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Infection rate of Schistosoma japonicum in the snail Oncomelania hupensis quadrasi in endemic villages in the Philippines: Need for snail surveillance technique

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Schistosomiasis japonica is one of seven NTDs endemic in the Philippines that continues to threaten public health in the country. The causative agent, the blood fluke Schistosoma japonicum, uses an amphibious snail Oncomelania hupensis quadrasi which can harbor larval stages that multiply asexually, eventually producing the infective cercariae which are shed into the water. Contamination of freshwater bodies inhabited by the snail intermediate host occurs through release of human and animal feces containing S. japonicum eggs. Miracidia hatching from these eggs subsequently infect the snails that inhabit these water bodies. The degree of fecal contamination can vary across snail sites and influences snail infection rates in these sites. In this study, conventional malacological surveys using intensive manual search for snails were conducted from 2015 to 2016 in seven selected endemic provinces, namely Leyte and Bohol in the Visayas and Surigao del Norte, Agusan del Sur, Bukidnon, Lanao del Norte and Compostela Valley in Mindanao. A total of 6,279 O. hupensis quadrasi snails were collected from 38 snail sites. The municipality of Trento in Agusan del Sur recorded the highest number of snail sites (7) that yielded O. hupensis quadrasi snails while only one snail site was found positive for O. hupensis quadrasi snails in Kapatagan in Lanao del Norte and Talibon in Bohol. Alegria in Surigao del Norte yielded the highest number of snail sites (5) that were found to harbor snails positive for S. japonicum infection. The snail infection rates in this municipality ranged from 0.43% to 14.71%. None of the snails collected from Talibon in Bohol was infected. Bohol is the only province among the 28 schistosomiasis-endemic provinces which has reached near elimination status. Snail infection rates were found to vary considerably across snail sites, which could be due to the degree of fecal contamination of the snail sites and their connectivity to water that can serve as contamination source.
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Tropical Biomedicine 36(2): 402–411 (2019)
Infection rate of Schistosoma japonicum in the snail
Oncomelania hupensis quadrasi in endemic villages in
the Philippines: Need for snail surveillance technique
Fornillos, R.J.C.1*, Fontanilla, I.K.C.1, Chigusa, Y.2, Kikuchi, M.3, Kirinoki, M.2, Kato-Hayashi, N.2,
Kawazu, S.4, Angeles, J.M.4, Tabios, I.K.5, Moendeg, K.4,6, Goto, Y.7, Tamayo, P.G.8, Gampoy, E.F.5,
Pates, I.8, Chua, J.C.9 and Leonardo, L.R.1,8
1Institute of Biology, National Science Complex, College of Science, University of the Philippines Diliman,
Regidor St, Quezon City, 1101 Metro Manila, Philippines
2Department of Tropical Medicine and Parasitology, Dokkyo Medical University, 880 Kitakobayashi,
Mibu-machi, Shimotsuga-gun, Tochigi, Japan
3Department of Immunogenetics, Institute of Tropical Medicine (NEKKEN) Nagasaki University, Nagasaki,
Japan
4National Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine,
Obihiro, Hokkaido, Japan
5College of Medicine, University of the Philippines Manila, 625 Pedro Gil St, Ermita, 1000 Metro Manila,
Philippines
6Department of Biology, School of Science and Engineering, Ateneo de Manila University, Loyola Heights,
Quezon City 1108, Metro Manila, Philippines
7Graduate School Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan
8Department of Parasitology, College of Public Health, University of the Philippines Manila,
625 Pedro Gil St, Ermita, 1000 Metro Manila Manila
9College of Medical Technology, Chinese General Hospital, 286 Blumentritt St, Sta. Cruz,
1014 Metro Manila, Philippines
*Corresponding author e-mail: raffyjayfornillos@gmail.com
Received 2 July 2018; received in revised form 31 December 2018; accepted 2 February 2019
Abstract. Schistosomiasis japonica is one of seven NTDs endemic in the Philippines that
continues to threaten public health in the country. The causative agent, the blood fluke
Schistosoma japonicum, uses an amphibious snail Oncomelania hupensis quadrasi which
can harbor larval stages that multiply asexually, eventually producing the infective cercariae
which are shed into the water. Contamination of freshwater bodies inhabited by the snail
intermediate host occurs through release of human and animal feces containing S.
japonicum eggs. Miracidia hatching from these eggs subsequently infect the snails that
inhabit these water bodies. The degree of fecal contamination can vary across snail sites
and influences snail infection rates in these sites. In this study, conventional malacological
surveys using intensive manual search for snails were conducted from 2015 to 2016 in
seven selected endemic provinces, namely Leyte and Bohol in the Visayas and Surigao del
Norte, Agusan del Sur, Bukidnon, Lanao del Norte and Compostela Valley in Mindanao. A
total of 6,279 O. hupensis quadrasi snails were collected from 38 snail sites. The
municipality of Trento in Agusan del Sur recorded the highest number of snail sites (7) that
yielded O. hupensis quadrasi snails while only one snail site was found positive for O.
hupensis quadrasi snails in Kapatagan in Lanao del Norte and Talibon in Bohol. Alegria in
Surigao del Norte yielded the highest number of snail sites (5) that were found to harbor
snails positive for S. japonicum infection. The snail infection rates in this municipality
ranged from 0.43% to 14.71%. None of the snails collected from Talibon in Bohol was
infected. Bohol is the only province among the 28 schistosomiasis-endemic provinces
which has reached near elimination status. Snail infection rates were found to vary
considerably across snail sites, which could be due to the degree of fecal contamination of
the snail sites and their connectivity to water that can serve as contamination source.
403
INTRODUCTION
Schistosomiasis japonica which was
discovered in the Philippines in 1906
continues to threaten the health of
agricultural communities especially the
farmers, fishermen and children who remain
constantly exposed to the disease through
their work and habits (Blas et al., 2004).
The disease is endemic in 12 regions of
the country covering 28 provinces, 14
cities, 189 municipalities and 2,221
barangays (Leonardo et al., 2016). O.
hupensis quadrasi was first described by
Mollendörff from specimens collected in
Surigao (McMullen et al., 1947) (Figure 1).
