Soil-transmitted helminth (STH) infection has long been an important public health problem in the Philippines.In this review, we describe the current status of STH infection there and highlight control measures to reduce STH burden.
A nationwide STH mass drug administration (MDA) program was launched in 2006, but the overall prevalence of STH in the Philippines remains high, ranging from 24.9% to 97.4%.The continued increase in prevalence may be due to challenges associated with MDA implementation, including a lack of awareness of the importance of regular treatment, misunderstandings about MDA strategies, lack of confidence in the medications used, fear of adverse events, and general distrust of government programs.Existing water, sanitation and hygiene (WASH) programs are already in place in communities [e.g., community-led comprehensive sanitation (CLTS) programs that provide toilets and subsidize toilet construction] and schools [e.g., school WASH (WINS) plan], but ongoing implementation is required to achieve the desired results.Despite the widespread teaching of WASH in schools, the integration of STH as a disease and a community issue in the current public elementary curriculum remains inadequate.Ongoing evaluation will be required for the Integrated Helminth Control Program (IHCP) currently in place in the country, which focuses on improving sanitation and hygiene, health education and preventive chemotherapy.The sustainability of the program remains a challenge.
Despite major efforts to control STH infection in the Philippines over the past two decades, persistently high STH prevalence has been reported across the country, possibly due to suboptimal MDA coverage and limitations of WASH and health education programs. .Sustainable delivery of an integrated control approach will continue to play a key role in controlling and eliminating STH in the Philippines.
Soil-transmitted helminth (STH) infections remain a serious public health problem worldwide, with an estimated infection of more than 1.5 billion people [1].STH affects poor communities characterized by poor access to adequate water, sanitation and hygiene (WASH) [2, 3]; and is highly prevalent in low-income countries, with most infections occurring in parts of Asia, Africa, and Latin America [4].Preschool children aged 2 to 4 years (PSAC) and school children aged 5 to 12 years (SAC) were the most susceptible, with the highest prevalence and intensity of infection.Available data suggest that more than 267.5 million PSACs and more than 568.7 million SACs reside in areas with severe STH transmission and require preventive chemotherapy [5].The global burden of STH is estimated to be 19.7-3.3 million disability-adjusted life years (DALYs) [6, 7].
STH infection may lead to nutritional deficiencies and impaired physical and cognitive development, especially in children [8].High-intensity STH infection exacerbates morbidity [9,10,11].Polyparasitism (infection with multiple parasites) has also been shown to be associated with higher mortality and increased susceptibility to other infections [10, 11].The adverse effects of these infections can affect not only health but also economic productivity [8, 12].
The Philippines is a low- and middle-income country.In 2015, about 21.6% of the 100.98 million Philippine population lived below the national poverty line [13].It also has some of the highest prevalence of STH in Southeast Asia [14].2019 data from the WHO Preventive Chemotherapy Database indicate that approximately 45 million children are at risk of infection requiring medical treatment [15].
Although several large initiatives have been initiated to control or interrupt transmission, STH remains highly prevalent in the Philippines [16].In this article, we provide an overview of the current status of STH infection in the Philippines; highlight past and current ongoing control efforts, document the challenges and difficulties of program implementation, assess its impact on reducing STH burden, and provide possible perspectives for the control of intestinal worms .The availability of this information can provide a basis for planning and implementing a sustainable STH control program in the country.
This review focuses on the four most common STH parasites – roundworm, Trichuris trichiura, Necator americanus and Ancylostoma duodenale.Although Ancylostoma ceylanicum is emerging as an important zoonotic hookworm species in Southeast Asia, limited information is currently available in the Philippines and will not be discussed here.
