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Review ArticleTHE NATIONAL MEDICAL JOURNAL OF INDIA VOL. 14, NO. 3,2001

Integrated programme for control of geohelminths:A perspective

SHANTHI ANANTHAKRISHNAN, P. K. DAS

ABSTRACTInfestation by geohelminths is an important public health prob-lem in developing countries like India. It is a major cause ofmorbidity in school-age children who have the highest burden ofworm infestation. Some of the morbid conditions attributed tointestinal helminthiasis are malnutrition, growth retardation,anaemia, vitamin A deficiency and impaired intellectual perfor-mance. Chemotherapy targeted at school-age children has beenrecommended as a cost-effective and feasible control programmefor the control of geohelminths. To optimize resources ageohelminth control programme can be integrated with otherexisting national health programmes. The availability of drugssuch as diethyl carbamazine (DEC) and albendazole, which haveanthelminthic and antifilarial properties, opens the possibility ofintegrating a geohelminth control programme with a filariacontrol programme. However, co-administration of DEC andalbendazole raises several issues of frequency of administration,efficacy, compliance and cost-effectiveness. Thus, integrating ageohelminth control programme with the existing mid-day mealor anaemia prophylaxis programme would be a more appropri-ate and cost-effective strategy to control geohelminths, alleviatethe morbidity caused by them and improve the overall health ofthe community.Natl Med J India 2001; 14: 148-53

INTRODUCTIONThe geohelminths-roundworm, hookworm and whipworm-are among the 10 most common infections in the world and areendemic in many developing countries. 1,2 The highest intensity ofworm infestation occurs in school-age children and is one of theleading causes of morbidity, accounting for 12,3% and 11.4% ofdisability adjusted life-years (DALYs) lost due to all causes ingirls and boys, respectively.' The disease conditions generallyattributed to geohelminths are malnutrition, anaemia, vitamin Adeficiency and impaired cognition+? The high prevalence ofmalnutrition among children in India, despite the existence ofnational nutritional programmes such as the mid-day meal andanaemia prophylaxis programmes is, perhaps, to some extent dueto the heavy infestation of geohelminths in them, A geohelminth

Vector Control Research Center (Indian Council of Medical Research),Medical Complex, Indira Nagar, Pondicherry, 605006, India

SHANTHI ANANTHAKRlSHNAN, P. K. DAS

Correspondence to SHANTHIANANTHAKRlSHNAN;mosquito@md5. vsnl.net. in

© The National Medical Journal of India 2001

control programme could help in improving their nutritionalstatus.

However, constraints of available resources and the increasingnumber of public health problems in developing countries createthe need for integrating several control programmes. India ac-counts for almost 40% of the total global burden of people withlymphatic filariasis" and geohelminths are an important publichealth problem." The availability of broad spectrum and highlyefficacious anthelminthics such as albendazole, which also havesome antifilarial action, has opened up the possibility of integrat-ing anthelminthic and antifilarial control measures in areas en-demic for filariasis.'? Helminth control measures might also beintegrated with existing nutritional programmes since malnutri-tion, anaemia and helminthiasis are observed to be importanthealth problems in school-age children in India, 11-14 The implica-tions of having such integrated control programmes for geo-helminths at a national level are discussed in this article,

PROBLEM AND CONTROL OF GEOHELMINTHSThe morbidity caused by geohelminths include malnutrition,growth retardation, vitamin A deficiency, anaemia, etc ,4-7 and canbe alleviated through effective control measures. These measuresare particularly recommended in communities with a high preva-lence of protein-energy malnutrition." Of the three measuresneeded for effective control of geohelminthic infections-goodenvironmental sanitation, health education and chemotherapy-improving environmental sanitation and health education arepreventive and have a long term impact. Good environmentalsanitation and a high standard of living have resulted in a reduc-tion in the prevalence of intestinal parasites in developed coun-tries. 16 However, the community does not perceive the benefitsimmediately, On the other hand, chemotherapy reduces the inten-sity of infection and quickly alleviates morbidity, The beneficialeffects, though short-lived, are well perceived by the communityin the form of expulsion of worms and/or improved appetite,growth, etc. These perceived benefits make chemotherapy the firstchoice in controlling geohelminths at the community level. How-ever, the best results are obtained when chemotherapy is accom-panied by improved environmental sanitation and health educa-tion,

ANTHELMINTHIC DRUGSLevamisole, pyrantel pamoate, albendazole and mebendazole aresome of the widely used anthelminthics. The benzimidazole deri-vatives, albendazole and mebendazole, are more effective thaneither levarnisole orpyrantel pamoate against hookworm and whip-worm." While albendazole is highly effective against roundworm

ANANTHAKRISHNAN, DAS : CONTROL OF GEOHELMINTHS

and hookworm, it is not very effective against whipworm.P-"Mebendazole, on the other hand, ismore effective than albendazoleagainst whipworm but has only limited efficacy against hook-worm.21.24Therefore, the drug of choice for control of helminths inan area depends on the prevalent species.

