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The control of soil-transmitted helminthiases in the Philippines: the story continues

Infectious Diseases of Poverty volume 10, Article number: 85 (2021) Cite this article

Abstract

Background

Soil-transmitted helminth (STH) infections have long been an important public health concern in the Philippines. In this review, we describe the current status of STH infections there and highlight the control efforts undertaken to reduce STH burden.

Main text

A nationwide STH mass drug administration (MDA) programme was started in 2006 but the overall STH prevalence remains stubbornly high across the Philippines, ranging from 24.9% to 97.4%. The continued increase in the prevalence may have been due to the challenges related to MDA implementation which include the lack of people’s awareness about the importance of regular treatment, misconceptions about the MDA strategy, lack of confidence on the drugs used, fear of adverse events and general distrust of government programs. There are existing water, sanitation and hygiene (WASH) programmes implemented in communities [e.g., Community-Led Total Sanitation (CLTS) program and providing toilet bowls and provision of subsidy for latrine construction] and schools [e.g., WASH in School (WINS) program], but sustained implementation is required to achieve expected outcomes. Although WASH in general is being taught in schools, integration of STH as a disease and community problem in the current public elementary school curriculum is still inadequate. The Integrated Helminth Control Program (IHCP) currently implemented in the country, which is focused on improved sanitation and personal hygiene, health education and preventive chemotherapy, will require continuous appraisal. The sustainability of this programme still continues to be a challenge.

Conclusions

Despite the major efforts to control STH infections for almost two decades in the Philippines, persistently high STH prevalence has been reported across the country, which is likely due to suboptimal MDA coverage and limitations in WASH and health education programs. Sustainable delivery of integrated control approaches will continue to play a pivotal role in the control and elimination of STH in the Philippines.

Graphic abstract

Background

Soil-transmitted helminth (STH) infections continue to be a serious public health problem worldwide with more than 1.5 billion people estimated to be infected [1]. STH affect underprivileged communities, characterised by poor access to adequate water, sanitation and hygiene (WASH) [2, 3]; and are highly endemic in low-income countries, with the majority of infections occurring in Asia, Africa, and parts of Latin America [4]. Pre-school-aged children (PSAC) aged 2–4 years and school-aged children (SAC) aged 5–12 years are the most vulnerable to infection and have the highest prevalence and infection intensity. Available data indicate that more than 267.5 million PSAC and more than 568.7 million SAC reside in areas with intense STH transmission, requiring preventive chemotherapy [5]. The global STH burden has been estimated to range from 1.97–3.3 million disability-adjusted life years (DALYs) [6, 7].

STH infections may result in nutritional deficiency and impaired physical and cognitive development especially in children [8]. High-intensity STH infections exacerbate morbidity [9,10,11]. Polyparasitism (infection with multiple parasite species) has also been shown to be associated with higher mortality rates and increased susceptibility to other infections [10, 11]. The adverse impact of these infections not only affects health but also economic productivity [8, 12].

The Philippines is a lower middle-income country. In 2015, approximately 21.6% of the Philippines’ 100.98 million population were living below the national poverty line [13]. It also has some of the highest prevalence levels of STH in Southeast Asia [14]. The 2019 figures from the WHO Preventive Chemotherapy Databank indicate that about 45 million children are at risk of infection necessitating drug treatment [15].

Although several large initiatives have been launched to control or interrupt transmission, STH remains highly endemic in the Philippines [16]. In this article, we provide an overview of the current status of STH infections in the Philippines; highlight the past and current control efforts being undertaken, document the challenges and travails of the program implementation, assess their impact to reduce the STH burden and provide possible prospects for the control of intestinal worms. The availability of this information may provide the basis for planning and implementing a sustainable STH control program in the country.

This review focuses on the four most common STH parasites—Ascaris lumbricoides, Trichuris trichiura, Necator americanus and Ancylostoma duodenale. Although, Ancylostoma ceylanicum is emerging as an important zoonotic species of hookworm in Southeast Asia, limited information is currently available in the Philippines, and so it will no longer be discussed here.

Search methodology

Although this is not a systematic review, the methods used for the literature review are as follows. We conducted a search of the relevant studies reporting STH prevalence in the Philippines using the PubMed, Scopus, ProQuest and Google Scholar online databases. The following words were used as keywords in the search: (“Helminthiases” OR Soil-transmitted helminths” OR “STH” OR “Ascaris lumbricoides” OR “Trichuris trichiura” OR “Ancylostoma spp.” OR “Necator americanus” or “Roundworm” OR “Whipworm” OR “Hookworm”), AND (“Epidemiology”) AND (“Philippines”). There was no restriction on the year of publication. Articles identified by the search criteria were initially screened by title and abstract content and those that did not investigate prevalence or intensity in at least one of the three STH were excluded. Full text screening included observational (cross-sectional, case control, longitudinal/cohort) studies or controlled trials which reported the baseline prevalence. Data extraction included study area, year the study was conducted, year the study was published, type of study (cross-sectional, case–control or longitudinal/cohort), sample size, study population, prevalence and intensity of each STH and the diagnostic methods used.

Based from the literature search, a total of 1421 records were identified through database searching [PubMed (n = 322); Scopus (n = 13); ProQuest (n = 151), and Google Scholar (n = 935)]. A total of 48 papers were screened based on title review, of which 6 papers were then excluded, bringing the final total to 42 papers included in the qualitative synthesis (Fig. 1).

Fig. 1
figure 1

Study selection

Full size image

Epidemiology of STH infections in the Philippines

Numerous studies have been conducted since the 1970s in the Philippines to determine the prevalence and intensity of STH infections. Table 1 shows a summary of studies identified. Differences in the methods of STH diagnosis were evident across these studies over time, with the formalin-ether concentration (FEC) method frequently being used in the early period (1970–1998). The Kato-Katz (KK) technique, however, was used increasingly in the later years and employed as the primary diagnostic method in the national surveys to monitor the STH control program.

Table 1 Key outcomes of studies investigating STH infections in the Philippines
Full size table

As indicated by studies conducted from the 1970s–2018, STH infections have been and still are important public health problems in the Philippines. The epidemiological patterns of STH infections and their prevalence are comparable to those reported in other endemic countries around the world, with the highest infection prevalence recorded in PSAC and SAC [17]. These age groups are at greater risk as these children are frequently exposed to STHs in outdoor settings.

Historically, the prevalence of any STH infections and heavy intensity infections in children aged 1–12 years before the implementation of the Integrated Helminth Control Program (IHCP) of the Department of Health ranged from 48.6–66.8% to 9.9–67.4%, respectively [18,19,20,21,22,23] (Table 1).

STH data from the national schistosomiasis survey undertaken from 2005 to 2008 across all ages showed wide-scale distributions of STH infection across three principal geographical divisions of the country, with A. lumbricoides and T. trichiura particularly prevalent in the Visayas [16, 24, 25].

