Optimizing School-based Intestinal Helminth Control .

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Page 2INVITED REVIEWOptimizing school-based intestinal helminth control interventions in thePhilippinesAUTHORS: Vicente Y. Belizario, Jr. *, Alexander H. Tuliao, *, Francis G. Totanes*, Camille L.Asuncion**National Institutes of Health, University of the Philippines, ManilaKEYWORDS:Soil-transmitted helminthes, Ascaris, Trichuris, Schistosomiasis, Schistosomes, Helminth controlCORRESPONDENCE:Dr. Vicente Y. BelizarioEmail: vbelizar@yahoo.comABSTRACTIntestinal helminth infections caused by soil-transmitted helminths and schistosomes bring about thegreatest burden of disease in poverty-stricken areas in the developing world. The most vulnerable group andthe most significant contributors to disease transmission are the school-age children. While awaiting majorimprovements on sanitation, the recommended strategy for helminth control is school-based, teacherassisted, mass drug administration (MDA). However, millions of individuals worldwide remain afflicted withthese diseases, and the Philippines is no different from many of the developing countries. The overallobjective of this paper is to review current Philippine control programs and initiatives and offer evidencebased recommendations for improvement. Discrepancies between parasitologic parameters and drugcoverage rates pose significant challenges in the control and prevention of helminth infections in thecountry. School-based MDA may be scaled up after successful local initiatives, where teachers have directparticipation in drug administration. There is also a need to involve the social science sector to help addressthe behavioral aspects of helminth control. Moreover, monitoring and evaluation of interventions throughidentification of success parameters will contribute to the optimization of school-based helminth control,and to strategies towards effective control of intestinal helminth infections as a public health problem in thecountry.Dr. Vicente Y. Belizario, Jr. earned his Doctor of Medicine degree from the University ofthe Philippines Manila (UPM) in 1985 and his Master of Tropical Medicine and Hygienedegree from the Uniformed Services University of the Health Sciences (USUHS) inBethesda, Maryland, U.S.A. in 1991 through a fellowship from the World HealthOrganization (WHO). He is a Professor of Parasitology and Public Health, and UniversityScientist II in the College of Public Health, UPM and also currently serves as the ViceChancellor for Research and Executive Director of the National Institutes of Health (NIH)in the same university. He is the principal investigator of research projects on variousaspects of tropical and parasitic diseases including their epidemiology, diagnosis,treatment, control and prevention. He is also the convenor of the Neglected TropicalDiseases Study Group in the UPM-NIH that advocates the use of research results as bases for policy and planningof the Department of Health, the Department of Education, and various local government units of the Republic ofthe Philippines. In the international arena, he has shared his expertise on parasitic diseases on many occasionsto the Southeast Asian Ministers of Education – Tropical Medicine and Public Health Network (SEAMEOTROPMED) and other non-government organizations. He currently serves as a member of the Scientific andTechnical Advisory Committee (STAC) of the WHO Special Programme for Research and Training in TropicalDiseases (TDR).Downloaded from www.pidsphil.org

