Enteroparasitism In Hard-to-Reach Community Dwellers: A .

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HindawiJournal of Parasitology ResearchVolume 2020, Article ID 8890998, 11 pageshttps://doi.org/10.1155/2020/8890998Research ArticleEnteroparasitism in Hard-to-Reach Community Dwellers: ACross-Sectional Study in Ga West Municipality in GhanaEnoch Aninagyei ,1 Ruby Yirenkyi,2 Tanko Rufai,3,4 and Margaretta Gloria Chandi51Department of Biomedical Sciences, School of Basic and Biomedical Sciences, University of Health and Allied Sciences, Ho,Volta Region, Ghana2Department of Molecular Biology and Biotechnology, University of Cape Coast, Cape Coast, Ghana3Ghana Health Service, Accra, Ghana4New Juabeng Municipal Health Directorate, Koforidua, Ghana5Ga North Municipal Health Directorate, Ofankor-Accra, Greater Accra Region, GhanaCorrespondence should be addressed to Enoch Aninagyei; eaninagyei@uhas.edu.ghReceived 15 June 2020; Revised 20 August 2020; Accepted 21 August 2020; Published 24 September 2020Academic Editor: Bernard MarchandCopyright 2020 Enoch Aninagyei et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work isproperly cited.Ga West Municipality in Ghana is predominantly rural with about forty-eight hard-to-reach communities. Several infectiousdiseases such as Buruli ulcer, tuberculosis, yaws, schistosomiasis, and malaria are prevalent in the municipality. However, theprevalence and characteristics of enteroparasites in the municipality are unknown. Therefore, this cross-sectional studydetermined the prevalence of enteroparasites in these hard-to-reach communities. Samples were collected from fivecommunities, namely, Opah, Otuaplem, Dedeman, Onyansana, and Manchie. A total of 538 stool samples were collected fromthe community dwellers. Each sample was examined with eosin-saline wet preparation and formol-ether concentrationtechnique. Body mass index, haemoglobin, and albumin concentrations were used to assess nutritional status. Seven differentparasite species were identified in 178 community dwellers (33.1% prevalence (95% CI: 0.29–0.37)). The individual prevalence ofthe identified parasites was Schistosoma mansoni (13.4%), Entamoeba histolytica (7.2%), Ascaris lumbricoides (6.9%), Giardialamblia (5.0%), hookworm (4.8%), Strongyloides stercoralis (4.8%), and Balantidium coli (1.6%). Among the 178 parasitizedindividuals, 68.0% were singly infected while 31.5% had dual parasitism. Significantly higher infections were associated withOnyansana dwellers (p 0:019), participants aged 16–20 years (p 0:006), unmarried participants (p 0:001), those withoutformal education (p 0:044), and crop farmers (p 0:044). However, among the Akan tribe (p 0:015), Christians (p 0:03),and participants with higher incomes (p 0:012), infections were found to be lower. Compared to monoparasitism, dualparasitism was significantly associated with underweight (17.8 vs. 20.3 kg/m2), anaemia (7.7 vs. 9.8 g/dL), and malnutrition (27.6vs. 31.9 g/L of albumin concentration). These findings underscore the fact that the Ga West Municipality is heavily burdenedwith different species of enteroparasites. Therefore, education on personal hygiene to reduce parasitic infections must beintensified while implementing regular mass deworming exercise in the municipality.1. IntroductionGa West Municipality is one of the sixteen districts in theGreater Accra Region of Ghana. The municipality is 60%rural, 25% periurban, and 15% urban. It is made up of about150 communities with Amasaman as its municipal capital[1]. It occupies a total land surface area of about 300 squarekilometers with an estimated population of 262,742 as of2015 [2]. Of the 150 communities in the municipality, about48 communities (32%) are hard-to-reach. These hard-toreach communities have been cut off from other communities by poor road infrastructure and defective bridges. Inrainy seasons (mid-May to July), these roads are not motorable. These communities lack good health facilities witheducational facilities only at the basic school level. Also, somebasic social amenities are lacking. Potable water is lacking in