In 2009, a follow-up assessment of the nationwide STH prevalence surveys for PSAC in 2004 [20] and for SAC in 2006 [21] was conducted to assess the impact of the IHCP [26]. The prevalence of any STH for PSAC was 43.7% (vs 66% in the 2004 survey) and 44.7% (vs 54% in the 2006 survey) for SAC [26]. These were significantly lower than reported in the earlier two surveys. The prevalence of heavy-intensity STH infections for PSAC in 2009 was 22.4% (comparison with the 2004 survey was not possible as the overall prevalence of heavy intensity infection was not reported), and 19.7% (vs 23.1% in 2006 survey) for SAC with a 14% reduction [26]. Although, reductions in infection prevalence were evident, the estimated prevalence of STH in the PSAC and SAC populations still did not meet the 2020 targets of less than 20% cumulative prevalence and less than 1% heavy intensity STH infection as defined by WHO to demonstrate morbidity control [27, 48].

Other studies employing parasitological surveys conducted at several time points (2006–2011) to monitor the impact of the school-based MDA among SAC also showed similar trends [22, 28, 29]. Results from these surveys demonstrated reductions in STH prevalence after several rounds of MDA; however, the reported overall prevalence for any STH (ranging from 44.3 to 47.7%) and heavy intensity infections (ranging from 14.5 to 24.6%) were still high at the follow-up surveys [22, 28, 29], again indicating that the prevalence had not been reduced to the target levels for morbidity control defined by WHO (Table 1).

Data from other studies identified after the launch of IHCP across the Philippines in 2007–2018 among PSAC and SAC showed persistently high levels of STH prevalence (Table 1) [30,31,32,33,34,35,36,37,38,39]. The prevalence of any STH reported from these studies ranged from 24.9 to 97.4% (by KK) and the prevalence of moderate to heavy intensity infections ranged from 5.9 to 82.6%. A. lumbricoides and T. trichiura remained the most prevalent STH with prevalence ranging from 15.8–84.1% to 7.4–94.4%, respectively, while the hookworm prevalence tended to be lower ranging from 1.2 to 25.3% [30,31,32,33,34,35,36,37,38,39] (Table 1). One study, however, in 2011, using the molecular diagnostic quantitative real time polymerase chain reaction (qPCR) showed a hookworm (Ancylostoma spp.) prevalence of 48.1% [45]. Co-infections of individuals with A. lumbricoides and T. trichiura were also commonly observed in several studies [26, 31, 33, 36, 45].

The KK method, recommended by the WHO due to its ease of use in the field and low cost [46], is primarily employed for assessing the government treatment program for STH control. However, differences in STH prevalence have been reported between KK and other diagnostic methods. In a study conducted in 2014 in the province of Laguna, a large discrepancy in the prevalence between KK and qPCR was noted in the detection of any STH infection (33.8% by KK vs 78.3% by qPCR), A. lumbricoides (20.5% by KK vs 60.8% by qPCR) and T. trichiura (23.6% by KK vs 38.8% by qPCR). There were also hookworm infections [6.8% prevalence; comprising Ancylostoma spp. (4.6%) and Necator americanus (2.2%)] detected using qPCR that were judged as negative by KK [36]. The true prevalence of hookworm infections can be considerably underestimated because the rapid lysis of hookworm eggs necessitates a rapid turn-around in KK slide preparation and reading [36, 45, 47], a process often difficult to achieve under field conditions. In addition, the eggs of hookworm species are indistinguishable morphologically, which presents a further challenge in terms of correct identification [45].

STH control in the Philippines

The main strategy for STH control advocated by WHO focuses on large-scale preventive chemotherapy using albendazole or mebendazole for at-risk populations with the target of treating at least 75% of PSAC and SAC by 2020 [48]. Until the recent launch of the Neglected Tropical Diseases (NTDs) 2030 roadmap, the WHO recommends that PSAC, SAC, and women of reproductive age (aged 15–49 years, including pregnant women in their second and third trimester) receive regular treatment [49]. Additionally, the guidelines include young children (aged 12–23 months) and adolescent girls (aged 10–19 years) [49] but exclude the previous recommendation of treating adults in high-risk occupations [50]. The WHO recommends annual MDA of young children, PSAC, SAC, adolescent girls and women of reproductive age in areas where the prevalence of STH is between 20 and 50% and semi-annual if the prevalence is above 50%. For pregnant women, the treatment interval was not defined [49]. In addition to preventive chemotherapy, the WHO has highlighted water, sanitation and hygiene (WASH) as important components of STH control [48, 49].

The IHCP was launched in 2006 to provide policy directions for the control of STH and other helminth infections [20, 51]. The program, which follows the strategies endorsed by WHO for STH control, has chemotherapy with albendazole or mebendazole as the primary strategy for STH control and targets children aged 1–12 years and other high-risk group such as pregnant women, adolescent females, farmers, food handlers, and the indigenous population. The control program is also supplemented with the installation of water and sanitation facilities and health promotion and education approaches [20, 46].

Preventive chemotherapy

The semi-annual MDA for PSAC is primarily conducted in the community setting by local barangay (village) health units, trained barangay health workers, and day care workers as part of the Garantisadong Pambata or “Healthy Children” (a program that delivers a package of health services for PSAC) while the MDA for SAC is overseen and implemented by the Department of Education (DepEd) [20]. MDA in public elementary schools is administered by teachers under the direction of health workers every first and third quarter of the school year [20]. In 2016, the DOH issued new guidelines to include deworming in secondary schools (children up to 18 years of age) [52].

The first nationwide semi-annual MDA was conducted among children aged 1–12 years in 2006 [20], reporting a deworming coverage of 82.8% of the 6.9 million PSAC and 31.5% of the 6.3 million SAC [53]. However, MDA deworming coverage from 2009–2014 went down considerably (range 59.5–73.9%), a figure consistently below the 75% benchmark recommended by the WHO [54]. The low deworming coverage may have been due to a lack of awareness of the importance of regular treatment [55], misconceptions about the MDA strategy [56, 57], lack of confidence in the drugs used [58], and fear of adverse events [55, 56, 58,59,60]. There have been reports of fear of birth defects as a reason for refusing STH treatment in pregnant women [61]. Moreover, the supply of MDA drugs and logistical issues have been identified as major shortcomings encountered during the nationwide MDA implementation [54].

In 2015, the DOH, in partnership with DepEd, conducted the first National School Deworming Day (NSDD) that aimed to deworm approximately 16 million SAC (grades 1 to 6) enrolled in all public elementary schools in one day [62]. This school-based initiative resulted in a national deworming coverage of 81%, which was higher than the previous years [54]. However, false information circulating in the community on deaths among children following deworming and the use of expired drugs caused mass hysteria and panic, resulting in an increase of reports of adverse events following MDA (AEFMDA) in Zamboanga Peninsula on the island of Mindanao [63]. However, a case-control study, showed that being an AEFMDA case was associated with no history of previous deworming [63].

