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Morphometric Characteristics of the Metacestode Echinococcus Vogeli Rausch & Bernstein, 1972 in Human Infections from the Northern Region of Brazil

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Morphometric Characteristics of the Metacestode Echinococcus Vogeli Rausch & Bernstein, 1972 in Human Infections from the Northern Region of Brazil Journal of Helminthology (2015) 89, 480–486 doi:10.1017/S0022149X14000376 q Cambridge University Press 2014 Morphometric characteristics of the metacestode Echinococcus vogeli Rausch & Bernstein, 1972 in human infections from the northern region of Brazil F. Almeida1, F. Oliveira1, R. Neves2, N. Siqueira3, R. Rodrigues-Silva1*, D. Daipert-Garcia1 and J.R. Machado-Silva2 1Laboratory of Helminth Parasites of Vertebrates, Oswaldo Cruz Institute, Av. Brasil 4365, Manguinhos, 21045-900, Rio de Janeiro, Brazil: 2Laboratory of Helminthology Romero Lascasas Porto, Department of Microbiology, Immunology and Parasitology, Faculty of Medical Sciences, Biomedical Centre, State University of Rio de Janeiro, Rua Prof. Manoel de Abreu 444/5 Floor, Vila Isabel, 20511-070, Rio de Janeiro, Brazil: 3Acre State Hospital Foundation and Federal University of Acre, Rodovia BR 364, s/n km 02, Distrito Industrial, Rio Branco, 69914-220, Acre, Brazil (Received 15 March 2013; Accepted 12 April 2014; First Published Online 22 May 2014) Abstract Polycystic echinococcosis, caused by the larval stage (metacestode) of the small-sized tapeworm, Echinococcus vogeli, is an emerging parasitic zoonosis of great public health concern in the humid tropical rainforests of South and Central America. Because morphological and morphometric characteristics of the metacestode are not well known, hydatid cysts from the liver and the mesentery were examined from patients following surgical procedures. Whole mounts of protoscoleces with rostellar hooks were examined under light and confocal laser scanning microscopy. Measurements were made of both large and small hooks, including the total area, total length, total width, blade area, blade length, blade width, handle area, handle length and handle width. The results confirmed the 1:1 arrangement of hooks in the rostellar pad and indicated, for the first time, that the morphometry of large and small rostellar hooks varies depending upon the site of infection. Light and confocal microscopy images displayed clusters of calcareous corpuscles in the protoscoleces. In conclusion, morphological features of large and small rostellar hooks of E. vogeli are adapted to a varied environment within the vertebrate host and such morphological changes in calcareous corpuscles occur at different stages in the maturation of metacestodes. Introduction disease worldwide, polycystic echinococcosis (PE) caused by E. vogeli is an emergent zoonosis of great public health Zoonotic larval cestode infections were recently significance in the humid and tropical rainforests of classified among the neglected tropical diseases (Budke South and Central America (D’Alessandro & Rausch, et al., 2009; WHO, 2012). While human echinococcosis 2008; Siqueira et al., 2010). Furthermore, the number of caused by E. granulosus is a serious life-threatening diagnosed cases of human PE may represent only the tip of the iceberg (D’Alessandro & Rausch, 2008). *Fax: þ 55-021-25621511 Echincoccus vogeli is considered to be the most E-mail: rsilva@ioc.fiocruz.br pathogenic species, responsible for a total of 179 reported Morphometrics of E. vogeli in human infections from Brazil 481 human cases in the past four decades (Knapp et al., 2009; Siqueira et al., 2010; Zegarra et al., 2010). Echinococcus vogeli is transmitted between canines, such as bush dogs (Speothos venaticus) and domestic dogs (Canis familiaris), that harbour the adult tapeworm, and rodents, such as the Agouti paca, that harbour E. vogeli during the larval cestode stage (D’Alessandro & Rausch, 2008). Wild canines become infected with E. vogeli through the consumption of infected pacas, which they hunt (Jenkins et al., 2005), while humans become infected accidentally after ingesting eggs present in canine faeces, which causes polycystic lesions that are found most frequently Fig. 1. Diagram of the rostellar hook of the protoscolex of in the liver and abdominal cavity (D’Alessandro & Echinococcus vogeli with measurements (mm) of the total Rausch, 2008). area (BA/HA), total width (TW), blade area (BA), blade width A number of studies have demonstrated that larval (BW), handle area (HA) and handle width (HW). hook morphology is a valid criterion, being faster and more cost effective than traditional techniques for the identification of E. granulosus (Gholami et al., 2011; Spring, Maryland, USA). For confocal laser scanning Mowlavi et al., 2012). Our previous study demonstrating microscopy (CLSM), protoscoleces were stained with the use of combining conventional and new morphologi- Langeron’s carmine. Whole mounts were examined cal