Although this is not a systematic review, the methodology used for the literature review is as follows.We searched for relevant studies reporting the prevalence of STH in the Philippines using online databases of PubMed, Scopus, ProQuest, and Google Scholar.The following words were used as keywords in the search: (“Helminthiases” or soil-borne worms” or “STH” or “Ascaris lumbricoides” or “Trichuris trichiura” or “Ancylostoma spp.” or “Necator americanus” or “Roundworm” or “Whichworm” or “Hookworm”) and (“Epidemiology”) and (“Philippines”). There is no restriction on the year of publication. Articles identified by search criteria were initially screened by title and abstract content, those not investigated for at least three Articles with prevalence or intensity of one of the STHs were excluded. Full-text screening included observational (cross-sectional, case-control, longitudinal/cohort) studies or controlled trials reporting baseline prevalence. Data extraction included study area, study year , year of study publication, study type (cross-sectional, case-control, or longitudinal/cohort), sample size, study population, prevalence and intensity of each STH, and method used for diagnosis.
Based on literature searches, a total of 1421 records were identified by database searches [PubMed (n = 322); Scopes (n = 13); ProQuest (n = 151) and Google Scholar (n = 935)].A total of 48 papers were screened based on the title review, 6 papers were excluded, and a total of 42 papers were finally included in the qualitative synthesis (Figure 1).
Since the 1970s, numerous studies have been conducted in the Philippines to determine the prevalence and intensity of STH infection.Table 1 shows a summary of the identified studies.Differences in the diagnostic methods of STH among these studies were evident over time, with the formalin ether concentration (FEC) method frequently used in the early days (1970-1998).However, the Kato-Katz (KK) technique has been used increasingly in subsequent years and is used as the primary diagnostic method for monitoring STH control procedures in national surveys.
STH infection has been and remains a significant public health problem in the Philippines, as shown by studies conducted from the 1970s to 2018.The epidemiological pattern of STH infection and its prevalence are comparable to those reported in other endemic countries of the world, with the highest prevalence of infection recorded in PSAC and SAC [17].These age groups are at greater risk because these children are often exposed to STH in outdoor settings.
Historically, prior to the implementation of the Department of Health’s Integrated Helminth Control Program (IHCP), the prevalence of any STH infection and severe infection in children aged 1-12 years ranged from 48.6-66.8% to 9.9-67.4%, respectively.
STH data from the National Schistosomiasis Survey of all ages from 2005 to 2008 showed that STH infection was widespread in the three main geographic regions of the country, with A. lumbricoides and T. trichiura being particularly prevalent in the Visayas [16] .
In 2009, follow-up assessments of the 2004 [20] and 2006 SAC [21] National STH Prevalence Surveys were conducted to assess the impact of IHCP [26].The prevalence of any STH was 43.7% in PSAC (66% in 2004 survey) and 44.7% in SAC (54% in 2006 survey) [26].These figures are significantly lower than those reported in the previous two surveys.The high-intensity STH infection rate was 22.4% in PSAC in 2009 (not comparable to the 2004 survey because the overall prevalence of severe infections was not reported) and 19.7% in SAC (compared with 23.1% in the 2006 survey), a 14% reduction [ 26].Despite the apparent decline in infection prevalence, the estimated prevalence of STH in PSAC and SAC populations has not met the WHO-defined 2020 target of a cumulative prevalence of less than 20% and a severe STH infection rate of less than 1% to demonstrate morbidity control [27, 48].
Other studies using parasitological surveys conducted at multiple time points (2006-2011) to monitor the impact of school MDA in SAC showed similar trends [22, 28, 29].The results of these surveys showed that STH prevalence decreased after several rounds of MDA; however, any STH (range, 44.3% to 47.7%) and severe infection (range, 14.5% to 24.6%) reported in follow-up surveys The overall prevalence of disease remains high [22, 28, 29], again indicating that the prevalence has not yet fallen to the WHO-defined incidence control target level (Table 1).
Data from other studies following the introduction of IHCP in the Philippines in 2007-2018 showed persistently high prevalence of STH in PSAC and SAC (Table 1) [30,31,32,33,34,35,36,37,38, 39].The prevalence of any STH reported in these studies ranged from 24.9% to 97.4% (by KK), and the prevalence of moderate to severe infections ranged from 5.9% to 82.6%.A. lumbricoides and T. trichiura remain the most prevalent STHs, with prevalence ranging from 15.8-84.1% to 7.4-94.4%, respectively, while hookworms tend to have lower prevalence, ranging from 1.2% to 25.3% [30,31, 32,33,34,35,36,37,38,39] (Table 1).However, in 2011, a study using molecular diagnostic quantitative real-time polymerase chain reaction (qPCR) showed a prevalence of hookworm (Ancylostoma spp.) of 48.1% [45].Co-infection of individuals with A. lumbricoides and T. trichiura has also been frequently observed in several studies [26, 31, 33, 36, 45].