In 2017, a new dengue vaccine was introduced by the DOH and given to some 800 000 school children. The provision of this vaccine raised major safety issues and resulted increased distrust in the DOH programs, including the MDA program [64, 65]. As a result, the deworming coverage decreased from 81 and 73% among PSAC and SAC in 2017 to 63% and 52%, respectively in 2018, and to 60% and 59%, respectively, in 2019 [15].

Additionally, in view of the current global COVID-19 (coronavirus disease 2019) pandemic, the DOH issued the Department Memorandum Number 2020–0260 or the “Interim Guidelines on Integrated Helminth Control Program and Schistosomiasis Control and Elimination Program during the COVID-19 pandemic” on June 23, 2020, prescribing the suspension of MDA until further notice. Due to school closures, routine deworming of children aged 1–18 was administered in the community either through house-to-house visits or fixed site distribution of drugs while maintaining physical distancing and appropriate infection prevention control measures against COVID-19 [66]. The restrictions on the movement of people and the public anxiety due to COVID-19 pandemic may however, lead to lower treatment coverage.

WASH

WASH is one of the key interventions outlined by the IHCP for STH control [20, 46]. It is a program that involves multiple government agencies including the DOH, Department of Interior and Local Government (DILG), local government units (LGUs) and DepEd. Among the WASH programs in the community are provision of access to safe water which is spearheaded by the LGUs with support of DILG [67] and sanitation improvements implemented by the DOH with the help of the LGUs in providing toilet bowls and subsidies for latrine constructions [68, 69]. Meanwhile, WASH programs in public elementary schools is supervised by the DepEd, in partnership with the DOH.

Recent data from the 2017 National Demographic Health Survey by the Philippines Statistics Authority (PSA) shows that 95% of Filipino households obtain their drinking water from an improved source, the greatest proportion (43%) sourcing their water from bottled water, with only 26% obtaining it from a piped sourced [70]. A quarter of Filipino households still use unsatisfactory sanitation [70]; and about 4.5% of the population openly defecate, a practice twice as prevalent in rural areas (6%) than in urban areas (3%) [70].

Other reports have shown that the provision of sanitation facilities alone did not guarantee their utilization nor did they result in improving sanitation and hygiene practices [32, 68, 69]. The most frequently cited reason for not improving sanitation among households that lack a toilet include technical barriers (i.e., lack of space in the home for toilets or around the home for septic tanks, and other geographical considerations such as soil conditions and proximity to waterways), land ownership and lack of funds [71, 72].

The DOH through the Development of Sustainable Sanitation in East Asia – Philippines Programme, adopted the Community-Led Total Sanitation (CLTS) approach in 2007 [68, 73]. CLTS is under the umbrella concept of total sanitation, which includes a range of behaviours such as stopping open defecation practices, ensuring that everyone uses a sanitary toilet, frequent and proper hand washing, hygienic handling of food and water, safe disposal of animal and domestic waste, and creation and maintenance of a clean and safe environment [68, 69]. To ensure sustainability of the CLTS approach, the ODF status of the villages should be continuously monitored even after the termination of the CLTS activities. Nevertheless, some studies have shown high STH prevalence in communities that have attained ODF status after the CLTS was implemented [32, 33]. This may have been due to the non-utilization of sanitary facilities, the possible reversion to open-defecation, and low MDA coverage [32].

The WASH programs implemented in schools follow the policies issued by the DOH and the DepEd. In 1998, the DOH issued the Implementing Rules and Regulations (IRR) of School Sanitation and Health Services of the Code on Sanitation of the Philippines (PD No. 856) [74]. This IRR specifies the rules and regulations on school sanitation and satisfactory sanitary facilities, which include toilets, water supply, and the care and maintenance of these facilities [74]. However, assessments of the DepEd’s implementation of this program in selected provinces showed that the guidelines have not been strictly implemented and there was insufficient budgetary support [57, 75,76,77]. Thus, monitoring and evaluation will remain critical to ensure the sustainability of the DepEd’s implementation of the WASH program.

In addition, to institutionalize good health practices among students, the DepEd issued Department Order (D.O.) No. 56, s. 2009 entitled “Immediate construction of Water and Hand Washing Facilities in All Schools for the Prevention of Influenza A (H1N1)” and D.O. No. 65, s. 2009 entitled “Implementation of the Essential Health Care Program (EHCP) for the school children” [78, 79]. Although the first program was aimed at preventing the spread of H1N1, this was also relevant for STH control. The latter follows the Fit for School approach and focuses on three evidence-based school health interventions: handwashing with soap, tooth brushing with fluoride toothpaste as a daily group activity, and semi-annual MDA for STH [78, 80]. In 2016, the EHCP was now integrated into the WASH In Schools (WINS) program. It was expanded to include provision of water, sanitation, food handling and preparation, hygiene improvement (e.g., menstrual hygiene management), deworming and health education [79].

Heath education

While in general WASH, is included in the elementary school curriculum [79], the inclusion of STH infections as a disease and public health problem is still lacking. A recent study conducted in selected public elementary schools in the province of Cagayan reported that health education related to WASH is available to all students regardless of their grade level and type of school and it is also integrated in several subjects and is pervasively promoted (i.e., materials that promote health education are visually present in classrooms, WASH areas and the entire school) [57]. However, the same study recommended the need for teachers to receive training on STH and deworming to develop a deeper understanding of the parasites and a greater appreciation of STH as a public health problem including: topics related to STH transmission, risk of infection, risk of open defecation and mode of reinfection after deworming being introduced into the school curriculum [57].

The relationship between health education and treatment acceptance has also been demonstrated in other studies [56, 60] which indicate that intensified health education and promotion (to improve STH knowledge and to correct MDA misconceptions on treatment and benefits) could increase MDA treatment participation and acceptance [56, 60].

Additionally, the importance of health education to influence good sanitation related behaviours has been identified as one of the crucial components of WASH implementation [33, 60]. As indicated in previous studies, open defecation does not necessarily arise from the lack of latrine access [32, 33]. Factors such as the habit of open defecation and non-use of sanitary facilities may influence open defecation outcomes [68, 69]. In another study, poor sanitation facilities have been linked to a high risk of functional illiteracy among SAC in the Visayas region [81]. Thus, the importance of incorporating health education and promotion strategies aimed at improving defecation and hygiene practices, and acceptance and appropriate use of these sanitary infrastructure, are needed to sustain the uptake of WASH interventions.

