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Original Article

Morphology and Molecular Identification of Echinostoma revolutum and Echinostoma macrorchis in Freshwater Snails and Experimental Hamsters in Upper Northern Thailand

Preeyaporn Butboonchoo1,2, Chalobol Wongsawad1,2,*, Pheravut Wongsawad1,2,3, Jong-Yil Chai4,5
The Korean Journal of Parasitology 2020;58(5):499-511.
Published online: October 22, 2020

1Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand

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*Corresponding author (wchalobol@gmail.com)
• Received: May 19, 2020   • Revised: September 21, 2020   • Accepted: September 22, 2020

Copyright © 2020 by The Korean Society for Parasitology and Tropical Medicine

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Morphology and Molecular Identification of Echinostoma revolutum and Echinostoma macrorchis in Freshwater Snails and Experimental Hamsters in Upper Northern Thailand
Korean J Parasitol. 2020;58(5):499-511.   Published online October 22, 2020
DOI: https://doi.org/10.3347/kjp.2020.58.5.499
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Morphology and Molecular Identification of Echinostoma revolutum and Echinostoma macrorchis in Freshwater Snails and Experimental Hamsters in Upper Northern Thailand
Korean J Parasitol. 2020;58(5):499-511.   Published online October 22, 2020
DOI: https://doi.org/10.3347/kjp.2020.58.5.499
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Morphology and Molecular Identification of Echinostoma revolutum and Echinostoma macrorchis in Freshwater Snails and Experimental Hamsters in Upper Northern Thailand
Image Image Image Image Image
Fig. 1 Map of upper northern Thailand showing 26 sampling sites in 7 provinces, including Chiang Mai, Chiang Rai, Lampang, Lamphun, Nan, Phare, and Phayao.
Fig. 2 Echinostoma revolutum. (A) The adult stage; permanent slide (A1) and drawing (A2). (B) Head collar revealing 37 collar spines. (C) A metacercaria, spherical in shape with double layer cyst wall and 37 collar spines.
Fig. 3 Echinostoma macrorchis. (A) The adult stage; permanent slide (A1) and drawing (A2). (B) Head collar with 45 collar spines. (C) A metacercaria, spherical in shape with double layer cyst wall and 45 collar spines.
Fig. 4 Comparison of sequence alignment of recovered E. revolutum and E. macrorchis with relative E. revolutum sequences in GenBank. (A) ITS2 region. (B) nad1 region.
Fig. 5 Phylogenetic trees of echinostomes in Upper Northern Thailand constructed based on ITS2 and nad1 sequences using maximum-likelihood (ML) and neighbor-joining (NJ) methods with 1,000 bootstrap replicates (NJ/ML). (A) ITS2 tree. (B) nad1 tree. NT1=E. revolutum adult from an experimental hamster fed the metacercariae from F. sumatrensis polygramma, NT2=E. revolutum metacercaria from F. martensi martensi, NT3=E. revolutum metacercaria from A. helena, NT4=E. revolutum metacercaria from B. puchella, NT5=E. revolutum metacercaria from B. siamensis, NT6=E. macrorchis adult from an experimental hamster fed with metacercariae from F. doliaris.

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

Morphology and Molecular Identification of Echinostoma revolutum and Echinostoma macrorchis in Freshwater Snails and Experimental Hamsters in Upper Northern Thailand

Locality of freshwater snails collected and the prevalence of echinostome infections in 26 sampling sites visited during 2017–2019 in upper northern Thailand

Provinces Districts Coordinates No. of snails examined No. of snails infected Prevalence (%)
Chiang Mai Hang Dong N 18.688800, E 98.955583 120 35 29.2
San Pa Tong N 18.599056, E 98.893472 143 68 47.6
Saraphi N 18.715167, E 99.040861 59 37 62.7
San Sai N 18.889160, E 99.001555 261 143 54.8
Mueang Chiang Mai N 18.859587, E 98.994790 140 16 11.4
Mae Rim N 18.896878, E 98.953528 125 28 22.4
Chiang Dao N 19.305276, E 98.966384 141 110 78.0
Mae Taeng N 19.143301, E 99.025522 38 9 23.7
Chiang Rai Wiang Pa Pao N 19.233538, E 99.503347 235 139 42.8
Mae Lao N 19.747362, E 99.682220 93 61 65.6
Phan N 19.583737, E 99.751051 222 56 25.2
Lampang Ko Kha N 18.859888, E 99.028305 112 15 13.4
Mueang Lampang N 18.339150, E 99.459369 220 23 10.4
Hang Chat N 18.327069, E 99.333365 307 119 38.8
Lamphun Mueang Lamphun N 18.591028, E 98.980222 280 119 42.5
Ban Thi N 18.630833, E 99.061417 292 147 50.3
Nan Wiang Sa N 18.484345, E 100.276411 30 4 13.3
Pua N 19.204124, E 100.945112 82 0 0
Mueang Nan N 18.733461, E 100.755168 118 30 25.4
Phare Rong Kwang N 18.303010, E 100.276411 64 64 100
Mueang Phrae N 18.249302, E 100.226446 83 55 66.3
Long N 18.070891, E 99.8021482 55 16 29.1
Phayao Mae Chai N 19.364023, E 99.813176 65 0 0
Dok Khamtai N 19.170412, E 100.017933 158 98 62.0
Phu Kamyao N 19.329287, E 99.790809 69 4 5.8
Mueang Phayao N 19.207747, E 99.943945 103 100 97.1