The KK method is recommended by WHO for its ease of use in the field and low cost [46], mainly for evaluating government treatment plans for STH control.However, differences in the prevalence of STH have been reported between KK and other diagnostics.In a 2014 study in Laguna Province, any STH infection (33.8% for KK vs 78.3% for qPCR), A. lumbricoides (20.5% KK vs 60.8% for qPCR) and T. trichiura (KK 23.6% vs 38.8% for qPCR).There is also hookworm infection [6.8% prevalence; includes Ancylostoma spp.(4.6%) and N. americana (2.2%)] were detected using qPCR and were judged negative by KK [36].The true prevalence of hookworm infection may be greatly underestimated because rapid lysis of hookworm eggs requires rapid turnaround for KK slide preparation and reading [36,45,47], a process that is often difficult to achieve under field conditions.Furthermore, the eggs of hookworm species are morphologically indistinguishable, which poses a further challenge for correct identification [45].
The main strategy for STH control advocated by WHO focuses on mass prophylactic chemotherapy with albendazole or mebendazole in high-risk groups, with the goal of treating at least 75% of PSAC and SAC by 2020 [48].Before the recent launch of the Neglected Tropical Diseases (NTDs) Roadmap to 2030, WHO recommended that PSAC, SAC and women of reproductive age (15-49 years, including those in the second and third trimesters) receive usual care [49].In addition, this guideline includes young children (12-23 months) and adolescent girls (10-19 years) [49], but excludes previous recommendations for the treatment of high-risk occupational adults [50].WHO recommends annual MDA for young children, PSAC, SAC, adolescent girls, and women of reproductive age in areas with STH prevalence between 20% and 50%, or semiannually if prevalence is above 50%.For pregnant women, treatment intervals have not been established [49].In addition to preventive chemotherapy, WHO has emphasized water, sanitation and hygiene (WASH) as an important component of STH control [48, 49].
The IHCP was launched in 2006 to provide policy guidance for the control of STH and other helminth infections [20, 51].This project follows the WHO-approved STH control strategy, with albendazole or mebendazole chemotherapy as the main strategy for STH control, targeting children aged 1-12 years and other high-risk groups such as pregnant women, adolescent women, farmers, food handlers and indigenous peoples.Control programmes are also complemented by the installation of water and sanitation facilities as well as health promotion and education methods [20, 46].
The semi-annual MDA of PSAC is carried out mainly by local barangay (village) health units, trained barangay health workers and day care workers in community settings as Garantisadong Pambata or “Healthy Children” (a package providing project) of PSAC’s Health Services), while SAC’s MDA is overseen and implemented by the Department of Education (DepEd) [20].MDA in public elementary schools is administered by teachers under the guidance of health workers during the first and third quarters of each school year [20].In 2016, the Ministry of Health issued new guidelines to include deworming in secondary schools (children under 18) [52].
The first national semiannual MDA was conducted in children aged 1-12 years in 2006 [20] and reported deworming coverage of 82.8% of 6.9 million PSACs and 31.5% of 6.3 million SACs [53].However, MDA deworming coverage declined substantially from 2009 to 2014 (range 59.5% to 73.9%), a figure consistently below the WHO-recommended benchmark of 75% [54].Low deworming coverage may be due to lack of awareness of the importance of routine treatment [55], misunderstanding of MDA strategies [56, 57], lack of confidence in the drugs used [58], and fear of adverse events [55, 56, 58, 59, 60].Fear of birth defects has been reported as one reason pregnant women refuse STH treatment [61].In addition, supply and logistical issues of MDA drugs have been identified as major deficiencies encountered in the implementation of MDA nationwide [54].