2almost all of these hard-to-reach communities except waterfrom hand-operated wells and dug-outs in some “fortunate”communities. Residents rely mostly on rivers and streams forsurvival [3].Some infectious diseases are very prevalent in the municipality, and residents in these hard-to-reach communities aremostly affected. Buruli ulcer, a disease caused by Mycobacterium ulcerans, is highly prevalent in these communities [1, 4]as well as yaws, a tropical disease caused by Treponema pertenue [5]. In these communities, tuberculosis, caused byMycobacterium tuberculosis [6, 7], has also been found tobe prevalent. Parasitic diseases such as malaria [8] and schistosomiasis [8, 9] are very common in the municipality, particularly in these poor communities.Despite high prevalence of these infectious diseases inthese communities, the burden of enteroparasites isunknown, hence scarcity of data in this regard. Therefore,this study was designed to determine the prevalence of enteroparasites in residents of these hard-to-reach communities inthe Ga West Municipality of the Greater Accra Region ofGhana and also to determine some factors and clinical effectsthat are associated with enteroparasitism in parasitizedindividuals.2. Methods2.1. Study Design and Study Plan. This observational study,conducted between September 2019 and March 2020, wascarried out to determine the prevalence of enteroparasitesin selected communities in Ghana. Demographic indicatorsassociated with parasitism were explored. Also, the effectsof enteroparasitism on parasitized individuals weredescribed. A list of hard-to-reach communities was obtainedfrom the Ga West Municipal Health Administration.2.2. Description of Study Areas. This study was done in hardto-reach communities in the Ga West Municipality in theGreater Accra Region of Ghana. The communities wereOpah, Otuaplem, Dedeman, Onyansana, and Manchie(Figure 1). These five communities were blindly selectedfrom a list of about 48 communities in a simple randommanner. From the municipal capital, Amasaman, where themunicipal hospital was located, Opah, Manchie, Onyansana,Dedeman, and Otuaplem are about 16 km, 19 km, 20 km,26 km, and 28 km away, respectively. These communitiesare connected to the municipal capital by poor road networks. By road, it takes approximately 45 minutes to travelfrom Opah to Amasaman and about 2 hours to travel fromthe other four communities to Amasaman. These are predominantly farming communities with uncoordinated sandwinning activities. None of these communities has either ahospital or a clinic. In Ghana, the basic health care facilityis community-based health services (CHPS). These hard-toreach communities do not have a CHPS compound. Residents travel to nearby communities to assess communityhealth services.2.3. Selection of Households, Study Participants, and StoolSample Collection. With the help of the community leaders,Journal of Parasitology Researcheach household was numbered after which 10% of households were randomly selected to select participants from.Consent to include the household in the study was soughtfrom the heads of the household. Consent to participatewas also obtained from all participants and assent for participants under 18 years obtained from their guardians. Afterobtaining consent, the number of household occupants wasnoted and half of that number, to the nearest whole number,was sampled. A number of stool containers corresponding tohalf the number of household occupants were given to theheads of the household to be given, randomly, to the occupants for provision of about 4 g stool samples. The heads ofthe household were taken through proper stool sample collection protocols. Briefly, during defecation, the prelabelledstool container was opened, with the aid of the accompanying plastic disposable spoon; at least five spoonfuls were collected into the container. In the case of watery stool,containers were filled, using the disposable plastic funnelprovided, to about one-third, without soiling the container.After sample collection, household heads ensured that thehands were properly washed and disinfected with a handsanitizer containing 70% alcohol. Stool samples were provided by participants early in the morning, placed in a prelabelled biohazard bag, and kept in a biohazard container.Samples were collected by 10 am and sent to the laboratory.2.3.1. Sample Size Determination. The minimum number ofsamples collected from the study sites was determined usingthe formula n z2 pð1 pÞ/d 2 , where n is the sample size, p prevalence of enteroparasitism in Ga West Municipality, z confidence level at 95% (standard value of 1.96), and d margin of error at 5% (standard value of 0.05) [10]. Prevalence of enteroparasitism in Ga West is unknown, so prevalence was estimated at 50%. The sample size was calculatedto be 384. To cater for missing and incomplete data, the sample size was increased by 10%. Therefore, the minimumsample size was 423.2.3.2. Inclusion and Exclusion Criteria. Households includedin this study were household with available heads to consentto the study. Also, participants included in the study werehousehold occupants over five years old and those that havestayed in the community for at least a year. On the otherhand, residents that have dewormed, using a Ministry ofHealth-approved dewormer, were excluded. Finally, household occupants that dissented participation and individualsthat declined blood sample collection were also excluded.2.4. Stool and Blood Sample Collection and Collection ofRelevant Study Information. Early in the morning of sampleprovision, the research team was in the household to collectstool and blood samples and then administer a questionnaireto obtain some information from the study participant.Information obtained from the participants was age, gender,highest education, and occupation. Stool samples weredivided into two equal parts; one part was fixed in 10%formol-saline solution and the other left unfixed. A samplepair was kept at ambient temperature prior to arrival in theGa North Municipal laboratory. Whole blood was collected