In 1932, Dr. Marcos Tubangui confirmed
the epidemiological role of O. hupensis
quadrasi as intermediate host to S.
japonicum from samples collected at
Barrio Gacao, Palo, Leyte (Blas 1988-89;
Leonardo et al., 2016).
To date, approximately 12 million
Filipinos are living in endemic areas, and
2.5 million individuals are directly exposed
to infection (Blas et al., 2004; Leonardo et
al., 2012, 2015, 2016). O. hupensis quadrasi
thrives in a wide array of freshwater bodies
such as rice fields, cemented waterways,
canals, irrigation systems, swamps,
lakeshores, riverbanks, and other shaded
and waterlogged areas (Blas, 1988-89;
Tanaka et al., 1978; Ohmae et al., 2003).
Some snail sites are located in close
proximity to households in endemic areas.
Since snail colonies populate rice fields
or irrigation canals, S. japonicum is
considered an occupational hazard among
farmers and inland fishermen (Blas,
1988-89).
Poor sanitation practices in endemic
areas perpetuate environmental con-
tamination with schistosome eggs while
lack of access to clean water increases risk
of exposure to the disease when people go
to possibly contaminated water bodies to
launder their clothes, wash their dishes
and bathe (Blas, 1991). A human infection
survey by Leonardo et al. (2008) in 13
provinces in Mindanao and five provinces
in the Visayas reported a prevalence rate
ranging from 0.08% (Agusan del Norte) to
3.95% (Agusan del Sur). New endemic foci
for schistosomiasis were further discovered
in Gonzaga, Cagayan Valley and Calatrava,
Negros Occidental in 2002 and 2005,
respectively. Various diagnostic procedures
from stool examination (Kato-Katz),
serodiagnosis (COPT and ELISA), and
ultrasound were used to confirm cases of
schistosomiasis in these new foci (Leonardo
et al., 2015). Based from the report of the
Philippine Department of Health in 2018,
1611 villages (barangays) are still endemic
to schistosomiasis with around 188 are
low endemic (11.67%), 382 are moderately
endemic, and 453 are highly endemic
(28.12%). For zero prevalence barangays,
242 (15.02%) have been recorded, but 346
remain to be determined due to lack of focal
surveys done in these areas. Stratification
of endemicity of villages were based on the
prevalence recorded during focal surveys
with >5% in high endemic areas, >1% but
<5% in moderately endemic and <1% in low
endemic areas (DOH, 2018).
A multifaceted schistosomiasis program
is required for the successful control and
eventual elimination of the disease, and
this necessitates sustained and regular data
from human, animal, and snail surveys.
Malacological surveys yield data such as
snail density, distribution and infection rate,
which can be used as indicators of the
possible extent of distribution and rate of
transmission of the disease (UP CPH
Foundation, 2012). This study therefore
aimed to provide baseline data of the snail
infection rate in seven selected endemic
Figure 1. Oncomelania hupensis quadrasi
(Mollendörff, 1895) snail collected from Alegria,
Surigao del Norte, Philippines.
404
provinces and provide information for
potential areas for transmission.
MATERIALS AND METHODS
Malacological surveys were conducted in
seven municipalities representing seven
schistosomiasis-endemic provinces that
were selected based on the national
prevalence survey conducted in 2005-
2008 (Leonardo et al., 2008, 2012). These
provinces were Bohol and Leyte in the
Visayas and Surigao del Norte, Agusan del
Sur, Bukidnon, Lanao del Norte, and
Compostela Valley in Mindanao (Table 1,
Figure 2A). Surveys were done from April
2015 to January 2016 (Table 1) through
intensive and purposive search in sites
known to support O. hupensis quadrasi
snails. There were common ecological
characteristics in the snail sites visited,
which include being waterlogged and
with thick vegetation shading swamps,
riverbanks, rice fields, irrigation canals,
ponds, and streams (Figure 2B-E). Survey
was done for one day from 8 am to 12 noon
and 1 pm to 3 pm. The number of snail
collectors per site varied depending on the
availability of personnel at the time of
survey (Table 1). The snails were collected
using forceps and placed in properly labeled
containers, after which they were air
dried in a conventional filter paper away
from direct exposure to sunlight or heat. Air
dried snails were transferred and packed
carefully in clean sheets of filter paper
and transported to the Department of
Parasitology, University of the Philippines
Manila for further processing.
Identity of snails was confirmed by
examination of shell morphology. O.
hupensis quadrasi snails have a distinct
ovately conic shell shape with sharp apex.
Shell color may vary from brown to black.
Juvenile snails are 3 milimeters (mm) in
Table 1. List of selected barangays surveyed in municipalities across seven provinces endemic to
schistosomiasis japonica in the Philippines
Endemic Villages/ Date No. of No. of
Island Province Municipality/ Barangays Surveyed Collectors sites
City surveyed
Leyte Northern Alang-alang Bugho, San Apr 13-17, 5 8
Leyte Antonio Farm, 2015
San Vicente
Bohol Bohol Talibon San Roque Jul 28-31, 4 1
2015
Agusan del Trento Manat, Jul 13-17, 5 11
Sur Tudela, 2015
San Isidro
Surigao del Alegria Poblacion, Aug 4-7, 5 8
Norte Alipao, 2015
San Pedro
Mindanao Lanao del Kapatagan Bagong Oct 27-30, 4 3
Norte Silang 2015
Curvada,
De Asis
Bukidnon Valencia Kahaponan, Nov 30- 3 3
Vintar, Dec 4,
San Isidro 2015
Compostela Maragusan Tigbao, Jan 24-27, 6 4
Valley Mapawa, 2016
New Albay
405
Figure 2. (A) Seven provinces in the Philippines surveyed for S. japonicum
infection to O. hupensis quadrasi snails. Visayas: Leyte, Bohol; Mindanao: Surigao
del Norte, Agusan del Sur, Bukidnon, Lanao del Norte, Compostela Valley. (B)
Malacological survey conducted in a rice field in Trento, Agusan del Sur with O.
h. quadrasi snails, (C) Sarong boggy, a snail site in a swampy area in Talibon,
Bohol, (D) wide and deep irrigation canals supplying water in many rice fields in
Agusan del Sur, (E) an O. hupensis quadrasi attached to a stone collected from a
riverside in Valencia, Bukidnon.
length or less and adult snails are 3 mm with
maximum of 6 mm in length (Garcia, 1988;
Leonardo & Solon, 1996).