In 2015, the DOH partnered with DepEd to host the inaugural National School Deworming Day (NSDD), which aims to expel the approximately 16 million SACs (grades 1 to 6) enrolled in all public elementary schools in one day [62].This school-based initiative resulted in a national deworming coverage rate of 81%, higher than in previous years [54].However, false information circulating in the community about child deworming deaths and the use of expired drugs has caused massive hysteria and panic, leading to increased reports of adverse events after MDA (AEFMDA) in the Zamboanga Peninsula, Mindanao [63].However, a case-control study showed that being an AEFMDA case was associated with no previous history of deworming [63].
In 2017, the Ministry of Health introduced a new dengue vaccine and provided it to around 800,000 schoolchildren.The availability of this vaccine has raised significant safety concerns and has led to increased mistrust in DOH programs, including the MDA program [64, 65].As a result, pest coverage decreased from 81% and 73% of PSAC and SAC in 2017 to 63% and 52% in 2018, and to 60% and 59% in 2019 [15].
In addition, in light of the current global COVID-19 (coronavirus disease 2019) pandemic, the Ministry of Health has issued Departmental Memorandum No. 2020-0260 or Interim Guidance for Integrated Helminth Control Plans and Schistosomiasis Control and Elimination Plans During the COVID-19 Pandemic 》” June 23, 2020, provides for MDA to be suspended until further notice. Due to school closures, the community is routinely deworming children ages 1-18, distributing medication through door-to-door visits or fixed locations, while maintaining physical distancing and targeting COVID-19 -19 appropriate infection prevention and control measures [66]. However, restrictions on the movement of people and public anxiety due to the COVID-19 pandemic may lead to lower treatment coverage.
WASH is one of the key interventions for STH control outlined by the IHCP [20, 46].This is a programme involving several government agencies, including the Ministry of Health, Ministry of Home Affairs and Local Government (DILG), Local Government Units (LGU) and Ministry of Education.The community’s WASH program includes the provision of safe water, led by local government departments, with the support of DILG [67], and sanitation improvements implemented by DOH with the help of local government departments, providing toilets and subsidies for toilet construction [68, 69] ].Meanwhile, the WASH program in public primary schools is overseen by the Ministry of Education in cooperation with the Ministry of Health.
The latest data from the Philippine Statistics Authority (PSA) 2017 National Population Health Survey shows that 95% of Filipino households obtain drinking water from improved water sources, with the largest proportion (43%) from bottled water and only 26% from piped sources[70] obtain it.A quarter of Filipino households still use unsatisfactory sanitation facilities [70]; approximately 4.5% of the population defecate openly, a practice twice as high in rural areas (6%) as in urban areas (3%) [70 ].
Other reports suggest that providing sanitation facilities alone does not guarantee their use, nor does it improve sanitation and hygiene practices [32, 68, 69].Among households without toilets, the most frequently cited reasons for not improving sanitation included technical barriers (ie, lack of space in the home for a toilet or a septic tank around the home, and other geographic factors such as soil conditions and proximity to waterways), Land ownership and lack of funding [71, 72].
In 2007, the Philippine Department of Health adopted a community-led total sanitation (CLTS) approach through the East Asia Sustainable Health Development Program [68, 73].CLTS is a concept of total hygiene that includes a range of behaviours such as stopping open defecation, ensuring everyone uses sanitary toilets, frequent and proper hand washing, sanitation of food and water, safe disposal of animals and livestock waste, and the creation and maintenance of Clean and safe environment [68, 69].To ensure the sustainability of the CLTS approach, village ODF status should be continuously monitored even after CLTS activities are terminated.However, several studies have shown a high prevalence of STH in communities that have achieved ODF status after the implementation of CLTS [32, 33].This may be due to lack of use of sanitation facilities, possible resumption of open defecation, and low MDA coverage [32].