MODALITIES OF TREATMENTChemotherapy could be selective, mass or targeted. Selectivechemotherapy is time-consuming, expensive and may not befeasible at the community level. Mass chemotherapy of the entirecommunity may not be cost-effective. Since a higher prevalenceand burden of worm infestation is seen among the school-agegroup, treatment of this age group alone is expected to reducetransmission and thereby prevalence in the entire community."Therefore, targeted chemotherapy of school-age children is rec-ommended as the most appropriate cost-effective strategy inreducing worm infestation in the community.'? Repeated treat-ment may ensure that despite re-infection, the infestation is keptbelow the level at which it causes morbidity."

RE-INFECTION FOLLOWING CHEMOTHERAPYFollowing a single dose of chemotherapy, re-infection occurswithin 6-12 months, with the re-infection prevalence and/orintensity reaching almost pretreatment levels.21.23-27While someinvestigators have observed a significant reduction in the preva-lence and/or intensity of worm infestation when deworrning wasrepeated once in 6 months over a 1-2-year period,18.28-JOothershave found it to be effective only when repeated once in 3-4months. 31.32A study from China reported that after giving albenda-zole twice a year for 2 years (between 1986 and 1988; 4 cycles),the prevalence of roundworm, hookworm and whipworm infesta-tion was significantly lower than the pretreatment levels andpersisted for over 8 years after completing chemotherapy. 30Inorder to be effective, deworrning may have to be repeated at leastonce in 6 months for 1-2 years. Some studies have shown that inareas where the initial prevalence is very high, the worm infesta-tion might be reduced though there may not be any significant fallin the prevalence.18,23,28,32,33In a control programme it is moreimportant to monitor the burden of worm infestation than theprevalence. 34

IMPACT OF CHEMOTHERAPY ON NUTRITIONALSTATUS, HAEMOGLOBIN LEVELS AND COGNITIONApart from a reduction in the worm burden and prevalence,several investigators observed an improvement in the nutritionalstatus, haemoglobin levels and cognition of children after singleor multiple doses of chemotherapy. Based on the frequency ofintervention, these children were evaluated 6 months or 1-2 yearsafter intervention. The reported nutritional benefits were an in-crease in weight (0.1-1.3 kg), height (0.1--0.6 em) and mid-armcircumference (0.2-3 cm).18,24,35-48In a study on preschool childrenin Lucknow, treatment with albendazole was found to reduce therisk of stunted growth although there was no difference in theoverall morbidity or cognition between the treated and untreatedgroups." Following repeated deworming once in 3-6 months, arise in haemoglobin levels (0.1-2 g/dl) has been observed after 1year by some investigators.30,31.4I,50,51While Curtale et al.52ob-served an increase in serum vitamin A levels following deworm-ing, a slight improvement in cognition has also been observed bysome.45,48,53Objective testing of cognition in these studies involvedperforming a battery of tests for measuring the attention span,short- and long-term memory and the learning process. The

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improvement was observed only in a few of the parameters tested.Objective testing for cognition in children is not a simple task andthe performance may be influenced by a number of factors. Asingle performance may not accurately evaluate the cognitivepowers and one has to be guarded in interpreting the results of suchtests. The prevalence of worm infestation ranged from 29% tomore than 95% in these studies and the beneficial effects wereseen mainly in malnourished children.

On the other hand, some investigators have not found anysignificant improvement in the nutritional status or cognitionfollowing chemotherapy, despite a reduction in the intensity ofworm infestation and prevalence.22,45,54-57Some of these stud-ies22,55,56were carried out in Guatemala, Malaysia and Bangladeshwhere the prevalence of worm infestation is high (26%-91 %).Hadidjaja et al.54observed that despite a high prevalence of worminfestation (44.5%), more than 80% of the children in the studywere well nourished. They also observed an improvement inconcentration and eye-hand coordination in the group of childrenwho were given only mebendazole but not in those who hadreceived mebendazole as well as health education. Other investi-gators also have not noticed any significant improvement incognition after deworming in well-nourished children.v-" Beachet al.58studied the effect of combined ivermectin and albendazoleon intestinal helminths and filariasis. They found that while theprevalence and intensity of worm infestation was reduced therewas significant nutritional benefit only on stratification. Childrenwho had only roundworms showed a height gain of 0.6 em, whilethose who had only whipworms had a weight gain of 0.5 kg aftertreatment.

While there is unanimity on the efficacy of targeted chemo-therapy of schoolchildren in reducing the worm burden and/orprevalence, there is no agreement regarding its impact on thenutritional and haemoglobin status or intellectual function oftreated children. Therefore, the benefits and cost-effectiveness ofdeworming school-age children, particularly in areas of lowprevalence, is doubtful.