Future directions

Data collected over the past two decades indicate that the prevalence and intensity of STH infections remain high among children aged ≤ 12 years in the Philippines, despite the various efforts of the Philippine government. Identification of barriers and challenges in MDA participation and treatment compliance is required to ensure high MDA coverage. It is also noteworthy to consider the efficacy of the two drugs (albendazole and mebendazole) currently used by the STH control program, as alarmingly high T. trichiura infections have been reported in some recent studies in the Philippines [33, 34, 42]. Both drugs are reported to have low efficacy against T. trichiura, with pooled cure rates of 30.7% and 42.1%, and egg reduction rates of 49.9% and 66.0%, for albendazole and mebendazole, respectively [82]. This may have critical implications in areas where T. trichiura is prevalent, given the minimal treatment impact of both drugs. Chemotherapy is effective at reducing the level of infection and reducing worm burdens of infected individuals below the morbidity threshold but as well as variable efficacy across the STH species. It is of note that the available drugs do not prevent reinfection, which can happen immediately after treatment. Thus, new drugs and drug combination strategies may be needed in the future [83].

Currently, there is no mandated MDA treatment for adults in the Philippines. The IHCP focuses only on children aged 1–18 years, and selective deworming of other at-risk groups such as pregnant women, adolescent females, farmers, food handlers, and the indigenous population [46]. However, recent mathematical modelling [84,85,86] and a systematic review and meta-analysis [87] show that expanding the deworming programmes community-wide, to encompass all age groups, is likely to reduce the prevalence of STH in the high-risk schoolchildren group. Scaling up from targeted drug administration to community-wide MDA may, however, have important economic implications for the STH control program since an increase in resources would be needed. Nevertheless, the effective mass treatment campaign for lymphatic filariasis conducted in the Philippines highlights the feasibility of delivering community-wide treatment [52].

As a result of the ongoing COVID-19 pandemic, the school-based MDA campaign for STH across the Philippines has been halted and so resurgence in STH infections is expected. Recent mathematical modelling showed that delays in MDA in high STH prevalence settings may mean that the 2030 target for STH elimination as a public health problem (EPHP) (defined as reaching < 2% prevalence of moderate-to-high intensity infections in SAC [88]) may not be achievable, although mitigation strategies (i.e. higher MDA coverage,  > 75%) to make up for the missed MDA rounds will be beneficial [89]. Therefore, more sustainable control strategies to augment MDA are urgently needed to combat STH infections in the Philippines.

In addition to MDA, transmission interruption also requires changes in hygiene behaviour, access to safe water and improvement of sanitation facilities through effective WASH and CLTS programmes. Somewhat discouragingly, however, there have been reports of sanitary facilities provided by LGUs not being fully utilized in some communities, reflecting existing challenges in WASH implementation [68, 69, 71, 72]. Furthermore, high STH prevalence has been reported in communities who have attained ODF status after CLTS implementation due to reversion to open defecation behaviour and low MDA coverage [32]. Cultivating knowledge and awareness of STH and improving hygiene behaviour is an important approach in lowering the individual risk of infection, essentially providing a low-cost supplement to MDA and WASH programmes.

Health education delivered in schools may help strengthen and improve both student and parental knowledge and awareness about STH in general, including the perceived benefits of deworming. An example of a recent and highly successful health education intervention delivered in schools is the “Magic Glasses” program. This is a short cartoon-based intervention designed to educate students on STH infection and prevention provided proof of principle that health education can improve knowledge and influence behaviour related to STH infection [90]. This program was first used on Chinese primary school children in Hunan Province which reduced the incidence of STH infection by 50% (odds ratio = 0.5, 95% confidence interval: 0.35–0.7, P < 0.0001) in intervention schools compared with control schools [90]. This has been adapted and rigorously tested in the Philippines [91] and in Vietnam; and is currently being developed for the Lower Mekong region including its adaptation to combat carcinogenic Opisthorchis liver fluke infections. Experiences in several Asian countries particularly Japan, Republic of Korea and Taiwan Province of China have shown that elimination of STH infections is possible with MDA, appropriate sanitation and hygiene education as part of national control programmes through a school-based approach and triangular cooperation among government agencies, non-government organizations and scientific experts [92,93,94].

There are several programmes incorporating STH control operating in the Philippines such as the WASH/EHCP or WINS implemented in schools and the CLTS implemented in communities. However, for greater chances of sustainability, there is a need for improved coordination among organizations implementing the program. Thus, a decentralised program and a multi-party endeavour such as that undertaken for STH control in the Philippines can only succeed with long term collaboration, cooperation and buy-in from the local government. There is a need for governmental support in the procurement and distribution of drugs and in prioritizing other components of the control program such as activities that improve environmental sanitation and health education to accelerate progress towards the 2030 EPHP goal [88]. With the challenges of the COVID-19 pandemic, these activities need to be continued and be integrated with the ongoing COVID-19 prevention efforts. Otherwise, compromising the already challenged STH control programme may result in severe long term public health outcomes.

Conclusions

The Philippines has undertaken major efforts to control STH infections for almost two decades. Nevertheless, persistently high STH prevalence has been reported across the country, which is likely due to suboptimal MDA coverage and limitations in WASH and health education programs. The National government should now consider strengthening school-based MDA and expansion to community-wide MDA; close monitoring of drug effectiveness during MDA campaigns and investigating the development and use of new antihelminthic drugs or drug combinations; and the sustainable delivery of WASH and health education as an integrated method of attack for future STH control in the Philippines.

Availability of data and materials

Not applicable.

Abbreviations

AEDMDA:

Adverse events following MDA

CLTS:

Community-led total sanitation

COVID-19:

Coronavirus disease 2019

DALY:

Disability-adjusted life year

DepED:

Department of Education

DILG:

Department of Interior and Local Government

DOH:

Department of Health

EPHP:

Elimination as a public health problem

EHCP:

Essential health care program

FET:

Formalin-ether technique

IHCP:

Integrated helminth control program

KK:

Kato-Katz

MDA:

Mass drug administration

NTDs:

Neglected tropical diseases

PSAC:

Pre-school children

qPCR:

Real-time polymerase chain reaction

SAC:

School-aged children

STH:

Soil-transmitted helminths

WASH:

Water, sanitation and hygiene

References

  1. WHO. Soil-Transmitted Helminth Infections. https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections. Accessed 4 April 2021.

  2. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014;11(3):e1001620.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Hotez PJ, Fenwick A, Savioli L, Molyneux DH. Rescuing the bottom billion through control of neglected tropical diseases. Lancet. 2009;373(9674):1570–5.

    Article  PubMed  Google Scholar 

  4. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37.

    Article  PubMed  PubMed Central  Google Scholar 

  5. WHO. Summary of global update on preventive chemotherapy implementation in 2016: crossing the billion. Weekly Epidemiol Record. 2017;40(92):589–608.

    Google Scholar 

  6. DALYs GBD, Collaborators H. Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388(10053):1603–58.

    Article  Google Scholar 

  7. Diseases GBD, Injuries C. Global burden of 369 diseases and injuries in 204 countries and territories, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet. 2020;396(10258):1204–22.

    Article  Google Scholar 

  8. Jourdan PM, Lamberton PHL, Fenwick A, Addiss DG. Soil-transmitted helminth infections. Lancet. 2018;391(10117):252–65.