tools, such as light microscopy, confocal laser scanning under a confocal microscope (LSM 510 – ZETA, Zeiss, microscopy, differential interference contrast and vari- Oberkochen, Germany) (Neves et al., 2004). All slides able-pressure scanning electron microscopy, helps were also examined under phase contrast by adding a prism to resolve matters in regard to protoscoleces from the (Zoom 3.8) to the laser scanning confocal microscope. E. granulosus metacestode (Almeida et al., 2009). However, Several linear measurements and areas of both large many of the phenotypic aspects of protoscoleces are and small hooks were analysed, including the total area, unknown. Parasitological diagnosis of human PE is based total length, total width, blade area, blade length, blade on morphometric features of rostellar hooks (D’Alessan- width, handle area, handle length and handle width dro & Rausch, 2008). The mean lengths of large and small (fig. 1). Images were captured with a digital camera hooks of E. vogeli are 41 and 33 mm respectively (Nikon Eclipse E200 camera; Nikon, Chiyoda, Japan) (D’Alessandro & Rausch, 2008). connected to a microscope (Olympus BX41 microscope; The aim of the present study was to extend our Olympus, Tokyo, Japan). The camera output was knowledge and understanding of E. vogeli with reference processed and analysed with Image Pro Plus 3 image to morphological and morphometric characteristics of the analysis software (Media Cybernetics). All measurements species, focusing on polymorphism of the rostellar hooks are in micrometres unless indicated otherwise. and the presence of calcareous corpuscles in the protoscolex. Data analysis Data analysis was carried out with GraphPad InStat Materials and methods (GraphPad Instat Software Inc. version 3.01, California, USA). Statistical analyses included analysis of variance Collection and examination of cysts (ANOVA) followed by a post-hoc Tukey’s test and Student’s The present investigation was carried out on hydatid t-test. Statistical significance was assessed at P # 0.05. cysts isolated from the livers and/or mesenteries of five female patients and three male patients, ranging in age Results from 4 to 49 years, from the cities of Feijo´ (0880905100S; 7082101300W), Sena Madureira (980305600S; 6883902500W), All microscopic techniques were necessary to examine Tarauaca´ (0880903900S; 7084505700W), Assis Brasil (1085602900S; the E. vogeli hooks and phenotypic aspects of proto- 6983400100W) and Pauini (0784205000S; 6685803300W) in the scoleces. Using light microscopy, it was possible to Amazonas and Acre states, Brazil. visualize some protoscoleces during different develop- Cysts were not pooled as each cyst was considered a mental stages and also visualize the high density single sample. The rostellar hooks of protoscoleces were and differential distribution of calcareous corpuscles aspirated under sterile conditions together with the (fig. 2A–D), which are mainly located close to the hydatid fluid from each cyst and then rinsed twice in a rostellar hooks (fig. 3A). In protoscoleces, no differences 0.85% NaCl solution. Each suspension of protoscoleces are shown in organization of the hooks (figs 2A and 3A). was passed through a sieve to remove larger debris. After There are two rows of hooks in the rostellar pad with a this step, the material was transferred and stored at room large hook intercalated by a small hook. Both large and temperature, in small tubes with 10% buffered formalin small rostellar hooks vary morphologically, although all (Almeida et al., 2007, 2009). hooks possess a handle, blade and guard (fig. 3B). Large For light microscopy, protoscoleces were mounted on and small hooks possess a central amorphous pulp glass slides coated with polyvinyl lactophenol and region. Large hooks frequently possess thin guards with crushed under a coverslip. Images were acquired using an irregular surface between the guard and the handle, Image Pro Plus software (Media Cybernetics Inc., Silver while small hooks are round and possess stout guards. 482 F. Almeida et al. Fig. 2. Echinococcus vogeli metacestode to show stages of (A) the invaginated protoscolex with the rostellar pad and calcareous corpuscles irregularly localized; (B) evaginated protoscolex with suckers ( ), rostellum (arrowhead), neck region (*) and a high density of calcareous corpuscles (arrow); (C) evaginated protoscolex with scolex (*), neck region (arrowhead), developing proglottid ( ) and cluster of calcareous corpuscles (arrow); (D) evaginated protoscolex showing the scolex with suckers (*), neck (arrowhead) with a lower density of calcareous corpuscles (arrow) than in (C) and the developing proglottid ( ). All scale bars ¼ 21 mm. In most cases, the surface between the guard and the When comparing hook measurements according to handle is irregular. The blade does not show any relevant the infected organ, hooks from the liver are larger for all features. parameters analysed, with
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