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Hypolobocera Guayaquilensis (Decapoda: Pseudothelphusidae): a New Crab Intermediate Host of Paragonimus Mexicanus in Manabí Province, Ecuador

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Hypolobocera Guayaquilensis (Decapoda: Pseudothelphusidae): a New Crab Intermediate Host of Paragonimus Mexicanus in Manabí Province, Ecuador ISSN (Print) 0023-4001 ISSN (Online) 1738-0006 Korean J Parasitol Vol. 56, No. 2: 189-194, April 2018 ▣ ORIGINAL ARTICLE https://doi.org/10.3347/kjp.2018.56.2.189 Hypolobocera guayaquilensis (Decapoda: Pseudothelphusidae): A New Crab Intermediate Host of Paragonimus mexicanus in Manabí Province, Ecuador 1 2 3 4 5, Manuel Calvopina , Daniel Romero-Alvarez , Melina Rendon , Hidekazu Takagi , Hiromu Sugiyama * 1OneHealth Group, Escuela de Medicina, Facultad de Ciencias de la Salud, Universidad de las Americas (UDLA), Quito, Ecuador; 2Department of Ecology and Evolutionary Biology-Biodiversity Institute, University of Kansas, Lawrence, Kansas, USA; 3Facultad de Ciencias Biologicas, Universidad Central del Ecuador, Quito, Ecuador; 4Department of Microbiology and Immunology, Aichi Medical University School of Medicine, Aichi, Japan; 5Department of Parasitology, National Institute of Infectious Diseases, Tokyo, Japan Abstract: To determine that Paragonimus sp. is actively transmitted in a tropical area of the Pacific region of Ecuador where human cases of pulmonary paragonimiasis have recently been documented, a total of 75 freshwater crabs were collected from 2 different streams in the Pedernales area of Manabí Province, Ecuador. All collected crabs were identified as Hypolobocera guayaquilensis based on morphological characteristics of the male gonopods. The hepatopancreas of each crab was examined by compressing it between 2 glass plates followed by observation under a stereomicroscope. Excysted Paragonimus metacercariae were detected in 39 (52.0%) crabs and their densities varied from 1 to 32 per in- fected crab. There was a positive relationship between crab size and metacercarial density. Sequences of the second in- ternal transcribed spacer region of the ribosomal RNA gene of the Paragonimus metacercariae obtained in this study were identical to those of Paragonimus mexicanus deposited in the DDBJ/EMBL/GenBank database. Thus, the present study is the first to confirm that the crab species H. guayaquilensis is the second intermediate host of P. mexicanus in Manabí Province, Ecuador. Because this crab might be the possible source of human infections in this area, residents should pay attention to improper crab-eating habits related with a neglected parasitic disease, i.e., paragonimiasis. Key words: Paragonimus mexicanus, Paragonimus kellicotti, Hypolobocera sp., crab, intermediate host, trematode, lung fluke, food-borne disease, PCR- RFLP, Ecuador INTRODUCTION and P. ecuadoriensis was recognized as possible cryptic/sibling species [5]. Paragonimus species are dispersed globally, but are most fre- In Ecuador, P. ecuadoriensis was described as a new species quently found in Asia, Africa, and the Americas, where nine of based on the distinct morphology of its ovary and testis in re- about 50 nominal species are known to infect humans. In the lation to that of P. mexicanus, Paragonimus inca, and Paragoni- USA, Paragonimus kellicotti is known to cause human illness, mus peruvianus [6]. However, further comparative studies re- while Paragonimus mexicanus is accepted as a pathogenic spe- vealed that P. ecuadoriensis is a junior synonym of P. mexicanus cies in Central and South American countries [1-3]. The meta- [4,7]. In Manabí Province, adult parasites obtained from ex- cercariae of P. mexicanus are unique in lacking a cyst wall, thus perimentally infected animals showed similar morphological being very motile inside the body of crab hosts [4]. Recent re- characteristics to P. mexicanus [3]. In Esmeraldas Province, bor- search on the scanning electron microscope-based morpho- dering Manabí, isolated metacercariae were also identified as P. logical and molecular features of Paragonimus metacercariae mexicanus by sequencing the second internal transcribed spacer from Mexico has evidenced P. mexicanus as a species complex, (ITS2) region of ribosomal RNA gene [2]. Two siblings showing pulmonary symptoms such as pro- Received 4 December 2017, revised 22 March 2018, accepted 2 April 2018. ductive coughs with bloody sputa were seen as outpatients in • Corresponding author ([email protected]) * a hospital in Quito. They came from the Pedernales area in © 2018, Korean Society for Parasitology and Tropical Medicine Manabí Province and had a history of consuming under- This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) cooked freshwater crabs captured in tributaries of the Cheve which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. River. Accordingly, they were both diagnosed with pulmonary 189 190 Korean J Parasitol Vol. 56, No. 2: 189-194, April 2018 paragonimiasis and then successfully treated. The discovery of Examination of crabs for Paragonimus metacercariae these cases prompted us to carry out an intensive field survey