Journal of Parasitology Research3% parasitismOpah (45.6%)Otuaplem (30.1%)Onyansana (34.9%)Dedeman (18.1%)Manchie (32.3%)Figure 1: Map of Ga West Municipality, Ghana, showing study sites in red and prevalence of parasitism in study communities (the map is theauthors’ own production).from a prominent vein at the antecubital fossa region ofthe forearm. Prior to blood collection, the selected areato perform venepuncture was disinfected with 70% alcoholand allowed to air dry before performing venepuncture.Five mL of whole blood was collected into the EDTA tube,mixed gently, and kept on ice till plasma was separatedinto another tube.2.5. Nutritional Assessment. Body mass index (BMI), haemoglobin, and albumin concentrations were used to assess thenutritional status of the participants as previously used [11, 12].2.5.1. Determination of Body Mass Indices. BMI was calculated by dividing the weight in kilograms (kg) by the squareof height in meters. Height was taken by a Seca 213 portable stadiometer (New Zealand), and body weight was takenby an Omron digital weighing scale (Omron, Kyoto,Japan). Height was taken barefooted, and weight was alsotaken in light cloths. Participants with BMI in kg/m2 18:5, 18.5-24.9, 25.0-29.9, and 30.0 were classified asunderweight, normal, overweight, and obese, respectively,according to [13].2.5.2. Determination of Haemoglobin Concentration. Haemoglobin concentration was determined by using a hand-heldhaemoglobinometer (URIT-12, Guangzhou, China). Priorto first use, the meter was calibrated using the accompanying calibration chip. The haemoglobin concentration wasdetermined following the manufacturer’s instruction.Briefly, a strip was inserted into the meter till the drop ofblood sign appears on the screen; a drop of well-mixedanticoagulated blood was dropped on the sample receptacleportion of the strip. A result was obtained in about 5 seconds. Haemoglobin levels 8:0 g/dL, 8.0-10.9 g/dL, 11.0–11.9 g/dL, and 12.0 g/dL were classified as severe anaemia,moderate anaemia, mild anaemia, and nonanaemic, respectively, according to a World Health Organization publication on haemoglobin concentrations for the diagnosis ofanaemia and assessment of severity [14].2.5.3. Determination of Albumin Concentration. The albuminconcentration was measured by a PKL-125 Italia fullyautomated chemistry analyser using an ELItech albumin endpoint reagent (France) based on the reaction: albumin bromocresol green ðBCGÞ albumin‐BCG complex.The albumin-BCG complex absorbs maximally at630 nm. Albumin values below mean minus 1SD and abovemean minus 2SD indicated malnourishment while valuesbelow mean minus 2SD indicated severe malnourishment.Classification was adopted from Omitola et al. [15].

4Journal of Parasitology ResearchTable 1: Association of prevalence of enteroparasitism with sociodemographic variables.Demographic characteristicsResident MalesFemalesAge range –40 40Marital tionalOthersbAverage monthly incomec0–500 (0–90)501–1000 (91–181)1001–1500 (182–272)1501–2000 (273–363) 2000 ( 364)Highest educationNonePrimaryJunior highSenior highPostsenior highNumber of samplesPrevalence of parasitismNumber of infected individuals%149 (27.7%)136 (25.3%)105 (19.5%)83 (15.4%)65 (12.1%)684119292145.630.118.134.932.3331 (61.5%)207 (38.5%)1156355.519.057 (10.6%)118 (21.9%)110 (20.4%)79 (14.7%)89 (16.5%)41 (7.6%)25 (4.6%)19 88 (34.9)294 (54.6)18 (3.3)38 (7.1)105633755.921.416.718.459 (11.0)87 (16.2)279 (51.9)33 (6.1)71 (13.2)9 (1.7)832711748213.636.825.451.567.622.2282 (52.4)192 (35.7)49 (9.1)15 (2.8)669119223.447.438.813.3120 (28.9)82 (19.8)78 (18.8)59 (14.2)76 (18.3)56332913946.740.237.222.011.893 (17.3%)181 (33.6%)153 (28.4)89 (16.5%)22 (4.1%)53613328356.933.721.631.513.6Chi-squared testp valueChi-squared value (χ2 )21.9 0.00011.10.30189.9 0.000167.9 0.000161.8 0.000191.1 0.000138.4 0.000137.1 0.0001

