implications ofpolyparasitismrdquo Reviews of Infectious Diseases vol 4 no 4 pp880ndash882 1982

[28] Webuye economic activities and soil types httpwwwchincicomtravelpaxq178201WebuyeKEKenya0

[29] FAO Corporate Document Repository 1988 ldquoManagement ofVertisols in sub-Saharan Africardquo in Proceedings of a Confer-ence Held at ILCA Addis Ababa Ethiopia September 1987httpwwwfaoorgWairdocsILRIx5493Ex5493e00htm

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

International Journal of

EndocrinologyHindawi Publishing Corporationhttpwwwhindawicom

Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

BioMed Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

PPARRe sea rch

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Parkinsonrsquos DiseaseHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 8: Webuye Health and Demographic Surveillance Systems

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

International Journal of

EndocrinologyHindawi Publishing Corporationhttpwwwhindawicom

Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

BioMed Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

PPARRe sea rch

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Parkinsonrsquos DiseaseHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom