ORIGINAL ARTICLE

Common Soil-Transmitted Helminthiasis in Private Elementary School Children in Two Areas of Metro Manila
Vicente Y. Belizario M.D. MTM&H, Carlo P. Mataverde M.D., Winifreda V. de Leon DAP&E MPH, Donato G. Esparar DAP&E M.Sc. and April Rose Lucero B.S.
University of the Philippines Manila, National Institutes of Health and College of Public Health

ABSTRACT Soil-transmitted helminth (STH) infections, which may have adverse effects on a childs growth and development, remain as one of the major public health problems in the Philippines. Studies have shown that helminth control strategies such as mass treatment can signicantly decrease morbidity and parasite transmission. Although there have been studies obtaining local parasitologic data in public elementary schools, there is still a lack of published studies conducted in private schools. This study aimed to address the problem by conducting a parasitologic assessment of common intestinal helminthiasis in private school children in two selected areas in Metro Manila. Methodology used was adapted from the WHO protocol. Stool specimens were collected, processed and examined utilizing Kato-Katz method that allowed both qualitative and quantitative assessment of the status of infection. Geometric mean egg counts were also derived. In this study, schools surveyed had cumulative prevalence levels that went as high as 32%. Soiltransmitted helminth infections were seen in all areas surveyed. The results of this study call attention to the seemingly neglected problem of intestinal helminth infections being a major cause of morbidity in Filipino children, not only from public schools, but even from private schools. Keywords: Ascaris, Trichuris, hookworm, soil-transmitted helminthiasis, intestinal helminthiasis, epidemiology, school-based control program, private schools

Introduction
In developing countries worldwide, soiltransmitted helminthiasis is ranked rst among the causes of all communicable and noncommunicable diseases in school-age children. Intestinal helminth infections remain as one of the major public health concerns in developing countries like the Philippines. Nationwide biomedical surveys done by the U.S. Naval Medical Research Unit No. 2 (US NAMRU 2) in the 1960s to the 1980s showed that infection rates of the three major soil-transmitted helminths (STH) were 74% for Trichuris trichiura (whipworm),

48% for Ascaris lumbricoides (roundworm) and 38% for hookworm.1 A study by Belizario et al. in 2005 involving public elementary school children in selected sites in Luzon, Visayas and Mindanao, yielded a cumulative prevalence of 67%, with all areas surveyed noted to have rates greater than 50%.2 Another local study on children living in residential institutions in Metro Manila yielded infection rates of 44.8%, 36% and 7% for Trichuris, Ascaris and hookworm, respectively.3 A recent nationwide study in 2004 revealed that 66% of pre-school children were infected with common intestinal helminthes (de Leon and Lumampao, personal communication). The continuing high prevalence of these infections
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may indicate the inadequacy of all past and current efforts by national and local authorities to control this public health problem affecting school children. Children are the largest reservoirs of intestinal helminth infections and are at highest risk because of poor personal hygiene, frequent outdoor exposures and high risk behavior. Studies in endemic areas have shown that the prevalence and intensity of STH such as Ascaris and Trichuris are highest among children 5 to 14 years of age, implying that this age group is at greatest risk for infection.4 These children are most prone to common intestinal helminth infections which lead to adverse effects on nutritional status, growth, academic performance and overall development of children. Chronic infections may also lead to impaired cognitive function and decreased learning ability if these remain untreated.5 Complications include malnutrition, anemia, growth retardation delayed motor activity and poor mental development, all of which compromise the childrens productivity, quality of life and future.6 Schools may provide the most effective and efcient way to control STH infections in large portions of the population. The ease of administration and safety of anthelmintic drugs allow them to be delivered with minimal supervision, even in the school setting. School children not only become beneciaries, but also agents of change in STH control for the whole population. It is widely known that school-based periodic mass treatment has yet to involve a wide area of coverage in the Philippines. Before undergoing such a wide-scale application of technology for control and prevention, it is important to establish the baseline status of intestinal helminth infections. This will help justify the need for the development, implementation and monitoring of control programs at district, provincial, regional or national levels.7 Although there have been
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several studies on intestinal helminth infection status in public schools, there is a lack of published studies conducted in private elementary schools in the Philippines. This study therefore aimed to conduct a parasitologic assessment of common intestinal helminthiasis in private school children in two selected cities in Metro Manila. Specic objectives were: 1) to describe cumulative prevalence of STH in private school children and 2) to describe the prevalence and intensity of each of the STH infections.