COST-EFFECTIVENESS AND LIMITATIONS OFSCHOOL-BASED CHEMOTHERAPYThe World Health Organization recommends that mass treatmentis warranted where the prevalence of worm infection is more than50%, At this level of prevalence, the estimated cost per infectedchild treated with school-based delivery of albendazole isUS$ 0.46.If the prevalence is about 25%, the cost per infected child treatedwould still be less than US$ 1.59In India, the prevalence ofintestinal parasites varies from 12.5% in some parts of UttarPradesh to 89.6% in some areas of Chandigarh.w" In a cross-sectional survey across the country the prevalence of roundwormswas observed to be 16.35%, hookworms 7% and whipworms3.7%.62The variation in the prevalence of different species ofgeohelminths in India is shown in Tables I and IJ.34,60,61,63-80Thus,it may not be cost-effective to have a school-based chemothera-peutic control measure allover the country. The other disadvan-tage of a school-based delivery system would be that it would misschildren who are not enrolled or who are absent. Although Raj etal." did not find significant school absenteeism in children withintestinal helminthiasis, a study from Egypt found that more than80% of girls infected with Schistosoma mansoni were not treatedbecause they did not attend school. 82Olsen=observed that, of thetotal population, a school-based programme would treat onlybetween 31% and 50% of infected persons leaving out adults, andpreschool and school-age children who were not enrolled. It might

150

Place

TABLE1. Prevalence of geohelminths in different parts of India

Numbersurveyed

Overall Round- Hook- Whip-prevalence" worm worm worm

Ambala=t 586 32.7Andaman and Nicobar" 204 79.2Andaman andNicobar" 29 82.7Andhra Pradesh65:j: 711 77.4ArunachaIPradesh~:j: 893 75.0

Chandigarh"] 976 12.5Darjeeling-'f 215 33.5Delhi68t 200 35.0Delhi69t 750 62.0

C 60.0Gujarat'"] 106 70.8Gujarar'P] 62 66.1Gujarat"f 505 20.6Kamataka'tr 1020 76.5Maharashtra'tr 817 34.6

C 28.6Orissa" 276 34.5t

19.9:j:Pondicherry=t na naPondicherry75:j: na naRajasthan'tr 305 32.5Rajasthan'ir na 62.3Tamil Nadu+t 224 naVaranasi:j: 249 89.6

C 87.6

12.746.234.53.0

45.0C 57.1A 34.8

8.334.89.0

14.3C 18.9

7.522.60.8

48.31.2

1.810.11.00.9

85.034.1

C42.4

8.421.020.627.140.9

C 31.9A 48.4

10.38.33.57.6

C4.70.91.60.2

46.82.3

na21.048.21.8

45.0

na19.4na0.9

CO.9o1.60.8

42.80.24

7.2 0.7 5.1

0.2 2.84.8 5.4

11.1 na0 na

32.0 95.024.9 na

"includes prevalence of all intestinal parasites such as Entamoeba histolytica, Giardia,etc. turban * rural C children A adults na not available

TABLEII. Prevalence of geohelminths in preschool children indifferent parts of India

Place Number Overall Round- Hook- Whip-surveyed prevalence* worm worm worm

De1hF8tWestBengal'ttAndaman and Nicobar"Udaipur=t

249321125

1022

50.644.34445.5

9.68.1

22.710.8

2.71.8

31.80.3

1.40.9

500.5

"includes prevalence of all intestinal parasites such as Entamoeba histolytica,Giardia, etc. turban * rural

also leave out older adolescents in whom hookworm is moreprevalent.

INTEGRATION OF A GEOHELMINTH CONTROLPROGRAMME WITH OTHER NATIONAL PROGRAMMES

Integration with filariasis control programmeIn India, filariasis is another nematode infection recognized as animportant cause of morbidity in adults as well as children.t'-" It isimportant to treat people during the initial stages of infection toprevent permanent damage to the lymphatic and renal system.India is a signatory to a resolution passed by the World HealthAssembly for eliminating filariasis." Success has been achievedin controlling this helminth by repeated community-based chemo-therapy." Consequently, as one of the elimination strategies,intense efforts are on to reduce the transmission of filariasis bymass treatment with diethyl carbamazine (DEC), a known effec-

THE NATIONALMEDICAL JOURNAL OF INDIA VOL. 14, No.3, 2001

tive antifilarial drug given alone or in combination with albendazoleor ivermectin, which have also been shown to have antifilarialaction. Administering a combination of albendazole with eitherDEC or ivermectin has been found to produce a rapid andsustained decrease in the prevalence of microfilaraemia. 58. 88, 89

Hence, it has been suggested as an important chemotherapeuticoption for reducing the transmission of filariasis. IO This combina-tion is also presumed to have the added potential of controlling andalleviating the morbidity caused by intestinal helminthiasis. It isexpected that these added benefits, perceived in the form of wormexpulsion, improved growth and health in children might enhancethe compliance rate within the community, and hence is advocatedas an important control strategy in some endemic areas. However,the administration of both the drugs together raises several issues.