Snail infection was determined micro-
scopically by demonstrating schistosome
cercariae and sporocysts in crushed snails.
Snails were placed individually in three
drops of distilled water in a glass slide. The
snails were crushed by pressing another
clean slide on top of the slide with the snails.
Snail tissues were further teased and shell
debris removed to better expose the
schistosome cercariae and sporocysts. The
crushed snails were examined under a
406
stereomicroscope (Bausch & Lomb OPT. Co.
U.S.A.). Snails were considered infected if
the characteristic furcocercous cercariae
and sac-like sporocysts were seen. The rate
of infection for the municipality surveyed
was computed as follows: [(number of
infected snails)/ (total number of collected
snails examined)] x100.
RESULTS
A total of 6,279 O. hupensis quadrasi
snails were collected from the seven
municipalities (Table 2). Agusan del Sur
yielded the highest number of sites surveyed
at 11 sites while the least number was in
Talibon, Bohol with only one site (Tables 1
& 2). The highest number of collected snails
was recorded in Agusan del Sur with a total
of 1,683 snails from Barangays Manat,
Tudela, and San Isidro (Table 2). The least
number was recorded in Valencia, Bukidnon
with 133 snails from Barangays Vintar,
Kahaponan, and San Isidro (Table 2). It was
observed during the survey that not much
is known about snail sites in Valencia,
Bukidnon. In the light of this paucity of
information, the survey was extended to all
possible snail habitats such as tributaries
of rivers, rice fields and water-logged areas,
which revealed few interspersed clumps of
snails. In Agusan del Sur where prevalence
of the disease has been known to be high,
sanitary inspectors and malacologists
previously conducted malacological
surveys to monitor the snail intermediate
hosts. Thus, records of snail sites and
their location provided crucial a priori
information on the municipality, leading to
a more focused survey and subsequently
resulting to a very high number of collected
snails.
The highest number of snail sites with
infected snails was recorded in Alegria,
Surigao del Norte (SDN) with five sites
(Table 1, Figure 3). Table 2 shows that snails
positive for schistosome infection were
found in snail sites surveyed in the 6 of the
7 provinces covered. The snails found from
the single site in Talibon, Bohol were
negative for S. japonicum cercariae or
sporocysts, the only province in this study
to yield such result (Tables 2 & 3). It should
be noted that among the 28 provinces which
are presently endemic for schistosomiasis,
only Bohol has reached near elimination
status on the basis of the absence of human
cases for the past many years according to
health authorities (Leonardo personal
communication). Widest range of snail
infection rate (IR) was noted in Alegria,
Surigao del Norte (0.43%–14.71%) while the
narrowest IR range was recorded in
Valencia, Bukidnon (0%-1.72%) (Table 3).
DISCUSSION
In the Philippines, the cornerstone of
schistosomiasis control has been mass drug
administration (MDA) while snail control
has not been given that much attention.
Malacological surveys are not regularly
Table 2. Summary of results for the different municipalities based on the malacological surveys conducted
from April 2015 to January 2016
Municipality Sites with Sites with Number of Number of
Ohq infected Ohq (%) collected snails infected snails (%)
Talibon 1 0 (0.00) 38 8 0 (0.00)
Alang-alang 5 3 (60.0) 1588 9 (0.57)
Trento 7 3 (42.9) 1683 6 (0.36)
Alegria 6 5 (83.3) 1229 12 (0.98)
Kapatagan 1 1 (100.0) 461 4 (0.87)
Valencia 3 1 (33.3) 1 33 1 (0.75)
Maragusan 4 3 (75.0) 7 97 12 (1.51)
Note: Ohq = Oncomelania hupensis quadrasi.
407
Table 3. Summary of snail infection rates (IR) of snail sites from the endemic municipalities
Island Province Municipality Site IR (%)
Maragusan 1 0
Compostela Valley Maragusan Maragusan 2 1.89
Maragusan 3 1.03
Maragusan 4 2.15
SDN 1 14.71
SDN 2 0.65
Surigao del Norte Alegria SDN 3 1.19
SDN 4 0.43
SDN 5 0.65
Mindanao
BKN 1 1.72
Bukidnon Valencia BKN 2 0
BKN 3 0
Agusan 1 0
Agusan 2 0
Agusan 3 2.22
Agusan del Norte Trento Agusan 4 0.32
Agusan 5 0
Agusan 6 2.38
Agusan 7 0
Bohol Bohol Talibon Bohol 0
Leyte 1 1
Leyte Leyte Alang-alang Leyte 2 0
Leyte 3 0.36
Leyte 4 0
conducted so that snail sites are not updated
and transmission sites are not identified.
The situation in Valencia, Bukidnon
illustrates this problem clearly where
paucity of information is further perpetuated
by the lack of manpower to conduct snail
surveys. In contrast, control efforts in
Agusan del Sur have included snails to bring
down the consistently high prevalence of
schistosomiasis in the province. While the
data for Bohol may be promising, i.e. no
infected snails and human cases, further
surveillance using more sensitive serologic
tests on humans and other animal reservoir
hosts and regular snail surveys should be
conducted to confirm the near elimination
status of schistosomiasis in the province and
potentially towards full elimination status.
In China, infected snails were still observed
even in areas where transmission was
declared to be controlled. Few areas showed
a decreasing trend in snail infection rate
while other areas that were monitored
for snail surveillance worsened, indicating
that snail control should be focused and
reinforced most especially in areas where
transmission were under control (Gen-Ming
et al., 2005).
In Alegria, Surigao del Norte, one snail
site (SDN1) was observed to have the highest
infection with 14.71% (Table 3). This snail
site was observed to be near human
settlement and even a pig farm and was
therefore a recipient of domestic wastes.