    Article  PubMed  Google Scholar 

  9. Gibson AK, Raverty S, Lambourn DM, Huggins J, Magargal SL, Grigg ME. Polyparasitism is associated with increased disease severity in Toxoplasma gondii-infected marine sentinel species. PLoS Negl Trop Dis. 2011;5(5):e1142.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Pullan R, Brooker S. The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? Parasitology. 2008;135(7):783–94.

    Article  CAS  PubMed  Google Scholar 

  11. Supali T, Verweij JJ, Wiria AE, Djuardi Y, Hamid F, Kaisar MM, et al. Polyparasitism and its impact on the immune system. Int J Parasitol. 2010;40(10):1171–6.

    Article  CAS  PubMed  Google Scholar 

  12. Bartsch SM, Hotez PJ, Asti L, Zapf KM, Bottazzi ME, Diemert DJ, et al. The global economic and health burden of human hookworm infection. PLoS Negl Trop Dis. 2016;10(9):e0004922.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Poverty incidence among Filipinos registered at 21.6% in 2015. https://psa.gov.ph/content/poverty-incidence-among-filipinos-registered-216-2015-psa. Accessed 28 December 2019.

  14. Hotez PJ, Ehrenberg JP. Escalating the global fight against neglected tropical diseases through interventions in the Asia Pacific region. Adv Parasitol. 2010;72:31–53.

    Article  PubMed  Google Scholar 

  15. WHO. Number of children (Pre-SAC and SAC) requiring preventive chemotherapy for soil-transmitted helminthiases. https://apps.who.int/neglected_diseases/ntddata/sth/sth.html. Accessed 10 January 2021.

  16. Magalhaes RJS, Salamat MS, Leonardo L, Gray DJ, Carabin H, Halton K, et al. Mapping the risk of soil-transmitted helminthic infections in the Philippines. Plos Neglect Trop D. 2015;9(9):e0003915.

    Article  Google Scholar 

  17. Jex AR, Lim YA, Bethony JM, Hotez PJ, Young ND, Gasser RB. Soil-transmitted helminths of humans in Southeast Asia–towards integrated control. Adv Parasitol. 2011;74:231–65.

    Article  PubMed  Google Scholar 

  18. Belizario VY, Amarillo ME, de Leon WU, de los Reyes AE, Bugayong MG, Macatangay BJ. A comparison of the efficacy of single doses of albendazole, ivermectin, and diethylcarbamazine alone or in combinations against Ascaris and Trichuris spp. Bull World Health Organ. 2003;81(1):35–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Belizario VY, De Leon W, Wambangco MAL, Esparar DG. Baseline assessment of intestinal parasitism in selected public elementary schools in Luzon. Visayas and Mindanao Acta Medica Philippina. 2005;39(2):11–21.

    Google Scholar 

  20. WHO. Review on the Epidemiological Profile of Helminthiases and their Control in the Western Pacific Region, 1997–2008 2008. https://apps.who.int/iris/bitstream/handle/10665/206899/Helminthiases_control_eng.pdf. Accessed 10 March 2019.

  21. Belizario VY Jr, de Leon WU, Lumampao YF, Anastacio MB, Tai CM. Sentinel surveillance of soil-transmitted helminthiasis in selected local government units in the Philippines. Asia Pac J Public Health. 2009;21(1):26–42.

    Article  PubMed  Google Scholar 

  22. Belizario Jr V, Totañes F, Sarmiento R, de Leon W, Ciro R. Monitoring School-based control of intestinal helminthiasis in selected school districts in Cavite, Province, The Philippines. 2013.

  23. Belizario VY, Bersabe MJJ, de los Reyes ABE, de Leon WU. School-based assessment of soil-transmitted helminthiasis and foodborne parasitosis (intestinal fluke infection) in Monkayo, Compostela Valley. Southeast Asian J Trop Med Public Health. 2004;35(Suppl 1):123–39.

    Google Scholar 

  24. Leonardo L, Rivera P, Saniel O, Villacorte E, Lebanan MA, Crisostomo B, et al. A national baseline prevalence survey of schistosomiasis in the Philippines using stratified two-step systematic cluster sampling design. J Trop Med. 2012;2012:936128.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Leonardo LR, Rivera P, Saniel O, Villacorte E, Crisostomo B, Hernandez L, et al. Prevalence survey of schistosomiasis in Mindanao and the Visayas. The Philippines Parasitol Int. 2008;57(3):246–51.

    Article  PubMed  Google Scholar 

  26. Belizario VY Jr, Totanes FI, de Leon WU, Ciro RN, Lumampao YF. Sentinel surveillance of soil-transmitted helminthiasis in preschool-aged and school-aged children in selected local government units in the Philippines: follow-up assessment. Asia Pac J Public Health. 2015;27(2):NP1604-15.

    Article  PubMed  Google Scholar 

  27. WHO. Helminth control in school-age children. A guide for managers of control programmes. 2nd ed. Geneva: World Health Organization; 2011.

    Google Scholar 

  28. Belizario VY, Totanes FI, de Leon WU, Matias KM. School-based control of soil-transmitted helminthiasis in western Visayas, Philippines. Southeast Asian J Trop Med Public Health. 2014;45(3):556–67.

    CAS  PubMed  Google Scholar 

  29. Sanza M, Totanes FI, Chua PL, Belizario VY Jr. Monitoring the impact of a mebendazole mass drug administration initiative for soil-transmitted helminthiasis (STH) control in the Western Visayas Region of the Philippines from 2007 through 2011. Acta Trop. 2013;127(2):112–7.

    Article  CAS  PubMed  Google Scholar 

  30. Belizario VY, Totañes FIG, de Leon WU, Lumampao YF, Ciro RNT. Soil-transmitted helminth and other intestinal parasitic infections among school children in indigenous people communities in Davao del Norte. Philippines Acta Trop. 2011;120(SUPPL. 1):S12–8.

    Article  PubMed  Google Scholar 

  31. Ng JV, Belizario VY Jr, Claveria FG. Determination of soil-transmitted helminth infection and its association with hemoglobin levels among Aeta schoolchildren of Katutubo Village in Planas, Porac. Pampanga Phil Sci Lett. 2014;7:73–80.

    Google Scholar 

  32. Belizario VY Jr, Liwanag HJ, Naig JR, Chua PL, Madamba MI, Dahildahil RO. Parasitological and nutritional status of school-age and preschool-age children in four villages in Southern Leyte, Philippines: Lessons for monitoring the outcome of Community-Led Total Sanitation. Acta Trop. 2015;141(Pt A):16–24.

    Article  PubMed  Google Scholar 

  33. Belizario VY Jr, Ng JV, Amarillo MLE, de los Trinos JPCR, Reyes MR, Fudalan O. High burden of soil-transmitted helminthiases in preschool-age children in masbate: a decade of implementation of the integrated helminth control program in the Philippines. Southeast Asian J Trop Med Public Health. 2016;47(4):667–79.