Efficacy. With respect to filariasis, the efficacy of DEC aloneis comparable to that of a combination of albendazole and DEC(personal communication,VCRC). Studies have shown the super-ior efficacy of albendazole and DEC or albendazole and ivermectinas compared to albendazole alone in treating filariasis. However,the added efficacy of the combined regimen compared with theconventional single dose of albendazole in treating roundwormand hookworm infections has not been studied. Some studies haveshown that albendazole in combination with ivermectin was moreeffective against whipworm than when given alone.58•89 In areaswhere the prevalence of filariasis and whipworm are high, thiscombination might be considered. The nutritional benefits ofanthelminthic treatment were also found to be more significantwith the combination therapy than with a single drug." Theindividual efficacy of albendazole, ivermectin and DEC againsthelminths is given in Table 111.90•91

Frequency. The treatment frequency of the drug combinationhas to be optimized. While an annual single dose of albendazoleand DEC or ivermectin for 4-6 years is recommended for thecontrol of filariasis,'? studies have shown that the optimum fre-quency of single-dose chemotherapy for the control of geohelrninthsmay be 6-monthly for 2 years.28,30 Therefore, if combinationtherapy has to have an impact in controlling geohelminths, anannual single dose may not be ideal and it may have to be given atleast once in 6 months. In a study from Bangladesh, Taylor et al."comparing 4 different regimens (mass chemotherapy, mass che-motherapy with health education, mass chemotherapy followedby targeted chemotherapy of children every 6 months, and masschemotherapy with targeted chemotherapy of children along withhealth education) for control of geohelminths observed masschemotherapy with albendazole given at an interval of 18 monthsto be the most cost-effective regimen. Further studies are requiredto evaluate the efficacy and cost -effectiveness ofthe annual single-dose combination drug regimen in controlling geohelminths.

Cost-effectiveness. For control of geohelminths the most cost-

TABLEIII. Comparison of the efficacy of albendazole, diethyl-carbamazine and ivermectin against geohelminths andWuchereria bancrofti="

Helminth Albendazole Diethylcarbamazine Ivermectin

Roundworm +++ + +++Hookworm +++Whipworm ++ +Wuchereria bancrofti +++ +++ +++- not effective or not given + weakly effective ++ moderately effecti ve+++highly effective

ANANTHAKRISHNAN, DAS : CONTROL OF GEOHELMINTHS

effective strategy is targeted chemotherapy of school-age childrensince they harbour the highest worm burden.'? This needs anassessment of the feasibility and cost-effectiveness of school-based delivery of drugs. On the other hand, the prevalence offilarial infection increases with age and higher prevalence ratesare found beyond the school-age group.85,93Therefore, targetedchemotherapy of school-age children alone may not be effectivefor filariasis and treatment may have to be targeted at the commu-nity. Thus, from a school-based targeted chemotherapy of chil-dren, the control option will become community-based masschemotherapy for filariasis and geohelminths. While school-based targeted chemotherapy is cost -effective if the prevalence ofgeohelminths is >25%, for community-based mass chemotherapyto be cost-effective the prevalence has to be >50%.59Althoughthere are a number of studies on the prevalence rates of filariasisand geohelminths in different parts of India,63-80.93there are littledata on the co-existence of these two infections in endemic areas.This information is essential for stratifying geographic areas andage groups according to different levels of prevalence and co-existence of these two infections. Mass chemotherapy with DECand albendazole may be implemented in those areas and/or agegroups' with a high prevalence of filariasis and geohelminths.Even then, the added nutritional impact and the cost-effectivenesswill have to be evaluated.

Compliance. Since combination treatment involves takingseveral tablets orally, compliance may be a problem. However, asthe need to take medicines is only once a year, with healtheducation and motivation this can perhaps be overcome. Theperceived benefit of deworming might also improve compliance.Direct observation of treatment, as is being advocated for tubercu-losis and leprosy, may also be tried.

These issues have to be resolved before integrating the anthel-minthic programme with the filariasis control programme.

INTEGRATION WITH EXISTING NUTRITIONALPROGRAMMESDespite a mid-day meal and anaemia prophylaxis programme toprovide supplementary calories, protein and iron, respectively,"anaemia and malnutrition continue to be important health prob-lems in schoolchildren.l'':" Some investigators have observed anutritional benefit only when deworming of schoolchildren wascombined with nutritional supplementation. 35.50The overall nutri-tional, health and intellectual status of schoolchildren may beimproved by a combination of deworming, and macro- and micro-nutrient supplementation. This might also prove to be cost-effective. It has been reported that even after consuming mid-daymeals, schoolchildren had a 45% energy deficit." Despite thisdeficit, it is possible that growth,might improve if anthelminthicmeasures are combined with the mid-day meal and/or anaemiaprophylaxis programmes. -

CONCLUSIONInfestation by geohelminths is an important health problem inmany parts ofIndia. However, it may not be appropriate to have auniform school-based geohelminth control programme. The widevariation in the prevalence of different species of geohelminths inIndia makes it imperative to obtain further epidemiological detailsat the national level. The anthelminthic drugs used in the controlprogramme have to be effective against the prevalent local speciesof geohelminths. The positive impact of dewormingper se on thephysical and intellectual development of school-age children isdoubtful and needs to be evaluated further, taking into consider-

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ation children with different grades of malnutrition and from areaswith different levels of endemicity of geohelminths. Integrating ageohelrninth control programme with a filariasis control programmeraises several unresolved issues such as efficacy of the drugcombination against geohelminths, frequency of administration,cost-effectiveness and compliance. For control of geohelminthsand alleviating the morbidity caused by them, the most appropri-ate strategy would be to integrate the geohelminth controlprogramme with the existing mid-day meal or the anaemia pro-phylaxis programmes. This would optimize health resources inimproving the overall health of the community in general andschool-age children in particular.