408
High snail infection rates are indicative of
intense fecal contamination either from
infected humans or infected animals caused
by poor environmental sanitation or failure
to manage waste disposal from livestock.
While snail population density and snail
distribution are important indicators of
possible presence and spatial distribution
of schistosomiasis, a better parameter
that indicates disease transmission is
snail infection rate. The lone snail site in
Kapatagan, Lanao del Norte (1/1 = 100%)
was found to harbor infected snails
(Table 2). This result should be a red flag
for the municipality, and efforts should be
intensified to locate more snail sites and
examine these for the presence of snails and
determine if they are infected. The presence
of infected snails means that their habitat is
being contaminated with feces coming
from infected vertebrates. Unless access
by potential hosts are restricted or removed
to disrupt the life cycle of the parasite,
this site will remain a transmission site.
Moreover, snail infection rate can be an
ideal monitoring tool to assess progress in
intervention programs such as MDA and
environmental sanitation. If these two main
key strategies are neglected and efforts not
sustained, infected cases without access to
clean and safe water for domestic purposes
will certainly contaminate freshwater bodies
where O. hupensis quadrasi colonies
thrive, infecting these snails.
Previous studies reporting snail
infection rates were conducted in other
endemic areas in the Philippines such as
Gonzaga in Cagayan Valley, Calatrava in
Negros Occidental, and Samar (Madsen
et al., 2008; Leonardo et al., 2015). For
instance, Leonardo et al. (2015) noted
higher snail infection rates in Gonzaga than
in Calatrava, particularly in Barangay
Magrafil that can be attributed to the closer
proximity of snails to human habitation
and the presence of infected animals that
may continuously contaminate the water
and subsequently infect the snails. Other
barangays showed comparatively lower
snail infection rates, and variability of snail
infection rates across barangays was high.
In another study, Madsen et al. (2008) com-
pared naturally rain-fed and artificially
irrigated villages and noted no significant
difference in snail density but with signifi-
cantly higher infection rate in artificially
irrigated villages, which they attributed to
the steady and consistent supply of water in
these areas that allowed for longer stay of
snail colonies and therefore greater
exposure time to the parasites.
The current study shows the importance
of snail data in elucidating the status of
schistosomiasis in endemic areas. Snail
population density, spatial distribution and
snail infection rates are critical indicators
of the possible presence and distribution
of the disease as well as occurrence of
transmission. The number of snails collected
and snail infection rate vary even if the snail
sites demonstrate striking similarity in
ecological characteristics such as being
waterlogged with thick vegetation. There-
fore, snail surveys must be regularly
conducted in schistosomiasis endemic
provinces.
The importance of identifying sites
positive not only for snails but for snails
infected with S. japonicum could not be
overemphasized. Whilst municipalities like
Talibon, Kapatagan and Valencia have only
few snail sites or sites with infected snails,
this information should spur them to
intensify efforts in expanding their surveys
to include other unvisited sites to determine
potential transmission sites.
For other endemic municipalities
such as Alang-alang, Trento, Alegria and
Maragusan, having identified the snail sites
and those with infected snails puts them at
first base, but further steps should be
undertaken such as restricting access of
humans and domesticated animals to these
sites in order to disrupt the life cycle of
S. japonicum.
Identification and mapping of snail
sites and continuous monitoring for snail
infection are therefore important com-
ponents of snail surveillance, which should
be standard for schistosomiasis intervention
programs in endemic areas. Snail control
methods can be done through environmental
modification measures such as cement
lining, dredging, and burying in order to
409
destroy the snail habitats. Japan was able
to eliminate schistosomiasis in the 1990’s
using mostly by mostly transforming
waterlogged areas into fruit plantations,
burying snail habitats, and converting them
into residences and even golf courses. To
date, however, O. hupensis nosophora, the
snail intermediate host of schistosomiasis
in Japan, remains in large number in
previously endemic areas in Japan such
as Yamanashi-Kofu River Basin, though no
human and animal cases have been noted
since 1977 after continuous control efforts
(Tanaka & Tsuji, 1997). This just goes to
show that the disease can be eliminated
without eliminating the snail intermediate
host. What is essential is to prevent trans-
mission by keeping the snails free from S.
japonicum infection.
In light of the call for elimination of
schistosomiasis by 2030, endemic countries
are encouraged to intensify control and
elimination efforts starting with deve-
lopment not only of highly sensitive
diagnostic methods to detect the disease in
humans and animal reservoirs but identify
snail sites and determine snail infection
rate. The Philippines can place its hopes on
Bohol to be the first province to eliminate
schistosomiasis given its present status of
no infected snails and no infected humans
(using Kato-Katz for diagnosis).
However, 0% infection rate status
must be confidently ascertained through
extensive snail survey coupled with the use
of sensitive diagnostic tools. Malacological
surveys could be very laborious, time-
consuming, and unreliable especially since
many of those involved may not have the
necessary expertise in identifying snails let
alone determine snail infection rate. Another
downside of intensive manual search is the
physical hazard in accessing possible snail
sites that can only be reached after crossing
steep and slippery slopes or boggy marsh
with unstable substrate.
A possible complement currently being
explored is detection of environmental
DNA (eDNA) from the parasite or the snail
intermediate host. This provides a rapid
and more accurate method that is also
safer to use. Several molecular markers
have already been used in detecting
helminth parasites. These markers include
transposons and retrotransposons for S.
japonicum (Driscoll et al., 2005; Hung &
Remais, 2008), and cytochrome c oxidase
subunit 1 gene (cox1) for O. viverrini
and O. lobatus (Hashizume et al., 2017).
Presence of environmental DNA (eDNA)
is indicative of the target organism’s
presence and can be used to estimate range
of endemicity of the parasite in a sampled
area.
CONCLUSION
Malacological surveys using intensive
search were used to confirm the presence
of snails in previously located snail sites
in selected villages in endemic muni-
cipalities in seven schistosomiasis endemic
provinces. The extent of collection in terms
of how many snail sites surveyed and the
number of snails collected was influenced
by available information on these snail
sites. Snail infection rates varied across
snail sites even if conditions seem to be
similar like heavily shaded water logged
areas. Variation was attributed to degree of
fecal contamination of the sites and/or their
degree of connectivity to sources of fecal
contamination.