    Google Scholar 

  34. Ross AG, Papier K, Luceres-Catubig R, Chau TN, Inobaya MT, Ng SK. Poverty, dietary intake, intestinal parasites, and nutritional status among school-age children in the rural Philippines. Trop Med Infect Dis. 2017;2(4):49.

    Article  PubMed Central  Google Scholar 

  35. Papier K, Williams GM, Luceres-Catubig R, Ahmed F, Olveda RM, McManus DP, et al. Childhood malnutrition and parasitic helminth interactions. Clin Infect Dis. 2014;59(2):234–43.

    Article  CAS  PubMed  Google Scholar 

  36. Mationg MLS, Gordon CA, Tallo VL, Olveda RM, Alday PP, Renosa MDC, et al. Status of soil-transmitted helminth infections in schoolchildren in Laguna Province, the Philippines: determined by parasitological and molecular diagnostic techniques. PLoS Negl Trop Dis. 2017;11(11):e0006022.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. de los Trinos JPCR, Belizario VY Jr, Sison OT, Erasmo JN, Te MJ, Modequillo MC. Child development center-based sentinel surveillance of soil-transmitted helminthiases in preschool-age children in selected local government units in the Philippines. Acta Trop. 2019;194:100–5.

    Article  Google Scholar 

  38. Liwanag HJ, Uy J, Battaler R, Gatchalian JR, De La Calzada B, Uy JS, et al. Soil-transmitted helminthiasis and schistosomiasis in children of poor families in Leyte, Philippines: lessons for disease prevention and control. J Trop Pediatr. 2017;63:335–45.

    PubMed  Google Scholar 

  39. Soriano GP, Aquino MGB. Prevalence of soil-transmitted helminths and associate transmission factors among school children in selected barangay in Trece Martires City, Cavite. Int J Med Sci Technol. 2019;9(5):33–8.

    Google Scholar 

  40. Belizario VY Jr, Totañes FIG, de Leon WU, Migrino JR Jr, Macasaet LY. Intestinal capillariasis, western Mindanao, the Philippines. Emerg Infect Dis. 2010;16(4):736.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Belizario V Jr, Chua PL, Liwanag HJ, Naig JR, Erfe JM. Soil-transmitted helminthiases in secondary school students in selected sites in two provinces in the Philippines: policy implications. J Trop Pediatr. 2014;60(4):303–7.

    Article  PubMed  Google Scholar 

  42. Ross AG, Olveda RM, McManus DP, Harn DA, Chy D, Li Y, et al. Risk factors for human helminthiases in rural Philippines. Int J Infect Dis. 2017;54:150–5.

    Article  PubMed  Google Scholar 

  43. Lirio GAC, Labana RV, Bernardo IRA, Bernarte RP, Dungca JZ, Nissapator V. Survey of intestinal parasites including associated risk factos among food vendors and slaughterhouse workers in Metro Manila. Philippines KnE Social Sci. 2018;3(6):493–505.

    Google Scholar 

  44. Delaluna JOC, Flores MJC, Belizario V Jr, Janairo JIB, Sumalapao DEP. Soil-transmitted helminth egg contamination from soil of indigenous communities in selected barangays in Tigaon, Camarines Sur, Philippines. Asia Pac J Trop Med. 2020;13(9):409–14.

    Article  Google Scholar 

  45. Gordon CA, McManus DP, Acosta LP, Olveda RM, Williams GM, Ross AG, et al. Multiplex real-time PCR monitoring of intestinal helminths in humans reveals widespread polyparasitism in Northern Samar, the Philippines. Int J Parasitol. 2015;45(7):477–83.

    Article  CAS  PubMed  Google Scholar 

  46. DOH. Guidebook for a Disease Prevention and Control for Soil-transmitted Helminth Infections and Diarrheal Diseases. 2010.

  47. Gordon CA, Kurscheid J, Jones MK, Gray DJ, McManus DP. Soil-transmitted helminths in tropical Australia and Asia. Trop Med Infect Dis. 2017;2(4):56.

    Article  PubMed Central  Google Scholar 

  48. WHO. Eliminating soil-transmitted helminthiases as a public health problem in children: progress report 2001–2010 and strategic plan 2011–2020. Geneva: World Health Organization; 2012.

    Google Scholar 

  49. WHO. Preventive chemotherapy to control soil-transmitted helminth infections in at-risk population groups. Geneva: World Health Organization; 2017. https://www.who.int/nutrition/publications/guidelines/deworming/en/. Accessed 29 March 2019.

  50. WHO. Preventive chemotherapy in human helminthiasis Geneva: World Health Organization; 2006. https://www.who.int/neglected_diseases/preventive_chemotherapy/pct_manual/en/. Accessed 2 December 2019.

  51. DOH. Administrative Order 2006–0028. Strategic and operational framework for establisng integrated Helminth Control Program; 2006. https://dmas.doh.gov.ph:8083/Rest/GetFile?id=336683. Accessed 4 April 2021.

  52. DOH. Memorandum No. 2016–0212: Guidelines on the Implementation of the Harmonized Schedule and Combined Mss Drug Administration (HSCMDA) for the Prevention and Control of Lymphatic Filariasis. Schistosomiasis, and Soil-Transmitted Hellminths Department of Health; 2016.

  53. WHO. Preventive chemotherapy and transmission of control: Philippines country profile Geneva: World Health Organization; 2006. http://www.who.int/neglected_diseases/preventive_chemotherapy/sth/en/. Accessed 2 December 2019.

  54. Villaverde MC, Gepte, Aguedo Troy D., Baquiran, Raymund S. Performance Assessment of the National Objectives for Health Philippines 2011–2016. Ateneo De Manila University 2016.

  55. Amarillo ML, Belizario VY Jr, Sadiang-Abay JT, Sison SA, Dayag AM. Factors associated with the acceptance of mass drug administration for the elimination of lymphatic filariasis in Agusan del Sur, Philippines. Parasit Vectors. 2008;1(1):14.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Parikh DS, Totanes FI, Tuliao AH, Ciro RN, Macatangay BJ, Belizario VY. Knowledge, attitudes and practices among parents and teachers about soil-transmitted helminthiasis control programs for school children in Guimaras, Philippines. Southeast Asian J Trop Med Public Health. 2013;44(5):744–52.

    PubMed  Google Scholar 

  57. Labana RV, Romero VA, Guinto AM, Caril AN, Untalan KD, Reboa AJC, et al. Gaps and barriers in interventions for the control of soil-transmitted helminthiasis among school-age children in an endemic area of the Philippines: a school-based point-of-view. J Public Health Policy. 2019;40(4):478–97.

    Article  PubMed  Google Scholar 

  58. Lorenzo PJ, Manzanilla DR, Cortel DK, Tangog E. Community perceptions of mass drug administration for soil-transmitted helminthiasis and schistosomiasis in selected schools in the Philippines. Infect Dis Poverty. 2019;8(1):87.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Leonardo LR, Acosta LP, Olveda RM, Aligui GD. Difficulties and strategies in the control of schistosomiasis in the Philippines. Acta Trop. 2002;82(2):295–9.