Page 3INTRODUCTIONNeglected tropical diseases (NTDs) arediseases of poverty that are among the mostcommon infections that plague developingcountries. The most common NTDs are of parasiticetiology, brought about by helminthiasis es, lymphatic filariae, and food-bornetrematodes.1 Helminth infections caused by STHsand schistosomes bring about the greatest burdenof disease in poverty-stricken areas in thedeveloping world.2 Recent worldwide estimatessuggest that 2 billion individuals are infected withsoil-transmitted helminthiasis and 200 million withschistosomiasis. Moreover, the chronic andinsidious clinical course of these infectionsdemonstrates the heavy burden of disease asshown by disability-adjusted life years (DALYs) lostof those infected (Table 1).3Table 1. Estimates of global morbidity in disability-adjustedlife years (DALYs) and mortality due to schistosomiasis and3STH infectionsNo.DALYsMortalityParasiteinfections andInfectedlost(thousands)diseases caused (millions) ylostomaduodenale, Necatoramericanus)Trichuris 0The objective of this paper is to review thecurrent situation of control programs andinitiatives in the Philippines and offer evidencebased recommendations for further improvementof strategies used in these large-scale healthinterventions in the school setting. Epidemiologicand morbidity data were collected from publishedscientific papers. Control strategies for STHinfections and schistosomiasis were gathered fromDownloaded from www.pidsphil.orgjournal articles and the World HealthOrganization. Philippine control programs andinitiatives were obtained from local scientificpublications and reports. Recommendations foroptimizing school-based control interventionswere formulated based on evidence andfeasibility.Soil-Transmitted Helminth InfectionsSTH infections refer to a group of parasiticdiseases caused by nematodes of major concernto humans: the roundworm, Ascaris lumbricoides;the whipworm, Trichuris trichiura; and thehookworms, Necator americanus and Ancylostomaduodenale. Transmission is through ingestion offecally-contaminated soil or water, and/or skinpenetration of larvae.2,3 STH infections persist indeveloping countries like the Philippines minate defecation,unhygienic eatingpractices, and lack of awareness predominate.EpidemiologyPrevalence of STH infections in the Philippineshas been investigated as early as the 1960s.Extensive biomedical studies on the prevalence ofhuman parasitic infections were conducted from1967 to 1983 by the former Philippine Ministry ofHealth through two research laboratories, the USNaval Medical Research Unit No. 2 (NAMRU-2) andthe Philippine Bureau of Research andLaboratories (BRL). The highest prevalence of STHinfection recorded in the studies was caused byTrichuris trichiura, with a prevalence of 94.5% inSorsogon, 90% in Northern Samar, and 80.5% inSurigao del Sur and Misamis Oriental.4Two parasitologic surveys conducted in 2000and 2006 demonstrated that STH infections stillpersist in the Philippines. In 2000, a baselinesurvey among public school children in selectedareas showed a cumulative prevalence of STHinfections from 51.6% in Quezon to City to 77% inNueva Ecija. The highest rates of heavy intensitySTH infections were from Cavite (22%) and Nueva

Page 4Ecija (11.3%). The most prevalent STHs, Ascarisand Trichuris, account for most of the heavyintensity infections.5A baseline survey was also done in 2006 for theIntegrated Helminth Control Program (IHCP) of theDepartment of Health (DOH). Among the publicelementary students in six sentinel sites, namely,Bulacan, Camarines Sur, Negros Occidental, Leyte,Compostela Valley, and Surigao del Norte, 54%were positive for STH infections. Cumulativeprevalence ranged from 33.2% in CompostelaValley to 67.4% in Negros Occidental. The overallproportion of heavy intensity infections was23.1%. Only Compostela Valley and Bulacan hadprevalence below 50% and heavy intensityinfections below 10%. However, prevalence of STHinfections may be higher than the estimatednumbers due to overall false negative rate of13.2%.6Morbidity and Public Health Implications onSchool-age ChildrenSevere Ascaris infection could lead to lunginfiltration, appendicitis, obstructive cholecystitis,pancreatitis, peritonitis, volvulus, and intestinalobstruction.7-10 A meta-analysis revealed thatobstruction is the most common clinicalcomplication of ascariasis.11 Infection withTrichuris could lead to dysentery, rectal prolapse,clubbing of fingers, and anemia.12 albuminemia, and pneumonitis.Of the three high-risk groups (pre-school agechildren, school-age children, and women ofchildbearing age), school-age children (SAC) bearthe highest burden of STH infections because oftheir increased nutritional needs, intensedevelopmental and learning capacities, and lack ofawareness in hygiene. As a result, heavy intensityinfections impair physical growth and cognitivedevelopment, induce micronutrient deficiencies,and lead to poor school performance andabsenteeism.3,14 In the previously mentionedbaseline study for the DOH-IHCP in 2006, availableDownloaded from www.pidsphil.orgdata on nutritional status showed that 14.8% ofthe school children were underweight while 19%were stunted. Furthermore, the average NationalAchievement Test score per subject was below thecompetency level of 75%, with the exception ofstudents in Loreto, Surigao del Norte.6 Thus,treatment of STH infections has been shown tosignificantly improve physical development of SACin the short-term and also produced a slightreduction in anemia in populations with relativelyhigh prevalence of STH infections.15Control StrategiesIn 2001, the Fifty-fourth World Health Assembly(WHA) drafted the WHA resolution 54.19 whichtargeted SAC (6-15 years) and endorsed schoolbased MDA as the main strategy in the short-termcontrol of STH infections in endemic areas, withthe overall aim of reducing the number of heavilyinfected individuals. The recommended drugs forSTH infections in school-based MDA arealbendazole 400 mg or mebendazole 500 mg. It isimportant to note that improvements insanitation, access to safe water, and behavioralchanges are still considered key factors toachieving long-term control. While improvementsin environmental and behavioral conditions arenot yet in place, the World Health Organization(WHO) recommends that school-based MDAshould take place twice a year because theprevalence of infections tends to return to theoriginal pre-treatment levels.16In the Philippines, the DOH in partnership withtheDepartmentofEducation(DepEd)implemented the IHCP according to AdministrativeOrder 2006-0028, with overall goals of: (1)reducing the prevalence of STH infections inchildren age 1 to 12 years to less than 50% by2010, and (2) lowering STH infections amongadolescent females, pregnant women, and otherspecial population groups. For control of STHinfections, the DOH recommends MDA withalbendazole or mebendazole twice a year forthree consecutive years, then yearly thereafter for