REFERENCESI World Health Organization. The World Health Report. Geneva:WHO, 1998:39-60.2 WHO Expert Committee. Public health significance of intestinal parasitic infections.

Bull World Health Organ 1987;65:575-88.3 World Bank. The global burden of disease. Appendix B. In: World development

report: Investing in health-world development indicators. New York: World Bankand Oxford University Press, 1993:213-25.

4 Tripathy K, Gonzalez F, Lotero H, Bolanos O. Effects of Ascaris infection on humannutrition. Am } Trap Med Hyg 1971 ;20:212-18.

5 Gupta MC, Basu AK, Tandon BN. Gastrointestinal protein loss in hookworm androundworm infections. Am} Trap Clin Nutr 1974;27: 1386-9.

6 Sivakumar B, Reddy V. Absorption of vitamin A in children with ascariasis.U TrapMedHyg 1975;78:114-15.

7 Crompton DWT. Nutritional aspects of infection. Trans R Sac Trap Med Hyg1986;80:697-705.

8 MichaelE, Bundy DAP, Grenfell BT. Re-assessingthe global prevalence and distributionoflymphatic filariasis. Parasitology 1996;112:409-28.

9 Kang G, Mathew MS, Rajan DP, Daniel 10, Mathan MM, Mathan VI, et al.Prevalence of intestinal parasites in rural Southern Indians. Trap Med lnt Health1999;3:70-5.

10 Ottesen EA, Ismail MM, HortonJ. The role of albendazole in programmes to eliminatelymphatic filariasis. Parasitol Today 1999;15:382-6.

II Tragler AT. A study of primary school health in Bombay. Indian Pediatr 1981 ;18:551-6.

12 Ananthakrishnan S, Ramachandran V, Bansal RD. Health status and scholasticperformance of school children. Indian } Prev Social Med 1987;18:27-31.

13 Gupta PK. Health status of rural school children. Indian Pediatr 1989;26:581-4.14 Bhattacharya R, Tandon J. A study of preventable morbidity among primary school

children of Varanasi. Indian} Prev Social Med 1992;23: 16-21.15 Stephenson L. Positive aspects of intervention: Improving the quality of life for

children. Proceedings of a workshop on intestinal parasites: A priority for primaryhealth care. NewYork:Cornell University, 1991: 14-20.

16 Report of WHO expert committee. Prevention and control of intestinal parasiticinfections. World Health Organ Tech Rep Ser 1987;749: 1-86.

17 Hall A. Intestinal nematode infections in children: Their importance and a strategy fortheir control. Postgrad Doc Caribbean 1998;14:147-51.

18 Stephenson LS, Latham MC, Adams EJ, Kinoti SN, PertetA. Weight gain of Kenyanschool children infected with hook worm, Trichuris trichiura ;mdAscaris lumbricoidesis improved following once or twice yearly treatment with albendazole. } Nutr1993;123:656-65.

19 Albonico M, Renganathan E, Bosman A, Kisumku UM, Alawi KS, Savioli L. Efficacyof a single dose of mebendazole on prevalence and intensity of soil-transmittednematodes in Zanzibar. Trap Geogr Med 1994;46: 142-6.

20 Hall A, NaharQ. Albendazole and infections with Ascaris lumbricoides and Trichuristrichiura in children in Bangladesh. Trans R Sac Trap Med Hyg 1994;88:110-12.

21 Albonico M, Smith PG, Ercole E, Hall A, Chwaya HM, Alawi KS, et al. Rate ofreinfection with intestinal nematodes after treatment of children with mebendazole oralbendazole in a highly endemic area. Trans R Sac Trap Med Hyg 1995;89:538-41.

22 Watkins WE, Cruz JR, Pollit E. The effects of deworming on indicators of schoolperformance in Guatemala. Trans R Sac Trap Med Hyg 1996;90:156-61.

23 Paul I, Gnanamani G. Re-infection estimation of soil-transmitted helminths amongslum schoolchildren in Vishakapatnam, Andhra Pradesh. } Commun Dis 1998;30:245-9.

24 Watkins WE, Pollitt E. Effect of removing Ascaris on the growth of Guatemalanschoolchildren. Pediatrics 1996;97:871-6.

25 Savioli L, Bundy DAP, Tomkins A. Intestinal parasitic infections: A soluble publichealth problem. Trans R Sac Trap Med Hyg 1992;86:353-4.

26 AlbonicoM, Savioli L.lntestinalparasitic infections. CTDIMIPIWP/93.7. Geneva:Division of communicable diseases, World Health Organization, 1993: 1-6.

27 Kightlinger LK, SeedJR, Kightlinger MB. Tbeepidemiology of Ascaris lumbricoides,Trichuris trichiura and hook worm in children in the Ranomafana rain forest,Madagascar. } Parasitol1995 ;81: 159-69.