    Article  PubMed  Google Scholar 

  60. Bacon KM, Shah M, Taylor L, Macatangay BJ, Veldkamp P, Belizario VY Jr. Assessment of a school-based mass treatment for soil-transmitted helminth infections in Capiz, the Philippines. Southeast Asian J Trop Med Public Health. 2012;43(3):589–600.

    PubMed  Google Scholar 

  61. Insetta ER, Soriano AJ, Totanes FI, Macatangay BJ, Belizario VY Jr. Fear of birth defects is a major barrier to soil-transmitted helminth treatment (STH) for pregnant women in the Philippines. PLoS One. 2014;9(2):e85992.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Department of Education Memoradum No. 80, s.2015. Guidelines on the Implementation of the National School Deworming Day (NSDD): Department of Education; 2015. https://www.deped.gov.ph/wp-content/uploads/2015/07/DM_s2015_080.pdf. Accessed 20 December 2019.

  63. Penas JA, de Los Reyes VC, Sucaldito MNL, Ballera JED, Hizon HL, Magpantay RL, et al. Epidemic hysteria following the National School Deworming Day, Zamboanga Peninsula, Philippines, 2015. Western Pac Surveill Response J. 2018;9(4):1–6.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Pareño R. Parents distrust deworming program due to Dengvaxia scare 2018. https://www.philstar.com/nation/2018/01/31/1783182/parents-distrust-deworming-program-due-dengvaxia-scare. Accessed 2 January 2020

  65. Fatima K, Syed NI. Dengvaxia controversy: impact on vaccine hesitancy. J Glob Health. 2018;8(2):010312.

    Article  PubMed  Google Scholar 

  66. DOH. Department Circular No. 2020–0302: Delivery of Routine Deworming Services under the Integrated Helminth Control Program (IHCP) during the COVID-19 pandemic 2020. https://dmas.doh.gov.ph:8083/Rest/GetFile?id=655678. Accessed 27 January 2021.

  67. Water supply and sanitation in the Philippines: turning finance into service in the future: World Bank Group; 2015. https://www.wsp.org/sites/wsp/files/publications/WSP-Philippines-WSS-Turning-Finance-into-Service-for-the-Future.pdf. Accessed 10 February 2020.

  68. DOH. Guidebook for Community-Led Total Sanitation. Department of Health (DOH) Philippines; 2010.

  69. DOH. Guidebook for a Zero Open Defecation Program. In: Philippines DoHD, editor. San Lazaro Compound, Sta. Cruz Manila; 2010.

  70. Philippines National Demographic Health Survey 2017: Key Indicators Report. Quezon City, Philippines, and Rockville, Maryland, USA: PSA and ICF: Philippine Statistics Authority (PSA) and ICF; 2018.

  71. Expanding Access to Improved Sanitation for the Poor, Insights from the Philippines. International Finance Corporation, World Bank Group; 2017

  72. Bank TW. Economic Assessment of Sanitation Interventions in the Philippines. 2011.

  73. Community Led-Total Sanition - Philippines 2016. https://www.communityledtotalsanitation.org/country/philippines. Accessed 8 April 2019.

  74. DOH. Code Sanitation of the Philippines (Presidential Decree No. 856): Department of Health Philippines; 1976, reprinted in 1998. https://www.doh.gov.ph/node/5731. Accessed 20 March 2019.

  75. Implementation of Water, Sanitation and Hygiene (WASH) in Public Schools: A citizen participatory Audit: Commision on Audit; 2017. https://www.coa.gov.ph/phocadownloadpap/userupload/citizen-participatory-audit-report/WASH-Project/WASH_Program_CDO.pdf. Accessed 10 January 2020.

  76. Mohini Venkatesh SS, Nanditha Gopal. Operation and Maintenance Finacing for School WASH Facilities in the Philippines. Save the Children; 2016.

  77. Haver J, Bethany A. Caruso, Anna Ellis, Murat Sahin, Jonathan Michael Villasenor, Karen L. Andes and Matthew C. Freeman. ‘WASH in Schools Empowers Girls’ Education in Masbate Province and Metro Manila, Philippines: An assessment of menstrual hygiene management in schools’. United Nations Children’s Fund, New York; November 2013.

  78. Department of Education Order No. 65 s. 2009, Implementation of Essential Health Care Program. 2009.

  79. Department Education Order 10, S. 2016 - Policy and guidelines for the comprehensive Water, Sanitation, and Hygiene in Schools (WINS) Program 2016.

  80. Monse B, Naliponguit E, Belizario V, Benzian H, van Helderman WP. Essential health care package for children–the “Fit for School” program in the Philippines. Int Dent J. 2010;60(2):85–93.

    PubMed  Google Scholar 

  81. Owada K, Nielsen M, Lau CL, Yakob L, Clements ACA, Leonardo L, et al. Functional illiteracy burden in soil-transmitted helminth (STH) endemic regions of the Philippines: an ecological study and geographical prediction for 2017. PLoS Negl Trop Dis. 2019;13(6):e0007494.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Moser W, Schindler C, Keiser J. Efficacy of recommended drugs against soil transmitted helminths: systematic review and network meta-analysis. BMJ. 2017;358:j4307.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Speich B, Moser W, Ali SM, Ame SM, Albonico M, Hattendorf J, et al. Efficacy and reinfection with soil-transmitted helminths 18-weeks post-treatment with albendazole-ivermectin, albendazole-mebendazole, albendazole-oxantel pamoate and mebendazole. Parasit Vectors. 2016;9:123.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  84. Anderson RM, Truscott JE, Pullan RL, Brooker SJ, Hollingsworth TD. How effective is school-based deworming for the community-wide control of soil-transmitted helminths? PLoS Negl Trop Dis. 2013;7(2):e2027.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Farrell SH, Coffeng LE, Truscott JE, Werkman M, Toor J, de Vlas SJ, et al. Investigating the effectiveness of current and modified world health organization guidelines for the control of soil-transmitted helminth infections. Clin Infect Dis. 2018;66(suppl_4):S253–9.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Truscott JE, Hollingsworth TD, Brooker SJ, Anderson RM. Can chemotherapy alone eliminate the transmission of soil transmitted helminths? Parasit Vectors. 2014;7:266.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Clarke NE, Clements AC, Doi SA, Wang D, Campbell SJ, Gray D, et al. Differential effect of mass deworming and targeted deworming for soil-transmitted helminth control in children: a systematic review and meta-analysis. Lancet. 2017;389(10066):287–97.

    Article  PubMed  Google Scholar 

  88. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030 Geneva: World Health Organization 2020. https://www.who.int/neglected_diseases/resources/who-ucn-ntd-2020.01/en/. Accessed 29 January 2021.