RECOMMENDATIONS
The present conventional malacological
surveys through intensive search can yield
fruitful results if there is enough manpower
and enough expertise in identifying snails
and the infective cercariae and sporocysts.
In the light of intensifying surveillance to
support efforts for elimination of the disease,
an alternative technique through eDNA
detection in water samples collected from
existing snail sites and possible snail sites
can be explored.
Acknowledgements. We thank the Depart-
ment of Science and Technology-Philippine
Council for Health Research and Deve-
lopment (DOST-PCHRD) and Accelerated
410
Science and Technology Human Resources
Development Program, DOST Science
Education Institute (ASTHRDP-DOST-SEI)
for funding this study. We also acknowledge
Nagasaki University, Dokkyo Medical
University, University of Tokyo, Obihiro
University of Agriculture and Veterinary
Medicine, rural health units of all
schistosomiasis-endemic municipalities,
and the local sanitary inspectors and
malacologists for the logistical support.
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... This snail species prefers aquatic environments, such as wet soils, rice paddies, ponds, streams and shaded areas in riverbanks (Gordon et al., 2019). Various studies and governmental reports have noted varying S. japonicum infection rates among snails collected in endemic areas, majority of which are in Mindanao (Abao-Paylangco et al., 2019;Fornillos et al., 2019a). Snail-infested bodies of water are sources of direct infection transmission due to a large amount of parasite cercariae infective stages released by S. japonicum-infected O. hupensis quadrasi. ...
... These snails are prevalent near water bodies, wherein they release the infective stage of the parasite (Fornillos et al., 2019;Leonardo et al., 2020b). Moreover, Fornillos et al. (2019a) reported that water-logged areas with thick vegetation, riverbanks, rice fields, ponds, irrigation cannals, swamps, and streams were common characteristics of habitats of O. hupensis quadrasi in the Philippines. These conditions provide adequate moisture and shade for the snails out of the 4 sampling sites having snails infected with S. japonicum. ...
... These were followed by Mindoro Oriental, Negros Occidental, Agusan del Sur, Leyte, Lanao del Norte, Bukidnon, New Corella in Davao del Norte, and Negros Occidental which had snails infected with S. japonicum but with infection rates at lower than 1%. Recently,Fornillos et al. (2019a) determined the S. japonicum SIR and positive sampling sites (PSS) of O. hupensis quadrasi in different edemic areas of the country. They reported that Maragusan, Compostela Valley had the highest infection rate (1.51 %), with 3 ...
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Schistosoma japonicum infections continue to be a public health concern in China, the Philippines, and Indonesia. In the Philippines, it has a focal distribution wherein an estimated 12.4 million people are at risk of infection, while 2.7 million are directly exposed across 12 regions. The country’s latest national prevalence revealed that some endemic communities had already reached infection control status. Recent advancements in schistosomiasis diagnostics have resulted in the development of assays that have superior diagnostic performance. The cost of adopting these novel techniques remains a huge bottleneck for those with developing economies and underfunded control and elimination programs like the Philippines. Mass Drug Administration (MDA) has significantly reduced the schistosomiasis morbidity rates in the Philippines through its protracted implementation. MDA fatigue among beneficiaries resulting in non-compliance has been reported. Control and elimination efforts still need continued local and national governmental support. A One Health approach is called for if the goal of transmission interruption in all endemic communities is to be achieved by 2025. This paper reviews the recent research and updates on S. japonicum infections in terms of disease occurrence, advancements in diagnostic techniques and approaches, and its treatment, prevention, control, and elimination in the Philippines and its neighboring countries.
... Schistosomiasis surveillance is performed to monitor progress of control programs, especially when prevalence levels have gone down to elimination levels. One specific conventional surveillance technique is the malacological survey where O. hupensis quadrasi snails are collected, crushed, and examined for the presence of the characteristic furcocercous cercariae of schistosomes [8,27]. The presence of infected snails is an indication of environmental contamination by fecal matter containing schistosome eggs in the freshwater [7]. ...
... The presence of infected snails is an indication of environmental contamination by fecal matter containing schistosome eggs in the freshwater [7]. Though this method is cost-effective, the demand for expertise in correctly identifying the snails in their natural habitat and for the mobilization of huge manpower during surveys, and the inaccessibility of some snail sites make the malacological survey a huge task to undertake [8,26,27]. ...
... The use of this type of DNA source material utilizing soil samples could be a useful tool for snail surveillance due to the amphibious nature of the snail. [8,27]. The presence of infected snails is an indication of environmental contamination by fecal matter containing schistosome eggs in the freshwater [7]. ...
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Background: The perpetuation of schistosomiasis japonica in the Philippines depends to a major extent on the persistence of its intermediate host Oncomelania hupensis quadrasi, an amphibious snail. While the malacological survey remains the method of choice in determining the contamination of the environment as evidenced by snails infected with schistosome larval stages, an emerging technology known as environmental DNA (eDNA) detection provides an alternative method. Previous reports showed that O. hupensis quadrasi eDNA could be detected in water, but no reports have been made on its detection in soil. Methods: This study, thus focused on the detection of O. hupensis quadrasi eDNA from soil samples collected from two selected schistosomiasis-endemic barangays in Gonzaga, Cagayan Valley using conventional and TaqMan-quantitative (qPCR) PCRs. Results: The results show that qPCR could better detect O. hupensis quadrasi eDNA in soil than the conventional method. In determining the possible distribution range of the snail, basic edaphic factors were measured and correlated with the presence of eDNA. The eDNA detection probability increases as the pH, phosphorous, zinc, copper, and potassium content increases, possibly indicating the conditions in the environment that favor the presence of the snails. A map was generated to show the probable extent of the distribution of the snails away from the body of the freshwater. Conclusion: The information generated from this study could be used to determine snail habitats that could be possible hotspots of transmission and should, therefore, be targeted for snail control or be fenced off from human and animal contact or from the contamination of feces by being a dumping site for domestic wastes.