Page 5children age 1 to 12 years. The target drugcoverage of the IHCP is at least 85%. Aside fromthe targeted mass treatment, other componentsof the IHCP include health education and provisionof safe water, environmental sanitation, andpersonal hygiene (WASH).17SchistosomiasisSchistosomiasis is caused by five majortrematodes that infect humans: istosoma japonicum, Schistosoma mansoni,and Schistosoma mekongi. The life cycle ofschistosomiasis involves an intermediate snail hostthat releases larval forms (cercariae) in the water.Transmission occurs through contact with infectedwater and subsequent penetration of cercariaeinto the skin. Similar to STH infections,schistosomiasis is also associated with poverty,inadequate sanitation and water supply, and is is caused by Schistosomajaponicum, and its distribution is primarilydetermined by the snail Oncomelania hupensisquadrasi.2,3EpidemiologyThe first case of schistosomiasis in thePhilippines was reported in 1906. It was only in1932, however, that the freshwater snailOncomelania hupensis quadrasi was discovered inthe municipality of Palo in Leyte. Extensiveresearch on schistosomiasis then followedthroughout the early 1960s to the 1970s.18 Theprevalence of schistosomiasis in the Philippinesaveraged 10.4% in 1981 to 1985, with significantreduction among at risk population from 7.4% in1986 to 4.5% in 1997. Control interventionsincluding mass chemotherapy along with provisionof safe water, health education, and snail controlcontributed to the reduction in prevalence.19As of 2010, however, schistosomiasis remainsendemic in 190 municipalities in 28 provinces of12 regions in the Philippines.20 Results of aDownloaded from www.pidsphil.orgnational survey conducted from 2005 to 2007revealed that Mindanao had the highestendemicity (60%), followed by Visayas (45%), andLuzon (37.5%). By region, the Caraga Region(Agusan del Norte, Agusan del Sur, Surigao delNorte, and Surigao del Sur) had the highestprevalence rate at 1.63%, followed by Region 8(Northern Samar, Southern Samar, NorthernLeyte, and Southern Leyte) at 1.5%. The provinceswith the highest prevalence rates were Agusan delSur (3.95%), Northern Samar (2.4%), and EasternSamar (1.79%).21Currently available statistics on the prevalenceof S. japonicum may be significantlyunderestimated; several studies suggest thatprevalence are actually higher than previous orcurrent estimates. In a local survey done in twotowns of Agusan del Sur in 2005, the overallprevalence of schistosomiasis among public schoolchildren was 31.8%, a significantly higher rate thanthe previously recorded prevalence of 4%.22 In across-sectional study done in Western Samar, 98%of the participants were positive forschistosomiasis.23 In the two municipalities mostrecently identified as endemic for schistosomiasis(Gonzaga in Cagayan and Calatrava in NegrosOccidental), prevalence were as high as 10% and69%, respectively.20,24 Moreover, poor stoolexamination technique and limited capacity oflaboratory staff may contribute to underreporting,leading to inadequate monitoring and evaluationof health programs and limitations in the updatingof program guidelines.22Morbidity and Public Health ImplicationsClinical schistosomiasis could be severe andtends to involve several systems. Dysentery,diarrhea, and mucosal ulcerations can occur whenthere is colonic involvement. Hepatic and portalinvasion could result in hepatosplenomegaly,portal hypertension, and ascites.25,26 Corpulmonale and pulmonary hypertension mayoccur if there is severe lung involvement.27Cerebral schistosomiasis may also develop, with