WASH programs implemented in schools follow policies published by the DOH and DepEd.In 1998, the Department of Health issued the Philippine Health Code School Health and Health Services Implementation Rules and Regulations (IRR) (PD No. 856) [74].This IRR sets out the rules and regulations for school hygiene and satisfactory sanitation, including toilets, water supplies, and the maintenance and upkeep of these facilities [74].However, evaluations of the Ministry of Education’s implementation of the program in selected provinces indicate that guidelines are not strictly enforced and budgetary support is insufficient [57, 75, 76, 77].Therefore, monitoring and evaluation remain critical to ensuring the sustainability of the Ministry of Education’s implementation of the WASH programme.
In addition, to institutionalize good health habits for students, the Ministry of Education has issued Departmental Order (DO) No. 56, Article 56.2009 entitled “Immediately constructing water and handwashing facilities in all schools to prevent Influenza A (H1N1)” and DO No. 65, s. 2009 entitled “Essential Health Care Program (EHCP) for School Children” [78, 79] .While the first program was designed to prevent the spread of H1N1, this is also related to STH control.The latter follows a school-appropriate approach and focuses on three evidence-based school health interventions: handwashing with soap, brushing with fluoridated toothpaste as a daily group activity, and STH’s biannual MDA [78, 80].In 2016, EHCP is now integrated into the WASH In Schools (WINS) program.It expanded to include provision of water, sanitation, food handling and preparation, hygiene improvements (eg, menstrual hygiene management), deworming, and health education [79].
Although in general WASH has been included in primary school curricula [79], the inclusion of STH infection as a disease and public health problem is still lacking.A recent study in selected public primary schools in Cagayan province reported that WASH-related health education is applicable to all students regardless of grade level and school type, and it is also integrated into multiple subjects and widely used. Outreach (ie, materials promoting health education are presented visually in classrooms, WASH areas, and throughout the school) [57].However, the same study suggested that teachers need to be trained in STH and deworming to deepen their understanding of parasites and better understand STH as a public health issue, including: topics related to STH transmission, risk of infection, risk of infection will drive Post-worm open defecation and reinfection patterns were introduced into the school curriculum [57].
Other studies have also demonstrated a relationship between health education and treatment acceptance [56, 60] suggesting that enhanced health education and promotion (to improve STH knowledge and correct MDA misconceptions about treatment and benefits) can increase MDA treatment participation and acceptance [56] , 60].
Furthermore, the importance of health education in influencing good hygiene-related behaviours has been identified as one of the key components of WASH implementation [33, 60].As previous studies have shown, open defecation is not necessarily due to lack of toilet access [32, 33].Factors such as open defecation habits and lack of use of sanitation facilities may influence open defecation outcomes [68, 69].In another study, poor sanitation was associated with a higher risk of functional illiteracy among SACs in the Visayas [81].Therefore, the inclusion of health education and promotion strategies aimed at improving bowel and hygiene habits, as well as the acceptance and appropriate use of these health infrastructures, needs to be incorporated to maintain uptake of WASH interventions.
Data collected over the past two decades indicate that the prevalence and intensity of STH infection among children under the age of 12 in the Philippines remains high, despite the various efforts of the Philippine government.Barriers and challenges to MDA participation and treatment adherence need to be identified to ensure high MDA coverage.It is also worth considering the efficacy of two drugs currently used in the STH control program (albendazole and mebendazole), as alarmingly high T. trichiura infections have been reported in some recent studies in the Philippines [33, 34, 42].The two drugs were reported to be less effective against T. trichiura, with combined cure rates of 30.7% and 42.1% for albendazole and mebendazole, respectively, and 49.9% and 66.0% reduction in spawning [82].Given that the two drugs have minimal therapeutic effects, this could have important implications in areas where Trichomonas are endemic.Chemotherapy was effective in reducing infection levels and reducing the helminth burden in infected individuals below the incidence threshold, but efficacy varied among STH species.Notably, existing drugs do not prevent reinfection, which can occur immediately after treatment.Therefore, new drugs and drug combination strategies may be required in the future [83].