... Schistosomiasis surveillance is performed to monitor progress of control programs, especially when prevalence levels have gone down to elimination levels. One specific conventional surveillance technique is the malacological survey where O. hupensis quadrasi snails are collected, crushed, and examined for the presence of the characteristic furcocercous cercariae of schistosomes [8,27]. The presence of infected snails is an indication of environmental contamination by fecal matter containing schistosome eggs in the freshwater [7]. ...
... The presence of infected snails is an indication of environmental contamination by fecal matter containing schistosome eggs in the freshwater [7]. Though this method is cost-effective, the demand for expertise in correctly identifying the snails in their natural habitat and for the mobilization of huge manpower during surveys, and the inaccessibility of some snail sites make the malacological survey a huge task to undertake [8,26,27]. ...
... The use of this type of DNA source material utilizing soil samples could be a useful tool for snail surveillance due to the amphibious nature of the snail. Pathogens 2018, 7, x FOR PEER REVIEW 3 of 25 is the malacological survey where O. hupensis quadrasi snails are collected, crushed, and examined for the presence of the characteristic furcocercous cercariae of schistosomes [8,27]. The presence of infected snails is an indication of environmental contamination by fecal matter containing schistosome eggs in the freshwater [7]. ...
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Full-text available
Background: The perpetuation of schistosomiasis japonica in the Philippines depends to a major extent on the persistence of its intermediate host Oncomelania hupensis quadrasi, an amphibious snail. While the malacological survey remains the method of choice in determining the contamination of the environment as evidenced by snails infected with schistosome larval stages, an emerging technology known as environmental DNA (eDNA) detection provides an alternative method. Previous reports showed that O. hupensis quadrasi eDNA could be detected in water, but no reports have been made on its detection in soil. Methods: This study, thus focused on the detection of O. hupensis quadrasi eDNA from soil samples collected from two selected schistosomiasis-endemic barangays in Gonzaga, Cagayan Valley using conventional and TaqMan-quantitative (qPCR) PCRs. Results: The results show that qPCR could better detect O. hupensis quadrasi eDNA in soil than the conventional method. In determining the possible distribution range of the snail, basic edaphic factors were measured and correlated with the presence of eDNA. The eDNA detection probability increases as the pH, phosphorous, zinc, copper, and potassium content increases, possibly indicating the conditions in the environment that favor the presence of the snails. A map was generated to show the probable extent of the distribution of the snails away from the body of the freshwater. Conclusion: The information generated from this study could be used to determine snail habitats that could be possible hotspots of transmission and should, therefore, be targeted for snail control or be fenced off from human and animal contact or from the contamination of feces by being a dumping site for domestic wastes.
... Common ecological characteristics in the snail sites included being waterlogged and with thick vegetation that shaded swamps, riverbanks, rice fields, irrigation canals, ponds and streams (Fornillos et al. 2019a). There are many areas which look favorable for snails yet snails are absent. ...
... Schistosomiasis is one of the seven neglected tropical diseases (NTDs) that are prevalent in the Philippines [1]. It is reported that it affects 207 million people across 76 countries [2]. ...
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Background and Aim: Schistosomiasis is one of the seven neglected tropical diseases that are of public health concern in the Philippines. The disease is prevalent in few of the barangays (communities) in Koronadal City, Philippines. Status of the Schistosoma japonicum infections in domestic animal reservoir host has yet to be explored in these endemic communities. The study aimed to determine the prevalence and infection intensity of the disease in cattle and water buffaloes of endemic communities of Koronadal City. Materials and Methods: Schistosomiasis was investigated in 70 cattle and 38 water buffaloes from three endemic communities in Koronadal City. The copro-parasitological technique used was the formalin-ethyl acetate sedimentation method. Results: S. japonicum infection was observed in 48.6% of cattle and 60.5% in water buffaloes. The bovine contamination index indicated that all infected animals released 3,505,500 eggs/day. On average, infected cattle released 1,674,500 eggs daily, while infected water buffaloes liberated 1,932,000 eggs in the environment daily. Conclusion: Cattle and water buffaloes in these endemic areas are infected with S. japonicum. These animals release large numbers of eggs in the environment daily; hence, played an important role in disease transmission. Those living and working in endemic areas should be aware of the inherent dangers of the disease.
... Snails were crushed gently just enough to break the shell by placing another clean glass slide on top of the slide containing the snails. Each aliquot containing a crushed snail was examined using a stereomicroscope and tissues were teased using forceps or a dissecting needle to facilitate release of the sporocysts or the characteristic furcocercous bifurcated cercariae of S. japonicum, which are indicators of an infected snail [24]. For the water collection, a plastic bottle was used to collect approximately 500 mL of surface water from each site, usually along the edge of the freshwater bodies (e.g. ...
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In recent years, the prevalence and infection intensity of Schistosoma japonicum in endemic areas of the Philippines have significantly decreased due to yearly population-based treatment strategies, yet transmission rates remain high and uninterrupted. An important indicator of active disease transmission is the presence of Schistosoma japonicum and its snail intermediate host Oncomelania hupensis quadrasi in freshwater habitats. In this study, we sought to apply a species-specific real-time PCR (qPCR) assay for the detection of S. japonicum and O. hupensis quadrasi in freshwater samples using environmental DNA approach that can complement the commonly utilized malacological survey in determining potential transmission foci in order to have a more effective snail surveillance strategy for schistosomiasis japonica in endemic areas. The newly developed assay was specific to S. japonicum and O. hupensis quadrasi with no amplification detected against non-target trematode Fasciola spp. and snails such as Lymnaea spp., Pomacea canaliculata, and Melanoides spp. that typically co-exist in the same environment. The assay effectiveness was determined using 19 environmental water samples collected from Northern Samar (N = 5 sites), Leyte (N = 11 sites) and Compostela Valley (N = 3 sites) and compared to malacological survey for determining O. hupensis quadrasi snail colonies and snail crushing to visualize S. japonicum cercariae. TaqMan qPCR targeting a short fragment of the cytochrome c oxidase subunit 1 (cox1) gene was positive for S. japonicum in 9 sites, for O. hupensis quadrasi in 9 sites, and for both S. japonicum and O. hupensis quadrasi in 5 sampling sites. Moreover, it was able to detect O. hupensis quadrasi in 3 out of 12 sites found negative and 6 out of 7 sites found positive through malacological survey, and in 4 of the 5 snail sites positive for snails with cercariae. Overall, this method can complement malacological surveys for monitoring of schistosomes in endemic areas of the Philippines, especially those with high risk of human infection.