Methods
Study Site and Population The study was conducted in seven schools in Quezon City (Divine Grace School, Grace Flous School, Mary the Queen Academy, Metro Manila College, Roosevelt College, Peacemaker International Academy and St. Vincent de Paul Academy of Novaliches) and six schools in Taguig City (M.C.A. Montessori Fort Bonifacio, Philippian Christian Academy, Royal Era Academy, Academia de San Bartolome de Taguig, Mt. Moriah Christian Academy Inc. and Sto. Nino Catholic School Inc.). The private schools were selected based on their proximity to one another in each selected city and their willingness to participate as expressed by school authorities. The scheme of sampling was based on the WHO protocol for sampling elementary school children for the conduct of parasitologic assessment and monitoring.6 Briey, the sample size was 200 to 250 school children from the third grade for each city selected, targeting 40 to 50 school children per school requested to submit stool specimens. Where the number of third grade pupils was lacking, second or fourth grade pupils were requested to submit stool specimens.

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parasitologic assessment was maintained through quality assurance measures. This included proper collection of specimens, availability of fresh reagents, appropriate laboratory technique, meticulous examination of processed specimens and accurate reporting of ndings. Ten percent of all slides were re-examined blindly by a designated expert microscopist to ensure accuracy of microscopic readings. Data handling and analysis Results were recorded as egg counts per parasite species and were double encoded using Epi Info Version 6.0. Cumulative prevalence and intensities of intestinal helminths were then derived with intensity of infection reported as number of eggs per gram (epg) and classied as light, moderate or heavy intensities as shown in Table 1.6 Arithmetic and geometric mean egg counts were derived according to prescribed guidelines.6 Parasitological data including infection rates and egg counts were compared using descriptive statistics.
Table 1. Classes of intensity for schistosome and soil-transmitted helminth infections by stool examination. (WHO, 2002)
Organism Lightintensity infections Moderateintensity infections 5,000-49,999 epg 1,000-9,999 epg 2,000-3,999 epg Heavyintensity infections 50,000 epg 10,000 epg 4,000 epg

Figure 1 - Map of Metro Manila showing Quezon City and Taguig (shaded areas)

Parasitologic Assessment and Quality Control Stool surveys were conducted for parasitologic assessment of school children submitting stool specimens. Stool cups were given to targeted children with appropriate collection instructions on the day prior to collection. Stool samples were then collected and brought to the diagnostic parasitology laboratory of the University of the Philippines Manila (UP Manila) for processing and analysis using Kato Katz method, as described in the World Health Organization Bench Aids for the Diagnosis of Intestinal Parasites.7 Processing was performed by trained research staff, while microscopy was done by expert microscopists in UP Manila. The accuracy and reliability of

A. lumbricoides 1-4,999 epga T. trichiura 1-999 epg Hookworms 1-1,999 epg

a

epg: eggs per gram (of faeces).

Results
Table 2 shows the cumulative prevalence of STH infections in selected schools in the two selected cities.
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Table 2. Summary of cumulative prevalence in selected private schools Quezon City and Taguig City, 2005
School prevalence (%) Divine Grace School Grace Flous School73 Mary the Queen Academy Metro Manila College Roosevelt College Peacemaker International Academy St. Vincent de Paul Academy Overall M.C.A. Montessori Fort Bonifacio Philippian Christian Academy Royal Era Academy31 Academia de San Bartolome Mt. Moriah Christian Academy Inc. Sto. Nino Catholic School Inc. Overall No. of pupils examined 14 13 46 12 41 50 19 255 44 25 5 40 94 38 272 No. of infected pupils 3 17.8 2 1 3 16 1 39 2 6 16.1 6 12 5 36 Cumulative 21.4 4.4 8.3 7.3 32.0 5.3 15.3 4.6 24.0 15.0 12.8 13.2 13.2