Currently, there is no mandatory MDA treatment for adults in the Philippines.IHCP focuses only on children 1-18 years of age, as well as selective deworming of other high-risk groups such as pregnant women, adolescent women, farmers, food handlers, and indigenous populations [46].However, recent mathematical models [84,85,86] and systematic reviews and meta-analyses [87] suggest that community-wide expansion of deworming programmes to cover all age groups may reduce the prevalence of STH in high-risk populations.- Groups of at-risk school children.However, scaling up MDA from targeted drug administration to community-wide may have important economic implications for STH control programs because of the need for increased resources.Nonetheless, an effective mass treatment campaign for lymphatic filariasis in the Philippines underscores the feasibility of providing community-wide treatment [52].
A resurgence of STH infections is expected as school-based MDA campaigns against STH across the Philippines have ceased due to the ongoing COVID-19 pandemic.Recent mathematical models suggest that delays in MDA in high STH-endemic settings could imply the goal of eliminating STH as a public health problem (EPHP) by 2030 (defined as achieving < 2% prevalence of moderate-to-high-intensity infections in SAC [88] ]) may not be achievable, although mitigation strategies to make up for missed MDA rounds (ie higher MDA coverage, >75%) would be beneficial [89].Therefore, more sustainable control strategies to increase MDA are urgently needed to combat STH infection in the Philippines.
In addition to MDA, transmission disruption requires changes in hygiene behaviors, access to safe water, and improved sanitation through effective WASH and CLTS programs.Somewhat frustratingly, however, there are reports of underutilized sanitation facilities provided by local governments in some communities, reflecting the challenges in WASH implementation [68, 69, 71, 72].In addition, high STH prevalence was reported in communities that achieved ODF status after implementation of CLTS due to resumption of open defecation behavior and low MDA coverage [32].Building knowledge and awareness of STH and improving hygiene practices are important ways to reduce an individual’s risk of infection and are essentially low-cost supplements to MDA and WASH programs.
Health education provided in schools may help to strengthen and improve general knowledge and awareness of STH among students and parents, including the perceived benefits of deworming.The “Magic Glasses” program is an example of a recently very successful health education intervention in schools.This is a short cartoon intervention designed to educate students about STH infection and prevention, providing proof-of-principle that health education can improve knowledge and influence behavior related to STH infection [90].The procedure was first used in Chinese primary school students in Hunan Province, and the incidence of STH infection was reduced by 50% in intervention schools compared with control schools (odds ratio = 0.5, 95% confidence interval: 0.35-0.7, P < 0.0001).90].This has been adapted and rigorously tested in the Philippines [91] and Vietnam; and is currently being developed for the lower Mekong region, including its adaptation to the carcinogenic Opisthorchis liver fluke infection.Experience in several Asian countries, notably Japan, Korea and Taiwan Province of China, has shown that through MDA, proper sanitation and hygiene education as part of national control plans, through school-based approaches and triangular Collaboration to eliminate STH infection is possible with institutions, NGOs and scientific experts [92,93,94].
There are several projects in the Philippines that incorporate STH controls, such as WASH/EHCP or WINS implemented in schools, and CLTS implemented in communities.However, for greater sustainability opportunities, greater coordination among the organizations implementing the program is required.Therefore, decentralized plans and multi-party efforts like the Philippines’ for STH control can only succeed with the long-term cooperation, cooperation and support of the local government.Government support for the procurement and distribution of medicines and prioritization of other components of control plans, such as activities to improve sanitation and health education, are needed to accelerate the achievement of the 2030 EPHP targets [88].In the face of the challenges of the COVID-19 pandemic, these activities need to continue and be integrated with ongoing COVID-19 prevention efforts.Otherwise, compromising an already challenged STH control program could have serious long-term public health consequences.
For nearly two decades, the Philippines has made great efforts to control STH infection.Nonetheless, the reported prevalence of STH has remained high nationwide, possibly due to suboptimal MDA coverage and limitations of WASH and health education programs.National governments should now consider strengthening school-based MDAs and expanding community-wide MDAs; closely monitoring drug effectiveness during MDA events and investigating the development and use of new antihelminthic drugs or drug combinations; and sustainable provision of WASH and health education as a comprehensive attack method for future STH control in the Philippines.
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Post time: Mar-15-2022