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Schistosomiasis remains a major public health concern affecting approximately 12 million people in the Philippines due to inadequate information about the disease and limited prevention and control efforts. Schistosoma japonicum, one of the causative agents of the disease, requires an amphibious snail Oncomelania hupensis quadrasi (O. h. quadrasi) to complete its life cycle. Using the geographical information system (GIS) and maximum entropy (MaxEnt) algorithm, this study aims to predict the potential high-risk habitats of O. h. quadrasi driven by environmental factors in the Philippines. Based on the bioclimatic determinants, a very high-performance model was generated (AUC = 0.907), with the mean temperature of the driest quarter (25.3%) contributing significantly to the prevalence of O. h. quadrasi. Also, the snail vector has a high focal distribution, preferring areas with a pronounced wet season and high precipitation throughout the year. However, the findings provided evidence for snail adaptation to different environmental conditions. High suitability of snail habitats was found in Quezon, Camarines Norte, Camarines Sur, Albay, Sorsogon, Northern Samar, Eastern Samar, Leyte, Bohol, Surigao del Norte, Surigao del Sur, Agusan del Norte, Davao del Norte, North Cotabato, Lanao del Norte, Misamis Occidental, and Zamboanga del Sur. Furthermore, snail habitat establishment includes natural and man-made waterlogged areas, with the progression of global warming and climate change predicted to be drivers of increasing schistosomiasis transmission zones in the country.
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Background: Schistosomiasis is of great public health concern with a wide distribution and multiple determinants. Due to the advances in schistosomiasis elimination and the need for precision prevention and control, identifying determinants at a fine scale is urgent and necessary, especially for resource deployment in practice. Our study aimed to identify the determinants for the seropositive rate of schistosomiasis at the village level and to explore their spatial variations in local space. Methodology: The seropositive rates of schistosomiasis were collected from 1714 villages or communities in Human Province, and six spatial regression models including ordinary least squares (OLS), spatial lag model (SLM), spatial error model (SEM), geographically weighted regression (GWR), robust GWR (RGWR) and multiscale GWR (MGWR) were used to fit the data. Principal/findings: MGWR was the best-fitting model (R2: 0.821, AICc:2727.092). Overall, the nearest distance from the river had the highest mean negative correlation, followed by proportion of households using well water and the annual average daytime surface temperature. The proportions of unmodified toilets showed the highest mean positive correlation, followed by the snail infested area, and the number of cattle. In spatial variability, the regression coefficients for the nearest distance from the river, annual average daytime surface temperature and the proportion of unmodified toilets were significant in all villages or communities and varied little in local space. The other significant determinants differed substantially in local space and had significance ratios ranging from 41% to 70%, including the number of cattle, the snail infested area and the proportion of households using well water. Conclusions/significance: Our study shows that MGWR was well performed for the spatial variability of schistosomiasis in Hunan province. The spatial variability was different for different determinants. The findings for the determinants for the seropositive rate and mapped variability for some key determinants at the village level can be used for developing precision intervention measure for schistosomiasis control.
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Schistosomiasis affects 28 provinces in the Philippines found along the southeastern part where there is continuous rainfall throughout the year. In 2002 and 2005 respectively, two new endemic foci were reported in the northernmost (Gonzaga, Cagayan) and central (Calatrava, Negros Occidental) parts of the country. This study conducted in March 2008 to March 2009 confirmed the presence of the disease by determining its prevalence using four diagnostic tests - Kato-Katz, circum-oval precipitin test (COPT), ELISA and ultrasonography. Oncomelania hupensis quadrasi was identified through snail surveys conducted in possible snail habitats in the seven new endemic villages. Animal surveys through stool examination confirmed the presence of schistosomiasis infection in animals in Gonzaga but not in Calatrava. Compared to Calatrava, Gonzaga demonstrated markedly higher prevalence of schistosomiasis using all four diagnostic methods. Proximity of snail habitats to human habitation including higher snail density and snail infection rate could be responsible for the high prevalence. Snail sites were more widespread in Gonzaga whereas those in Calatrava were confined only in areas not frequented by the general population except by farmers. GIS maps showing spatial distribution of snails in Gonzaga and Calatrava indicated differences in elevation among the snail sites. It is hypothesized that the snail intermediate host has been in these sites for sometime but discovered only lately. Migration of people from endemic provinces into Gonzaga and Calatrava brought in cases and in the presence of snail intermediate hosts, emergence of disease was just a matter of time.
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For the first time in the country, a national baseline prevalence survey using a well-defined sampling design such as a stratified two-step systematic cluster sampling was conducted in 2005 to 2008. The purpose of the survey was to stratify the provinces according to prevalence of schistosomiasis such as high, moderate, and low prevalence which in turn would be used as basis for the intervention program to be implemented. The national survey was divided into four phases. Results of the first two phases conducted in Mindanao and the Visayas were published in 2008. Data from the last two phases showed three provinces with prevalence rates higher than endemic provinces surveyed in the first two phases thus changing the overall ranking of endemic provinces at the national level. Age and sex distribution of schistosomiasis remained the same in Luzon and Maguindanao. Soil-transmitted and food-borne helminthes were also recorded in these surveys. This paper deals with the results of the last 2 phases done in Luzon and Maguindanao and integrates all four phases in the discussion.