Taguig

Quezon City

Quezon City A total of 255 pupils were examined with a range of 12 to 73 pupils examined per school. There were 39 pupils infected with at least one STH giving a cumulative prevalence of 15.3%. Trichuris was the most common STH among pupils examined with an overall infection rate of 9.0%. Ascaris was noted in 7.8% of pupils examined, while hookworm was seen in none of the pupils. The highest cumulative prevalence of STH infection was noted in Peacemaker International Academy with 32.0% infected with STH, while Mary the Queen Academy had the lowest cumulative prevalence (4.4%). No heavy infections were seen in any of the schools. Light intensity Ascaris infections comprised 85% of all infections, while the rest were of moderate intensity (15%). For Trichuris infections, 95.7% were of light intensity, and the remaining 4.3% were of moderate intensity. Overall geometric mean Ascaris egg count was 1.7 epg, while overall mean Trichuris egg count was 1.5 epg. Geometric mean egg counts for both helminths were highest and above the overall mean egg counts in three of the seven schools,
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namely, Divine Grace School, Grace Flous School and Peacemaker International Academy. Taguig A total of 272 pupils were examined with a range of 25 to 94 pupils examined per school. There were 36 pupils infected with at least one STH giving a cumulative prevalence of 13.2%. Ascaris was the most common STH among pupils examined with an overall infection rate of 9.9%. Trichuris was noted in 5.2% of pupils examined, while hookworm was seen in none of the pupils. Highest prevalence for STH infection was noted in Philippian Christian Academy with 24% of pupils examined, while M.C.A. Montessori Fort Bonifacio had the lowest prevalence at 4.6%. No heavy infection was seen in any of the schools. Light intensity Ascaris infections comprised 81.5% of all infections, while the rest were of moderate intensity (18.5%). All Trichuris infections were of light intensity. Overall geometric mean Ascaris egg count was 1.9 epg, while overall mean Trichuris egg count was 1.3

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epg. Geometric mean Ascaris egg counts were highest and above the overall mean egg count in four out of six schools, namely, Philippian Christian Academy, Royal Era Academy, Academia de San Bartolome de Taguig, and Mt. Moriah Christian Academy Inc. Geometric

mean Trichuris egg counts were highest and above the overall mean egg count in three out of six schools, namely, M.C.A. Montessori Fort Bonifacio, Royal Era Academy, and Mt. Moriah Christian Academy Inc.

Table 3. Intestinal helminth infection rates in selected private schools Quezon City and Taguig City, 2005
School No. of pupils examined No. Quezon CityDivine Grace School 14 73 46 12 41 50 19 255 44 25 31 40 94 38 272 1 8 1 1 0 8 1 20 2 4 4 5 10 2 27 Ascaris % 7.1 11.0 2.2 8.3 0.0 16.0 5.3 7.8 4.6 16.0 12.9 12.5 10.6 5.3 9.9 Trichuris No. % 2 8 1 0 3 9 0 23 0 3 1 3 4 3 14 14.3 11.0 2.2 0.0 7.3 18.0 0.0 9.0 0.0 12.0 3.2 7.5 4.3 7.9 5.2

Quezon City

Grace Flous School Mary the Queen Academy Metro Manila College Roosevelt College Peacemaker International Academy St. Vincent de Paul Academy Overall TaguigM.C.A. Montessori Fort Bonifacio Philippian Christian Academy

Taguig

Royal Era Academy Academia de San Bartolome Mt. Moriah Christian Academy Inc. Sto. Nino Catholic School Inc. Overall

Discussion
Cumulative prevalence of STH infections in the two areas ranged from 4.4% to 32% in Quezon City, and 4.6% to 24% in Taguig, showing that none of the schools surveyed were free from STH infection. The study may provide an estimate of the STH infection status of private schools in each area surveyed; however, the results of this study may not be generalized to the two cities, much less all private schools in the country. Even though only one, or a few grade levels were included in