  89. NTD Modelling Consortium. The potential impact of programmes interruptions due to COVID-19 on 7 neglected tropical diseases: a modelling-based analysis. Meeting report: Gates Open Research; 2020. https://gatesopenresearch.org/documents/4-115. Accessed 27 January 2021.

  90. Bieri FA, Gray DJ, Williams GM, Raso G, Li YS, Yuan L, et al. Health-education package to prevent worm infections in Chinese schoolchildren. N Engl J Med. 2013;368(17):1603–12.

    Article  CAS  PubMed  Google Scholar 

  91. Mationg MLS, Williams GM, Tallo VL, Olveda RM, Aung E, Alday P, et al. Determining the impact of a school-based health education package for prevention of intestinal worm infections in the Philippines: protocol for a cluster randomized intervention trial. JMIR Res Protoc. 2020;9(6):e18419.

    Article  PubMed  PubMed Central  Google Scholar 

  92. Hesham M. Al-Mekhlafi YALL, Norhayati Moktar, Romano Ngui. Chapter 11 Soil-transmitted helminths: the neglected parasites. parasites and their vectors. 2013.

  93. Hong ST, Chai JY, Choi MH, Huh S, Rim HJ, Lee SH. A successful experience of soil-transmitted helminth control in the Republic of Korea. Korean J Parasitol. 2006;44(3):177–85.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Ohta N, Waikagul J. Disease burden and epidemiology of soil-transmitted helminthiases and schistosomiasis in Asia: the Japanese perspective. Trends Parasitol. 2007;23(1):30–5.

    Article  PubMed  Google Scholar 

  95. Cabrera BD, Arambulo PV 3rd, Portillo GP. Ascariasis control and/or eradication in a rural community in the Philippines. Southeast Asian J Trop Med Public Health. 1975;6(4):510–8.

    CAS  PubMed  Google Scholar 

  96. Carney WP, Banzon T, de Veyra V, Daña E, Cross JH. Intestinal parasites of man in northern Bohol, Philippines, with emphasis on schistosomiasis. Southeast Asian J Trop Med Public Health. 1980;11(4):473–9.

    CAS  PubMed  Google Scholar 

  97. Cabrera B, Cruz A. A comparative study on the effect of mass treatment of the entire community and selective treatment of children on the total prevalence of soil-transmitted helminthiases in two communities in Mindoro, Philippines. Collected Papers Control Soil Transmitted Helminthiases. 1983;2:226–87.

    Google Scholar 

  98. Oberst RB, Alquiza LM. Survey of intestinal parasites on Palawan, Philippines. Southeast Asian J Trop Med Public Health. 1987;18(18):197–201.

    CAS  PubMed  Google Scholar 

  99. Carney WP, Vergel AG, Pagaraan I, Mercado A, Cross JH. Intestinal parasites of man in Agusan Del Norte, Philippines with emphasis on schistosomiasis and capillariasis. Phil J Microbiol Infect Dis. 1987;16(1):5–9.

    Google Scholar 

  100. Cross JH, Zaraspe G, Alquizia L, Ranoa C. Intestinal parasites in some patients seen at San Lazaro Hospital, Manila, Philippines. Philippine J Microbiol Infect Dis. 1989;18(1):25–7.

    Google Scholar 

  101. Chigusa Y, Kirinoki M, Yokoi H, Kawai S, Matsuda H, Yasuraoka K, et al. A survey of intestinal parasitic infections in San Narciso, Victoria, Oriental Mindoro, Philippines. Japan J Trop Med Hygiene. 1997;25(1):7–9.

    Article  Google Scholar 

  102. Lee KJ, Ahn YK, Yong TS. A small-scale survey of intestinal parasite infections among children and adolescents in Legaspi city, the Philippines. Korean J Parasitol. 2000;38(3):183–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Yamamoto R, Nagai N, Kawabata M, Leon WU, Ninomiya R, Koizumi N. Effect of intestinal helminthiasis on nutritional status of schoolchildren. Southeast Asian J Trop Med Public Health. 2000;31(4):755–61.

    CAS  PubMed  Google Scholar 

  104. Olson CL, Acosta LP, Hochberg NS, Olveda RM, Jiz M, McGarvey ST, et al. Anemia of inflammation is related to cognitive impairment among children in Leyte, the Philippines. Plos Neglect Trop D. 2009;3(10):e533.

    Article  Google Scholar 

  105. Kim B-J, Ock M-S, Chung D-I, Yong T-S, Lee K-J. The intestinal parasite infection status of inhabitants in the Roxas city, the Philippines. Korean J Parasitol. 2003;41(2):113–5.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Baldo ET, Belizario VY, De Leon WU, Kong H-H, Chung D-I. Infection status of intestinal parasites in children living in residential institutions in Metro Manila, the Philippines. Korean J Parasitol. 2004;42(2):67.

    Article  PubMed  PubMed Central  Google Scholar 

  107. Cauyan GA, Andaman DE, Maricar S. Prevalence of intestinal parasites among schoolchildren in a coastal rural area of Maragondon, Cavite, southern Luzon. Philippines Acta Manilana. 2008;56:43–9.

    Google Scholar 

  108. Ezeamama AE, Friedman JF, Acosta LP, Bellinger DC, Langdon GC, Manalo DL, et al. Helminth infection and cognitive impairment among Filipino children. Am J Trop Med Hyg. 2005;72(5):540–8.

    Article  PubMed  Google Scholar 

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UBS Optimus Foundation. National Health and Medical Research Council (Australia).

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  1. Donald P. McManus and Darren J. Gray—Joint Senior Author

Authors and Affiliations

  1. Department of Global Health, Research School of Population Health, The Australian National University, Building 62 Mills Rd, Acton ACT, Canberra, 2601, Australia

    Mary Lorraine S. Mationg & Darren J. Gray

  2. Department of Epidemiology and Biostatistics, Research Institute for Tropical Medicine, Manila, Philippines

    Mary Lorraine S. Mationg & Veronica L. Tallo

  3. School of Public Health, University of Queensland, Brisbane, Australia

    Gail M. Williams

  4. Molecular Parasitology Laboratory, Infectious Diseases Division, QIMR Berghofer Medical Research Institute, Brisbane, Australia

    Catherine A. Gordon & Donald P. McManus

  5. Faculty of Health Sciences, Curtin University, Perth, Australia

    Archie C. A. Clements

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DJG and MLM conceived the idea; MLM wrote the first draft and all authors (MLM, DJG, VLT, CAG GMW, AC, DPM) contributed to the drafting of manuscript. All authors read and approved the final manuscript.

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Mationg, M.L.S., Tallo, V.L., Williams, G.M. et al. The control of soil-transmitted helminthiases in the Philippines: the story continues. Infect Dis Poverty 10, 85 (2021). https://doi.org/10.1186/s40249-021-00870-z

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Infectious Diseases of Poverty

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