The crabs were sacrificed using thermal shock by immersing around the Cheve River to determine (1) the presence of active them in water at about 2˚C for 10 min [9]. Then, the genitalia transmission of Paragonimus in the area, (2) the Paragonimus of each crab was examined for gender and species identifica- sp. involved, and (3) the identification of crab hosts and their tion. Next, the maximum width of the carapace was measured respective infection rate, which are presented in this study. using a caliper. After that, the carapace was removed from the posterior end of the body and only the hepatopancreas was MATERIALS AND METHODS removed as previously described [10]. The hepatopancreas was finally compressed between 2 glass plates (6×10 ×0.2 cm), Study site and crab collection which were examined under a dissecting microscope (CRX-32, Freshwater crabs, Hypolobacera guayaquilensis, were collected Olympus, Tokyo, Japan). When Paragonimus metacercariae by local people in August 2011 in 2 tributary streams of the were detected, the glass plate was carefully removed to recover Cheve River flowing through the Pedernales area of Manabí the metacercariae using teasing needles or tweezers. The isolat- Province, northwestern Pacific Coast of Ecuador (Fig. 1). This ed metacercariae were transferred into a Petri dish containing region, located between 120 and 500 m above sea level, and physiological saline solution using a capillary pipet. After tak- at latitude 0.138633˚ N and longitude 79.874267˚ W, is a sea- ing photographs under a microscope (DP71, Olympus), Para- sonal green forest of the Equatorial Pacific Coast Range in gonimus metacercariae were preserved in 70% ethanol for mo- Chongon-Colonche Mountains. Selected geographical areas lecular analysis. are dedicated to agriculture and cattle ranching [8]. To collect crabs, an active search was performed in advance Molecular identification of metacercariae in the 2 tributaries of the Cheve River, which descends from The molecular characterization of the metacercariae was the mountains. Shallow and slowly flowing streams with performed by DNA isolation, amplification of the ITS2 region rocky and muddy areas are the typical habitats where crab bur- by PCR, and PCR-restriction fragment length polymorphism rows are found. Collected crabs were transferred to the labora- (PCR-RFLP); all processed material was sequenced as previ- tories in Quito and maintained alive in 20-L plastic containers ously described [9]. Specifically, the primers used for PCR am- with 2 L of river water at about 25˚C (room temperature) until plification and sequencing were 3S (forward, 5´-GGTACCG- examined. GTGGATCACTCGGCTCGTG-3´; [11]) and A28 (reverse, 5´-GGGATCCTGGTTAGTTTCTTTTCCTCCGC-3´; [12]). The 80˚W Collection site Colombia Cheve-medio Nalpe Pedernales Rivers 0 5 km canton Manabi Tabiaza river Cheve river Pacific ocean Altitude -10 - 625 625-1,434 Peru Pedernales 1,435-2,319 Vite river 2,320-3,245 town 0˚ 3,246-6,169 Fig. 1. Map of the study area in the Pedernales area, Manabí Province, Ecuador. The Cheve River, collection site, and Cheve Medio com- munity are indicated in the left panel. Cheve Medio is located -20 km inland from nearby Pedernales on the coast of the Pacific Ocean. Calvopina et al.: A new crab intermediate host of P. mexicanus in Ecuador 191 PCR amplification was conducted using 0.25 µM of each prim- Ethics er and 2.5 U of Phusion High-Fidelity DNA Polymerase (Ther- Ethical approval of the study was given by the Ethics Com- mo Fisher Scientific, Waltham, Massachusetts, USA). The PCR mittee of the Universidad Central del Ecuador (License num- was carried out on a thermal cycler (TaKaRa PCR Thermal Cy- ber LEC IORG 0001932, FWA 2482, IRB 2483.COBI-AM- cler Dice Gradient, Takara Bio, Shiga, Japan), with 30 cycles of PHI-0064-11). 98˚C for 10 sec, 55˚C for 10 sec, and 72˚C for 15 sec. An initial denaturation and final extension were performed at 98˚C for RESULTS 30 sec and at 72˚C for 7 min, respectively. For the PCR-RFLP, 10-µl portions of the amplified products were treated with 5 U Of a total of 75 crabs examined, 50 were males (66.7%) and of the restriction enzyme Hinc II (New England Biolabs, Ips- 25 were females (33.3%). All male crabs had gonopods with wich, Massachusetts, USA) at 37˚C for 1 hr. Then, the ampli- morphological features characteristic H. guayaquilensis. The av- cons with or without enzymatic treatment were separated by erage carapace size of the 75 crabs was 3.5 cm ( ±1.18 cm, electrophoresis on 2% (w/v) agarose gels. All amplified prod- SD), ranging from 1.3 to 5.7 cm. Of the 75 crabs, 39 (52.0%) ucts were sequenced using the corresponding primers and the were infected with Paragonimus metacercariae. Of these crabs, BigDye Terminator v3.1 Cycle Sequencing Kit (Thermo Fisher 24 (32.0%) were males and 15 (20.0%) were females; no sta- Scientific) on an automated sequencer (3730xl DNA Analyzer, tistically significant relationship was detected between crab Thermo Fisher Scientific). Sequences were aligned and com- gender and metacercarial presence (P =0.46; Table 1). pared using GENETYX-Win software (Ver.
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