the sample selection, infection rates may not vary signicantly across different grades of a school because this age group of elementary school age children is considered high risk.9 The results suggest that contrary to popular belief, private schools are not spared from STH infections. Although the cumulative STH prevalence rates and intensities of infection for both areas were markedly less than prevalence and intensity levels from surveys in public schools in the Philippines,2 this study suggests that up to one out of three children may be infected.
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Table 4. Summary of distribution of Ascaris intensities in selected schools Quezon City and Taguig City, 2005
School Divine Grace School Grace Flous School Mary the Queen Academy Metro Manila College Roosevelt College Peacemaker International St. Vincent de Paul Academy Overall M.C.A. Montessori Ft. Boni Philippian Christian Academy Royal Era Academy Academia de San Bartolome Mt. Moriah Christian Academy Sto. Nino Catholic School Inc. Overall No. of pupils infected (%) Light (%) 1 (7.1) 8 (11.0) 1 (2.2) 1 (8.3) 0 (0.0) 8 (16.0) 1 (5.3) 20 (7.8) 2 (4.6) 4 (16.0) 4 (12.9) 5 (12.5) 10 (10.6) 2 (5.3) 27 (9.9) 0 (0.0) 8 (100.0) 1 (100.0) 1 (100.0) 0 (0.0) 6 (75.0) 1 (100.0) 17 (85.0) 2 (100.0) 4 (100.0) 3 (75.0) 5 (100.0) 6 (60.0) 2 (100.0) 22 (81.5) Intensity of Infection Mod (%) 1 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (25.0) 0 (0.0) 3 (15.0) 0 (0.0) 0 (0.0) 1 (25.0) 0 (0.0) 4 (40.0) 0 (0.0) 5 (18.5) Heavy (%) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

Compared to the public school survey, infections in this study were composed of only light and moderate intensities, with no incidence of heavy intensity infections. Although there is a lower chance for major morbidities in light and moderate STH infections, these should not be taken lightly. STH infections can cause respiratory and gastrointestinal symptoms, which although milder than symptoms resulting from a heavy infection, can at times be clinically signicant. The lower prevalence and intensities of STH infections found in these private schools could be attributed to better environmental sanitation and personal hygiene, compared to children from public schools.
Table 5. Summary of distribution of Trichuris intensities in selected schools Quezon City and Taguig City, 2005
School Divine Grace School Grace Flous School Mary the Queen Academy Metro Manila College Roosevelt College Peacemaker International St. Vincent de Paul Academy Overall TaguigM.C.A. Montessori Ft. Boni Philippian Christian Academy Royal Era Academy Academia de San Bartolome Mt. Moriah Christian Academy Sto. Nino Catholic School Inc. Overall No. of pupils infected (%) Light (%) 2 (14.3) 8 (11.0) 1 (2.2) 0 (0.0) 3 (7.3) 9 (18.0) 0 (0.0) 23 (9.0) 0 (0.0) 3 (12.0) 1 (3.2) 3 (7.5) 4 (4.3) 3 (7.9) 14 (5.2) 2 (100.0) 8 (100.0) 1 (100.0) 0 (0.0) 2 (66.7) 9 (100.0) 0 (0.0) 22 (95.7) 0 (0.0) 3 (100.0) 1 (100.0) 3 (100.0) 4 (100.0) 3 (100.0) 14 (100.0) Intensity of Infection Mod (%) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (33.3) 0 (0.0) 0 (0.0) 1 (4.4) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) Heavy (%) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0)

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Taguig

Quezon City

Taguig

Quezon City

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STH infections may be controlled by relatively simple and cost-effective interventions. Periodic mass treatment in the form of chewable and attractive preparations of albendazole or mebendazole tablets, given single dose, two to three times a year, has shown excellent activity against STH. With periodic mass treatment, a signicant reduction in the number of heavily infected individuals plus an improvement in nutritional status can be achieved over time, which results in an overall better quality of life for schoolchildren.10 Mass treatment of schoolage children can already reduce STH infection burden by 70% in the community as a whole.11 Studies have shown that treatment targeted specically at children can be implemented within an existing health infrastructure and can achieve an overall reduction in prevalence and intensity of helminth infection.11 Delivering a universal, standard, school-based health intervention can also offer signicant savings in delivery costs.12 Schools can therefore provide an ideal setting in which to implement helminth control for an important high-risk group.13 Community-based chemotherapy control programs for soil-transmitted helminthiasis are recommended by the WHO, depending on community category in terms of prevalence and proportion of heavy intensity infections (WHO, 1998). Since there were no areas in this study with heavy infections, areas in this study will only require selective treatment. However, additional stool examinations can entail greater costs. A more cost-effective strategy is recommended in the form of mass treatment implemented once a year in these schools. In the Philippines, a proposed model for schoolbased worm control involving mass treatment and health education has been well documented. This method has been shown to result in sustained and signicant drops in terms of parasitologic indicators.9 The programs objective is to deliver the appropriate intervention package to as many school-age children as possible, in the form of antihelminthic chemotherapy, micronutrient