Page 6complications of decreased sensorium, motor andsensory deficits, and meningoencephalitis.28Schistosomiasis is also linked to subtlemorbidities such as anemia, growth stunting,undernutrition, predisposition to and exacerbationof co-infections, cognitive underdevelopment,decreased work capacity, and chronic pain.14 In astudy done on children, adolescents, and youngadults in Leyte, results showed that high intensityinfections of S. japonicum may be related to irondeficiency anemia.29 Results of a cross-sectionalstudy done on SAC and adolescents in Leytesuggested that infection with S. japonicum mayalso have effects on intelligence.30 Hence,treatment of schistosomiasis is important toprevent the onset of severe clinical complicationsand could have positive effects on the nutritionalstatus and quality of life of children.31Control StrategiesThe WHA resolution 54.19 also targetedschistosomiasis and recommended praziquantel40-60 mg/kg to be given once a year, with addedemphasis on improvements in sanitation, accessto safe water, and behavioral changes.16,32 In thePhilippines, the DOH created the SchistosomiasisControl Program (SCP) according to AdministrativeOrder 2007-0015, with the goal of reducing theprevalence rate of schistosomiasis to less than 1%by 2010. In areas with prevalence greater than10%, the target drug coverage is at least 85%.Strategies of the SCP include mass administrationof praziquantel to exposed population, active casefinding and treatment of infected individuals,improvements in sanitation, environmentalmodification and snail control, health promotion,and health education.WHO RECOMMENDATIONS FOR CONTROL OFSTH INFECTIONS AND SCHISTOSOMIASISThe WHO strategy for the control of STHinfections and schistosomiasis includes schoolbased, teacher-assisted periodic MDA withoutprior screening of SAC. SAC have the highestDownloaded from www.pidsphil.orgprevalence and heavy intensity infection rates ofintestinal helminths among all age groups, makingthem the most vulnerable group and the mostsignificant contributors to the transmission of STHinfections and helminthiasis. The interventionstrategy is based on the principle of preventivechemotherapy (PC), with emphasis on theintegrated and coordinated use of available drugsrather than on specific forms of helminthiasis. Inareas endemic for STH infections, therecommended anthelminthics are albendazole ormebendazole. In areas endemic for STH andschistosomiasis, the recommended drugs arealbendazole or mebendazole with praziquantel.These anthelminthics possess broad-spectrumactivity and have the capability to address severalparasitic diseases simultaneously. The goal ofschool-based control programs is to offer periodicMDA to cover at least 75% of all SAC living inhighly endemic areas.32Safety Profile of AnthelminthicsThe key justification of MDA is safety ofanthelminthics.32 The adverse events related toanthelminthic drugs are rare and generally mildand transient when given in appropriate cdrugs,thebenzimidazoles(albendazole, mebendazole) in particular, are verysafe and there is no known harm in treatinguninfected individuals.13 The most commonadverse event that needs immediate interventionis allergic skin reaction, which could be treatedwith antihistamines.16 Heavily infected individualsare also more likely to experience allergicreactions due to degeneration of eradicatedworms.34 As such, the incidence of adverse drugreactions is highest during the first round oftreatment and decreases in subsequent doses.35Studies have also shown that majority of theadverse events of praziquantel are mild andtransient. In fact, the most common adverse eventof praziquantel is mild abdominal pain, whichrequires no treatment and could be prevented by

Page 7administration on a full stomach.16 In a doubleblind, randomized control trial on school childrenin Agusan del Sur, it was established that the 40mg/kg regimen of praziquantel had significantlyless incidence of adverse events, while having thesame effectivity, compared to the 60 mg/kgregimen.36 In addition, praziquantel can also besafely co-administered with either albendazole ormebendazole.37,38 Aside from administration ofchemotherapyforSTHinfectionsandschistosomiasis, school-based programs could alsooffer other interventions like health education,food and micronutrient supplementation, and coadministration of ivermectin for co-infection withfilariasis.39Cost-effectiveness of School-based, Teacherassisted Helminth Control ol programs are among the most costeffective public health interventions (Table 2).Involving teachers in MDA activities is logical,strategic, and advantageous since the existinginfrastructures used are schools and the targetpopulation are the SAC. Drug administration doesnot require complex skills because of their safetyprofile. Trained teachers and other non-medicalpersonnel should therefore be more than capableto ensure precautions and to identify andappropriately respond to adverse events.32 Thecost of treatment administration and programmonitoring is reduced to almost zero becausethere is no additional workload for teachers andschool administrators during MDA events.Teachers also generally outnumber the schoolparamedical and medical personnel, and theirassistance in drug administration and monitoringincreases the efficiency of the implementation ofschool-based MDA. Furthermore, teachers are inthe best strategi

optimizing school-based control interventions were formulated based on evidence and feasibility. Soil-Transmitted Helminth Infections STH infections refer to a group of parasitic diseases caused by nematodes of major concern to humans: the roundworm, Ascaris

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