28 Curtale F. Selective treatment and targeted chemotherapy: Effect on prevalence and

152

intensity of infection for two intestinal helminths in Nepalese children. PanminervaMed 1995;37:214--19.

29 Magnussen P, Muchiri E, Mungai P, Ndzovu M, Ouma J, Tosha S. A school basedapproach to the control of urinary schistosomiasis and intestinal helminth infections inchildren in Matuga, Kenya. Impact of a two-year chemotherapy programme on theprevalence and intensity of infections. Trop Med Int Health 1997;2:825-31.

30 Yong WL, Zhaohua X, Ying YS, Long SY, Ping RS, Changcun S. A ten-yearlongitudinal observation on the control of hookworm and other soil-transmittednematodiasis in the study site. Chinese} Parasitic Dis Control 1998;11:165-7.

31 Anjaneyulu G, Nagaiah G. Periodic deworming with pyrantel in an industrialisedtownship. Indian } Public Health 1989;33:5-7.

32 Holland CV, Asaolu SO, Crompton DW, Whitehead RR, Coombs l. Targetedanthelminthic treatment of school children: Effect of frequency of application on theintensity of Ascaris lumbricoides infection in children from rural Nigerian villages.Parasitology 1996;113:87-95.

33 Machado MT, Machodo TM, Yoshikae RM, Schmidt AL, Faria de C, PaschoalottiMA, et al. Ascariasis in the subdistrict of Cavacos municipality of Alterosa (mg),Brazil: Effectofmass treatment with albendazole on the intensity of infection. Rev InstMed Trop Sao Paulo 1996;38:265-71.

34 Elkins DB, Haswell-Elkins M, Anderson RM. TIle epidemiology and control ofintestinal helminths in the Pulicat lake region of Southern India I. Study design andpre- and post-treatment observations onAscaris lumbricoides infection. Trans R SocTrop Med Hyg 1986;80:774--92.

35 Gupta MC, Arora KL, Mithal S, Tandon BN. Effect of periodic deworming onnutritional status of Ascaris-infected pre-school children receiving supplementaryfood. Lancet 1977;2:108-10.

36 Hagel I, Lynch NR, DiPrisco MC, Perez M, Sanchez JE, Pereyra BN, et al. Helminthinfection and anthropometric indicators in children from a tropical slum-Ascaris re-infection after anthelminthic treatment.J Trop Pediatr 1999;45:215-20.

37 Hadju V, Stephenson LS, Abadi K, Mohammed HO, Bowman DD, Parker RS.Improvements in appetite and growth in helminth-infected school boys three and sevenweeks after a single dose ofpyrantel pamoate. Parasitology 1996;113:497-504.

38 Adams EJ, Stephenson LS, Latham MC, Kinoti SN. Physical activity and growth ofKenyan school children with hook worm, Trichuris trichiura andAscaris lumbricoidesinfections are improved after treatment with albendazole.J Nutr 1994;124: 1199-206.

39 Stephenson LS, Latham MC, Kurz KM, Kinoti SN, Brigham S. Treatment with a singledose of albendazole improves growth of Kenyan schoolchildren with hook worm,Trichuris trichiura and Ascaris lumbricoides infections. Am } Trop Med Hyg1989;41:78-87.

40 Stoltzfus RJ, Albonico M, TielschJM, ChwayaHM, Savioli L. School-baseddewormingprogram yields small improvement in growth of Zanzibari school children after oneyear.} Nutr 1997;127:2187-93.

41 StoltzfusRJ, AlbonicoM, ChwayaHM, TielschJM, Schulze KJ, Savioli L. Effects ofthe Zanzibar school-based deworming program on iron status of children. Am J ClinNutrl998;68: 179-86.

42 Stephenson LS, Latham MC, Adams EJ, Kinoti SN, Pertet A. Physical fitness, growthand appetite of Kenyan school boys with hookworm, Trichuris trichiura, and Ascarislumbricoides infections are improved 4 months after a single dose of albendazole. }Nutr 1993;123: 1036--46.

43 Forrester JE, Bailar JC, Esrey SA,Jose MV, CastillejosBT, Ocampo G. Randomisedtrial of albendazole and pyrantel pamoate in symptomless trichuriasis in children.Lancet 1998;352: 1103-8.

44 Koroma MM, Williams RA, de la Haye RR, Hodges M. Effects of albendazole ongrowth of primary school children and the prevalence and intensity of soil transmittedhelminths in Sierra Leone. J Trop Pediatr 1996;42:371-2.

45 Ananthakrishnan S, Das PK, Simeon DT, Grantham McGregor SM, Wong MS.Trichuris trichiura infection and cognition in children. Results of a randomisedclinical trial. Parasitology 1995;110:457-64.

46 Simeon DT, Grantham McGregor SM, Callender JE, Wong MS. Treatment ofTrichuris trichiurainfections improves growth, spelling scores and school attendancein some children.Z Nutr 1995;125:1875-83.