supplementation, health education activities, latrines, hand-washing, proper waste disposal, proper wearing of footwear, and others. Key players for school-based worm control in public schools are the local government and their health units. In contrast, key players in the private school sector would also include the childrens families, especially their parents. The most important factor for sustaining helminth control programs in schools is the support of the childrens parents and families, and of the community in general.13 With the help of information dissemination, families should be tapped as important resources, to provide for the cost of drugs, to improve hygiene and sanitation, and to reinforce health education activities. Parents and school ofcials should spearhead advocacy campaigns on handwashing and health education, with a focus on STH infection transmission, diagnosis, treatment, prevention, and control. The parasitologic indicators evaluated in this study can be used for assessment of progress and impact, and monitoring of control in the private schools surveyed. The results from this study provide us a glimpse of STH status in private schools in the Philippines. The results also call to attention a seemingly neglected problem in Filipino children, which spares no child, not even those from private schools. As one of the top worldwide causes of morbidity among children ages 5 to 14 years, STH infection should be one of the problems given priority in all countries, to enhance quality of life, health and productivity of children.5 Thus, school-based STH control programs are recommended not only for public schools, but also for private schools.

Acknowledgments
This project would not have been successful without the invaluable assistance of the teachers and school ofcials from the participating schools in Quezon City and Taguig, namely: Divine Grace School, Grace Flous School, Mary the Queen Academy, Metro Manila College, Roosevelt College, Peacemaker International Academy, St.
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Common Soil-Transmitted Helminthiasis schistosomiasis at community level (WHO/CTD/ SIP/98.1). Geneva: World Health Organization, 1998. 7. World Health Organization. Bench aids for the diagnosis of intestinal parasites. Geneva: World Health Organization, 1994. 8. Belizario VY, Solon JA, eds. Study Guide in Medical Parasitology. Manila, Philippines: Department of Parasitology, College of Public Health, University of the Philippines Manila; 1999. 9. Belizario VY, Amarillo ML, de los Reyes AB, et al. A model for school-based mass treatment for common intestinal helminth infections: parasitologic assessment. Transaction of the National Academy of Science and Technology of the Philippines 2000; 22:137-156. 10. World Health Organization. Monitoring helminth control programmes. (WHO/CDS/SIP/99.3). Geneva: World Health Organization, 1999. 11. Bundy DAP, Wong MS, Lewis LL & Horton J. Control of geohelminths by delivery of targeted chemotherapy through schools. Transactions of the Royal Society of Tropical Medicine and Hygiene, 1990, 84: 115-120. 12. Azene G, Guyatt H, Brooker S, Hall A, Bundy DAP. The cost of large-scale school health programmes which deliver anthelmintics to children in Ghana and Tanzania. Acta Tropica, 1999, 73: 183-204. 13. Montressor A, et al. Helminth Control in schoolage children: a guide for managers of control programmes. Geneva, World Health Organization, 2002.

Vincent de Paul Academy of Novaliches, M.C.A. Montessori Fort Bonifacio, Philippian Christian Academy, Royal Era Academy, Academia de San Bartolome de Taguig, Mt. Moriah Christian Academy Inc. and Sto. Nino Catholic School Inc. Special thanks also goes to Janssen Pharmaceutica for providing nancial support to make this undertaking possible.

References
1. Cross J, Basaca-Sevilla V. Biomedical Surveys in the Philippines. United States Naval Medical Research Unit No.2, Manila, Philippines. 1984. 2. Belizario VY, de Leon W, Wambangco MA, Esparar D. Baseline Parasitologic Assessment in Selected Public Elementary Schools in Luzon, Visayas and Mindanao, 2005. 3. Baldo ET, Belizario VY, De Leon WU, Kong HH, Chung DI. Infection Status of intestinal parasites in children living in residential institutions in Metro Manila, the Philippines. The Korean Journal of Parasitology 2004; 42(2):67-70. 4. Xu LQ, Yu SH, Jiang ZX, et al. Soil transmitted helminthiasis: nationwide survey in China. Bulletin of the World Health Organization 1995;73:507-513. 5. World Health Organization. WHO Information series on school health. (WHO/SCHOOL/96.1, WHO/HPR/HEP/96.1). Geneva: World Health Organization, 1997. 6. World Health Organization. Guidelines for the evaluation of soil-transmitted helminthiasis and

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