Journal of Parasitology Research5Table 1: Continued.Demographic characteristicsOccupationUnemployedPupilPetty tradingSand winningFarmingType of farmingCropPoultryLivestockNumber of samplesPrevalence of parasitismNumber of infected individuals%41 (7.6%)82 (15.2%)30 (5.6%)47 (8.7%)338 (62.8%)112751711826.832.916.736.134.9209 (61.8%)47 (13.9%)82 (24.3%)98713Chi-squared testp valueChi-squared value (χ2 )5.10.27836.9 0.000146.914.615.8aOther tribes were Frafra (n 1), Guan (n 2), Hausa (n 3), and Krobo (n 3); bBuddhist (n 2), Afrikanian mission (n 4), unification movement (n 4),and atheist (n 5); cincome quoted in Ghana cedi ( ), exchange rate of 1 USD to 5.5 Ghana cedis.2.6. Microscopic Detection of Enteroparasites2.6.1. Detection of Enteroparasites Using Eosin-Saline WetPreparation. On the same day of sample arrival in the laboratory, wet preparation was made to determine viable parasites. The stool sample was well mixed in its container anda drop transferred onto a microscope slide. The samplewas emulsified on the slide using equal volume of normalsaline and eosin mixture. The emulsified stool sample wasexamined using 10 and 40 objective of the microscope.Parasites were identified using their characteristic shapeand motility [16].2.6.2. Detection of Enteroparasites Using Formol EtherConcentration (FEC) Method. Stool samples were emulsifiedwith saline (0.9% NaCl) into a homogenous mixture. OnemL of the homogenate was poured into a centrifuge tubeafter which 4.0 mL of formol-saline reagent was added. Themixture was vortexed vigorously before another 3.0 mL of10% formol-saline was added. The content was mixed andsieved through a nonabsorbent sieve (3- or 4-folds). Subsequently, 3 mL of diethyl ether (Honeywell, USA: bp: 34.6 C,mp: -116.3 C, mm: 74.12 g/mol) was added and vortexed vigorously. The content was centrifuged at 3,000 rpm for 2minutes. Supernatant was discarded, and iodine-mixeddeposits were examined at 10 and 40. Parasite ova wereidentified using characteristic shapes [16].2.7. Deworming of the Infected Individuals. Infected individuals were referred to nearby hospitals for treatment according to World Health Organization guidelines [17, 18].Whereas praziquantel (20 mg/kg) was used to treat for S.mansoni, the other parasites were treated with albendazole(400 mg). This treatment protocol was reviewed andapproved by the Ghana Health Service Ethical Review Committee (Reference: GHS-REC002/03/18).2.8. Outcome of the Study. The study reported overall andindividual prevalence of enteroparasites identified in thestudy sites. The morphological characterization of the parasites was reported. Also, the frequencies of parasitism in thevarious age ranges, gender category, educational status, andoccupation were reported. Finally, the effects of the parasiteson nutritional status determined by body mass index, haemoglobin, and albumin concentrations were also reported.2.9. Data Analysis. Frequencies were presented usingpercentages while prevalence was calculated based on thenumber of individuals parasitized divided by the total number of individuals tested in each category. Parasitism wasclassified as single, dual, and triple parasitism when one,two, or three different parasites were found in an individual.A chi-squared test was used to examine the associationbetween infectious status and the independent variableswhile the logistic regression model was used as a post hocanalysis tool. Statistical analysis was done by SPSS Version24 (Chicago, IL, USA). p value of less than 0.05 was considered statistically significant.3. Results3.1. Demographic Characteristics of the Study Participants.Study participants (n 538) were selected from five hardto-reach communities in Ga West Municipality, namely,Opah (n 149), Otuaplem (n 136), Dedeman (n 105),Onyansana (83), and Manchie (n 65). Majority of the participants (61.5%) were males while the modal age range was16–20 years. A little over 50% of the participants has neverhad formal education or has had only primary education. Itwas also found that 62.8% of the participants were farmerswhile the rest were either unemployed, pupils in primaryschool, petty traders, or sand winners. Of the 338 (62.8%)farmers, 61.8% were crop farmers and 13.9% were poultryfarmers while 24.3% were livestock farmers (Table 1).3.2. Prevalence of Enteroparasitism. The overall prevalence ofenteroparasitism in the hard-to-reach communities in themunicipality was 33.1% (178/538) (95% CI: 0.29–0.37). Themost prevalent community was Opah (45.6%) while Dedeman was the least prevalent (18.1%). The other three communities were almost equiprevalent (30.1–34.9%)(Figure 1). Prevalence of parasitism among males andfemales was 55.5% and 19.0%, respectively. Community

6Journal of Parasitology ResearchTable 2: Logistic regression analysis of significant associations of enteroparasitism with study variables.Study variablesResident communityOpahOtuaplemDedemanOnyansanaManchie (reference)Age range –40 40 (reference)Marital statusSingleMarriedWidowedDivorced (reference)TribeAkanGaEweDagombaFulaniOthers (reference)ReligionChristianityβS.E.WalddfSig.Exp .019 .2237.61510.6490.0720.006 5010.2490.3985.9331.60613.6441 0.001 .4622.665-2.9641.2135.96910.015 0.05

2Department of Molecular Biology and Biotechnology, University of Cape Coast, Cape Coast, Ghana 3Ghana Health Service, Accra, Ghana 4New Juabeng Municipal Health Directorate, Koforidua, Ghana 5Ga North Municipal Health Directorate, Ofankor-Accra, Greater Accra Region, Ghana Correspondence should be addressed to Enoch Aninagyei; eaninagyei@uhas .

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