Prevalence and intensity of echinostome metacercariae in each species of freshwater snails randomly collected from upper northern Thailand

Family Species of snails No. of snails examined No. of snails infected Prevalence (%) Intensity
Viviparidae Filopaludina martensi martensi 1,337 293 21.9 10.3
Filopaludina doliaris 1,042 529 50.8 15.2
Filopaludina sumatrensis polygramma 1,032 633 61.3 18.3
Bithyniidae Bithynia siamensis siamensis 103 15 14.5 3.4
Bithynia pulchella 50 19 38.0 2.7
Nassariidae Anenthome helena 141 7 4.9 20.0
Total 3,705 1,496 40.4 15.2

The worm recovery of echinostome adults from hamsters experimentally infected with metacercariae from each species of snails at week 2 post-infection

Species of snail No. of metacercariae fed to hamster No. of adults obtained from hamster Worm recovery rate (%)
F. martensi martensi 60 0 0
F. doliaris 60 12 20.0
F. sumatrensis polygramma 60 10 16.7
B. siamensis siamensis 10 0 0
B. pulchella 10 0 0
A. helena 5 0 0

Comparative features and measurements (μm) of Echinostoma macrorchis adults recovered from various experimental hosts infected with the metacercariae

Details This study (Thailand) Lo (1995) (Taiwan) Sohn et al. (2013) (Lao PDR) Sohn et al. (2017) (Korea) Sohn et al. (2019) (Lao PDR)
No. of specimens 12 20 10 40 -
Experimental host hamster rat rat rat mouse
Period after infection 2 weeks 1 week 2 weeks 2–4 weeks 2 weeks
No. collar spines 45 - 43–45 45 43
Body (L) 4,200–5,900 (4,930) 3,650–5,050 3,900–4,730 3,950–6,000 (5,167) 3,250–4,275 (3,670)
 (W) 780–930 (850) 680–900 730–880 700–1,175 (939) 600–800 (713)
Oral sucker (L) 110–140 (120) 100–170 100–160 105–150 (123) 103–130 (115)
 (W) 100–160 (130) in diameter in diameter 150–185 (167) 118–158 (138)
Pharynx (L) 110–200 (150) 120–150 100–150 130–165 (150) 108–138 (121)
 (W) 80–160 (110) in diameter in diameter 95–130 (115) 78–108 (95)
Esophagus (L) 70–190 (150) 120–210 100–170 95–175 (135) 88–183 (142)
Ventral sucker (L) 420–550 (470) 400–490 390–470 395–490 (441) 350–435 (391)
 (W) 400–590 (460) in diameter in diameter 405–490 (447) 385–430 (403)
Ovary (L) 200–300 (260) 170–350 170–260 150–290 (227) 150–200 (175)
 (W) 190–310 (240) in diameter in diameter 160–335 (250) 150–225 (184)
Anterior testis (L) 550–810 (620) 440–750 500–700 460–990 (701) 425–650 (499)
 (W) 370–500 (430) 250–450 330–450 270–630 (427) 225–375 (314)
Posterior testis (L) 620–980 (760) 400–850 540–830 550–1,080 (821) 400–750 (556)
 (W) 350–490 (410) 240–440 330–420 280–550 (401) 225–340 (301)
Table 1 Locality of freshwater snails collected and the prevalence of echinostome infections in 26 sampling sites visited during 2017–2019 in upper northern Thailand
Table 2 Prevalence and intensity of echinostome metacercariae in each species of freshwater snails randomly collected from upper northern Thailand
Table 3 The worm recovery of echinostome adults from hamsters experimentally infected with metacercariae from each species of snails at week 2 post-infection
Table 4 Comparative features and measurements (μm) of Echinostoma macrorchis adults recovered from various experimental hosts infected with the metacercariae

Table 1

Table 2

Table 3

Table 4

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