47 Pamba HO, Bwibo NO, Chunge CN, Estambale BB. A study ofthe efficacy and safetyof albendazole (Zen tel) in the treatment of intestinal helminthiasis in Kenyan childrenless than two years of age. East Afr Med J 1989;66: 197-202.

48 Callender JE, Walker SP, Grantham McGregor SM, Cooper ES. Growth anddevelopment four years after treatment for the Trichuris dysentery syndrome. ActaPediatr 1998;87:1247-9.

49 Awasthi S, Pande VK, Fletcher RH. Effectiveness and cost-effectiveness of albendazolein improving nutritional status of pre-school children in urban slums. Indian Pediatr2000;37: 19-29.

50 Gopaldas T. More nutrients, fewer parasites and better learning. World Health Forum1996;17:367-8.

51 Mohapatra SC, Gaur SD. Effect of periodic deworming on haemoglobin level of a ruralcommunity in Varanasi.lndian} Prev Soc Med 1996;27: 17-22.

52 Curtale F, Vaidya Y, Muhilal, Tilden RT. Ascaris and hookworm infection and serumretinol amongst children in Nepal. Panminerva Med 1994;36: 19-21.

53 Nokes C, Gratham McGregor SM, Sawyer AV, Cooper ES, Bundy DAP. Parasitichelminthic infection and cognitive function in school children. Proc R Soc Land Bioi1992;247:77-81.

54 HadidjajaP, Bonang E, Suyardi MA, Abidin SA, Ismid IS, Margogno SS. The effect

THE NATIONAL MEDICAL JOURNAL OF INDIA VOL. 14, No.3, 2001

of intervention methods on nutritional status and cognitive function of primary schoolchildren infected .with Ascaris lumbricoides. Am J Trop Med Hyg 1998;59:791-5.

55 Mascie Taylor MC, Rousham EK. An 18-month study of the effect of periodicanthelminthic treatment on the growth and nutritional status of pre-school children inBangladesh. Ann Hum Bioi 1994;21 :315-24.

56 Lai KP, Kaur H, Mathias RG, Owyang CK. Ascaris and Trichuris do not contribute togrowth retardation in primary school children. South East} Trop Med Pub Health1995;26:322-8.

57 Gardner JM, Grantham McGregor SM, Baddeley A. Trichuris trichiura infection andcognitive function in Jamaican school children. Ann Trop Med ParasitoI1996;90:55-63.

58 Beach MJ, Streit TG, Addiss DG, Prospere R, Roberts JM, Lammie PJ. Assessmentof combined ivermectin and albendazole for treatment of intestinal helminth andWuchereria bancrofti infections in Haitian school children. Am } Trop Med Hyg1999;60:479-86.

59 Guyatt HL. Mass chemotherapy and school-based anthelminthic delivery. Trans R SocTropMedHyg 1999;93:12-13.

60 Agarwal DK, Dutta A, Arora RR, Nair MRV. Prevalence of intestinal parasites in arural community in Varanasi, Uttar Pradesh.J Commun Dis 1977;9:69-70.

61 Ramesh GN, Malla N, Raju GS, Sehgal R, Ganguly NK, Mahajan RC, et al.Epidemiological study of parasitic infestations in lower socio-economic group inChandigarh (North India). Indian} Med Res 1991 ;93A:47-50.

62 Gadgil SD, Kulkarni SS, Apte VV, Nanivadekar AS. Intestinal nematode infections inIndia: A cross-sectional survey.J Postgrad Med 1984;30: 137--43.

63 Singh J, Chib SK. Prevalence of intestinal parasites and hemoglobin level in schoolchildren in Ambala Cantt. JCommun Dis 1978;10:218-25.

64 Kalra NL, Mathur KK. Intestinal parasites among tribals of Andaman and Nicobarislands} Commun Dis 1982;14:16-25.

65 Das NC, Apparao MC, Venkatasubbaiah N, Rao CK. Prevalenceof'intestinal parasitesin rural population of West Godavari district, Andhra Pradesh. J Commun Dis1981 ;13: 165-71.

66 Paul RC, Das NC, John VM, Rao CK. Prevalence ofintestinal parasitic infections inselected rural population of Arunachal Pradesh.J Commun Dis 1982;14:309-12.

67 Saha SS, Behl JP, Sharma JK, Kumar A. Distribution of intestinal parasitic infectionin rural area of district Darjeeling, West Bengal.} Commun Dis 1993;25:43--4.

68 Arya SC. Intestinal parasite in a higher socioeconomic community. } Commun Dis1982;14: 152-3.

69 Biswas H, Sehgal S, Arora RR, Mathur KK. Intestinal parasites and different speciesof hookworm in slum dwelling people around Delhi. J Commun Dis 1978;10:234--7.

70 Das NC, Russel S, Trivedi GK, Joshi UK, RaoCK. Prevalence of intestinal parasitesin Jamnagar and Okha towns-Gujarat.} Commun Dis 1981 ;13:67-70.

71 Raina VK, Mohanty B, Kumar A. Prevalence ofintestinal parasitic infection amongsturban population in district Val sad, Gujarat state. J Commun Dis 1989;21 :245-7.