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In China alone, an estimated 30 million people are at risk of schistosomiasis, caused by the Schistosoma japonicum parasite. Disease has re-emerged in several regions that had previously attained transmission control, reinforcing the need for active surveillance. The environmental stage of the parasite is known to exhibit high spatial and temporal variability, and current detection techniques rely on a sentinel mouse method which has serious limitations in obtaining data in both time and space. Here we describe a real-time PCR assay to quantitatively detect S. japonicum cercariae in laboratory samples and in natural water that has been spiked with known numbers of S. japonicum. Multiple primers were designed and assessed, and the best performing set, along with a TaqMan probe, was used to quantify S. japonicum. The resulting assay was selective, with no amplification detected for Schistosoma mansoni, Schistosoma haematobium, avian schistosomes nor organisms present in non-endemic surface water samples. Repeated samples containing various concentrations of S. japonicum cercariae showed that the real-time PCR method had a strong linear correlation (R(2) = 0.921) with light microscopy counts, and the detection limit was below the DNA equivalent of half of one cercaria. Various cercarial concentrations spiked in 1 liter of natural water followed by a filtration process produced positive detection from 93% of samples analyzed. The real-time PCR method performed well quantifying the relative concentrations of various spiked samples, although the absolute concentration estimates exhibited high variance across replicated samples. Overall, the method has the potential to be applied to environmental water samples to produce a rapid, reliable assay for cercarial location in endemic areas.
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Schistosomiasis is a snail-borne neglected tropical disease affecting 78 countries and territories in Africa, Asia, South America and the Middle East.Three species are highly pathogenic to man namely Schistosoma japonicum, S. mansoni and S. haematobium. In the Philippines, the endemic species is S. japonicum to which 2.5 million Filipinos are directly exposed. This paper describes schistosomiasis in the Philippines, the status of the disease, the efforts in controlling it, the numerous problems in the implementation of the control program and good practices developed in endemic areas that have contributed to even limited success and possible prospects in control of the disease. It traces the history of the control program from the time that the disease was discovered in 1906 and cites various administrative orders that provided for the implementation of the different components of the program. Much of the information contained in this paper were collated from the program implementation review of the control program in 2012, consultative meetings conducted in 2013 with health officials involved in the program, reports delivered in the 15th meeting of the RNAS+ in July 2015, personal communications with program implementers in endemic areas visited in researches of the principal author, and her research team. The principal author was involved in all these activities and wrote the final reports.
Article
Among the areas in Japan where schistosome infections have occurred for many years, three major areas were Katayama District, Kofu Basin and Chikugo River Basin and three minor areas were Numazu District, Tone River Basin and Obitsu River Bank. The presence of the disease had long been recognised in the Katayama Memoir written by Fujii (1847, in the Chinese Classics). The cause of this endemic disease had been studied by many researchers, and finally a new trematode, Schistosoma japonicum, was discovered by Katsurada in 1904 [Tokyo Iji Shinshi, Vol. 1371, pp. 13-32]. The route of percutaneous infection was proven by Fujinami & Nakamura (1909) [Kyoto Medical Journal, Vol. 6, pp. 224-252] using 17 calves. Miyairi & Suzuki (1913) [Tokyo Iji Shinshi, Vol. 1836, pp. 1961-1965] determined a small snail, Oncomelania nosophora, as being the intermediate host, and clarified the development of the schistosome in the snail. To kill schistosome eggs, human faecal matter ('night soil') was stored for 2 weeks or more before using as fertiliser. Control of the parasite used caustic lime and calcium cyanamide to kill eggs, cercariae and Oncomelania snails. Susceptible cows were replaced with horses, which were more resistant to infection as the animal of burden for agriculture. Ditches around the rice fields were cemented for destruction of snail habitats. For snail control, sodium pentachlorophenate (NaPCP) was sprayed extensively. Some wetlands were drained and reclaimed and in selected localities, the river bottom was dredged. Such projects were undertaken with government support and aided by community participation. Epidemiological surveys began in 1910, first at Kofu, and infected people were treated with sodium tartar emetic (Stibnal) after 1921. The total number of cases detected in Japan in 1920 was about 8000. This figure was reduced annually down to 438 by 1970. The last human case of new infection found in Japan was at Kofu in 1977. Although snails were eradicated in most areas by 1983, a limited number of uninfected snails remain at Kofu and Obitsu.
Article
Except for imported cases, we have had no new Schistosoma japonicum infection in Japan since 1977. But there are still two habitats of the intermediate snail host: Oncomelania nosophora in the previous endemic areas of Kofu Basin and Obitsu. O. nosophora from Kofu Basin and Obitsu are susceptible to Chinese and Philippine strains of S. japonicum. The number of immigrants from current endemic areas in China or the Philippines is increasing. In order to prevent re-emerging of S. japonicum infections in Japan, we should continue monitoring on those existing snail hosts and investigate an adequate quarantine system. In Japan, elimination of schistosomiasis has been mainly accomplished by control of the snail host. As measures of snail control, cement-lining of ditches and chemical mollusciciding were most effective in Japan. But the cost of this joint program is too expensive compared with health budget in almost developing countries. In endemic areas of Japan, land reformation from paddy field to fruit farm was also effective. The intermediate snail host in the Philippines, Oncomelania quadrasi is much more aquatic than O. nosophora. For control of O. quadrasi, small drainage of the water and land reclamation from swampy field to rice-field were effective. Based on biological characteristics of Oncomelania spp., we can modify the past successful snail control program in Japan to be adapted ecologically and economically to each endemic area of developing countries.
Article
A descriptive study was carried on the schistosomiasis problem in the Philippines from the time the disease was discovered in 1906 to the latter part of the 1990 s. Some research findings were reviewed including the nature of the disease itself. Based on the thrust of the control program which is centered mainly on selective mass treatment and progressed to disease stratification and mass treatment using praziquantel, a downward trend in the prevalence of the disease was observed-from an average of 10.4% in 1981-1985 to 4.1% in 1996. Recommended prospective action, among others, include the development of strategies on environmental sanitation and snail control/eradication in the thrust of the schistosomiasis control program. Other policy related concerns should be formulated subject to the results of further research activities such as on (a) chemotherapy; (b) drug delivery schemes; (c) diagnosis; (d) search for a safe, economical and effective chemical(s) for vector control; and (e) prophylaxis and vaccine production for protection against infection for disease modulation or reduction of pathology.