72 SubbhannayyaK, Babu MH, Kumar A, Rao TS, ShivanandaPG. Entamoebahistolyticaand other parasitic infections in south Kanara district, Karnataka. J Commun Dis1989;21:207-13.

73 Nagoba BS, Basutkar SH, BhatSD. Status ofintestinal parasitic infections in Loni-a rural area of Ahmednagar district of Maharashtra.Z Commun Dis 1992;24:58-9.

74 Saha SS, Behl JP, SharmaJK, Kumar A. Distribution of intestinal parasitic infectionsin selected areas of District Puri, Orissa. J Commun Dis 1993;25:86-7.

75 Reddy GS, Venkatesvarlou N. A comprehensive epidemiological study of intestinalprotozoan and helminthic infection in Pondicherry.ICMR Report. New Delhi:IndianCouncil of Medical Research, 1992.

76 Paul RC, Das NC, Rao CK, Joshi M, Mathur AB. Prevalence of intestinal parasites in3 villages ofDungarpurdistrict, Rajasthan.} CommunDis 1982;14: 149-51.

77 SharmaRS, Mahadik VJ. Prevalence of intestinal parasites in a rural area of Rajasthan.LCommun Dis 1988;20:312-15.

78 BanikND. Intestinal parasitic infections in pre-school children in lower socioeconomiccommunity in Delhi. } Commun Dis 1981 ;13:92-5.

79 Saha DR, Gupta DN, Sengupta PG, Mondal SK, Ghosh S, Saha NC, et al. Intestinalparasitism: A childhood problem in rural Bengal. } Commun Dis 1995 ;27: 170--4.

80 Bhandari B, Gupta GP, Mandowara SL. Prevalence of intestinal parasites in Udaipur.Indian} Pediatr 1985;52:299-302.

81 Raj SM, Sein KT, Anuar AK, MustaffaBE. Effect of intestinal helminthiasis on schoolattendance by early primary school children. Trans R Soc Trop Med Hyg 1997;91:131-2.

82 Husein MH, TalaatM, EI-SayedMK, EI- Badawi A, Evans DB. Who misses out withschool-based health programs? A study of schistomiasis control in Egypt. Trans R SocTrop Med Hyg 1996;90:362-5.

83 Olsen A. The proportion of helminth infections in a community in western Kenyawhich would be treated by mass chemotherapy of schoolchildren. Trans R Soc TropMedHyg 1998;92:144--8.

84 Lammie PJ, Hightower AW, Eberhard ML. Age-specific prevalence of antigenemia ina Wuchereria bancrofti exposed population. Am} Trop Med Hyg 1994;5:348-55.

85 Simonsen PE, Lemnge MM, Msangeni HA, Jakobsen PH, Bygbjerg IC. Bancroftianfilariasis: The patterns of filarial-specific immunoglobulin GI (IgGI) IgG4 andcirculating antigens in endemic community of northeastern Tanzania. Am} Trop MedHyg 1996;55:69-75.

86 World Health Organization. WHO Division of Tropical Diseases. Progress Report

ANANTHAKRISHNAN, DAS CONTROL OF GEOHELMINTHS

1997. Geneva:WHO, 1997.87 BundyDAP. This wormy world-Then and now. Parasitol Today 1997;13:407-8.88 Ismail MM, Jayakody RL, Weil GJ,NinnalanN, JayasingheKS,Abeyewickrema W,

et al. Efficacy of single dose combination of albendazole, ivermectin and diethylcarbamazine for the treatment of bancroftian filariasis. Trans R Soc Trop Med Hyg1998;92:4-7.

89 Ismail MM, Jayakody RL. Efficacy of a1bendazole and its combinations with ivermectinordiethyl carbamazine (DEC) in the treatment of Trichuris trichuria infections in SriLanka. Ann Trop Med Parasitol 1999;93:501-4.

90 Hall A. Antihelminthics:drugs for treating worms. Africa Health. Sep 1998:4--6.91 de SilvaN, Guyatt H, Bundy D. Anthelminthics. A comparative review of their clinical

pharmacology. Drugs 1997;53:769-88.

92 Mascie Taylor CG, Alam M, Montanari RM, Karim R, Ahmed T, Karim E, et al. Astudy of the cost-effectiveness of selective health interventions for the control ofintestinal parasites in rural Bangladesh. J Parasitol 1999;85:6--1 I.

93 Pani SP, BalakrishnanN, Srividya A, Bundy DAP, Grenfell BT. Clinical epidemiologyof Bancroftian filariasis: Effect of age and gender. Trans R Soc Trop Med Hyg1991;85:260-4.

94 Park K. Health care ofthe community In: Park K, Park J. Text book of preventive andsocial medicine. Jabalpur:Banarsidas Bhanot, 1995: 513-31.

95 Laxmaiah A, Sarma KVR, Rao DH, Reddy CG, Ravindranath M, Rao MV, et al.Impact of mid-day meal program on educational and nutritional status of schoolchildren in Kamataka.1ndian Pediatr 1999;36: 1221-8.

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