Abstract
Histopathological alterations caused by Thaparocleidus vistulensis (Siwak, 1932) on the European catfish Silurus glanis Linnaeus, 1758 were investigated by histopathology and scanning electron microscopy (SEM). The pathological effects of T. vistulensis on the gills of the European catfish were mainly related to the attachment sites of the parasite to its host, but damage also affected adjacent structures. The primary attachment relies on the anchors at the opisthaptor which commonly adheres both superficially and deeply, into the basal region between adjacent secondary lamellae. At the attachment sites, the haptoral disc of the parasites formed deep concave cup-like depressions on the surface of the gill lamellae. Deep anchor penetration occasionally distorted the extracellular cartilaginous matrix and induced a marked proliferation of epithelial tissue. Epithelial hyperplasia leading to lamellar fusion and subsequent extravasated erythrocytes in the gill lamellae was also observed. The damage caused by the parasites also led to the fusion of lamellae at the tips of the heavily infected gill filaments, forming club-like structures. Epithelial eosinophilic granular cells were frequently observed at the attachment sites. The pathological changes caused by this monopisthocotylan parasite frame the need to implement effective management strategies for controlling T. vistulensis infections in farmed European catfish populations.
Introduction
Monopisthocotyla and Polyopisthocotyla have recently been suggested as new classes, suppressing Monogenea as the conventional terminology (Brabec et al., 2023). The diversity in anatomy, physiology, and the most crucial feeding behaviour of these two classes has substantial implications for their impact on their host; the monopisthocotylans primarily feed on epithelial tissues, whereas the polyopisthocotylans feed on blood (Buchmann and Bresciani, 2006). Most monopisthocotylans and polyopisthocotylans are browsers that move freely on their host (i.e., body surface, fins and gills) and can be transmitted within a population speedily due to their direct life cycle and short-generation time (Bychowsky, 1957; Turgut and Akin, 2003). In aquaculture, where farms are often characterized by high host density, infection of these parasites often progresses to a disease situation (Bauer, 1987; Bakke et al., 2002; Buchmann and Lindenstrøm, 2002), which may cause severe mortality (Thoney and Hargis, 1991; Cone, 1995; Ogawa, 1996; Bondad-Reantaso et al., 2005; Shirakashi et al., 2006).
Monopisthocotylans infect economically important fish including anguillids, salmonids, cyprinids, ictalurids, clariids, fundulids, poeciliids, gasterosteids, cyclopterids, cichlids and pleuronectids (Thoney and Hargis, 1991). Among monopisthocotylans, Thaparocleidus vistulensis (Siwak, 1932) is one of the most pathogenic ectoparasites of European catfish Silurus glanis Linnaeus, 1758 in aquaculture (Wan Sajiri et al., 2023). The congeneric species Thaparocleidus siluri and Thaparocleidus magnus mainly occur in wild populations of this fish (Molnár, 1968, 1980; Székely and Molnár, 1990; Molnár et al., 2019). Although they are often found in mixed infections with other parasites (Soylu, 2005; Akmirza and Yardimci, 2014; Roohi et al., 2014), the monopisthocotylan T. vistulensis is capable of causing mortalities of European catfish alone (Papp, 1955; Molnár, 1980). Similar to most monopisthocotylans, T. vistulensis uses its opisthaptor as the primary attachment apparatus during the infection of the host (Molnár, 1980; Wan Sajiri et al., 2024). The mechanical action of anchors and marginal hooklets penetrating host gill structures is believed to elicit inflammation of the epithelium of the primary and secondary lamellae (Dezfuli et al., 2007). Additionally, lifestyle habits involve consuming cells detached from ruptured tissue or browsing on the gills, removing epithelial cells leading to localized haemorrhages (Bauer, 1987; Buchmann, 2012; Madanire-Moyo and Avenant-Oldewage, 2015).
Histopathological investigations regarding the effects of monopisthocotylans on gills have already been done on various important freshwater fish, for instance, the pike perch Sander lucioperca (see Molnár et al., 2016), the European eel Anguilla anguilla (see Abdelmonem et al., 2010; Buchmann, 2012), the grass carp Ctenopharyngodon idella (see Molnár, 1972) and the common carp Cyprinus carpio (see Jalali and Barzegar, 2005). However, Paladini et al. (2008) and Reading et al. (2012) have reported pathogenic effects associated with T. vistulensis on its hosts, noting a lack of previous histopathological studies. Molnár (1980) conducted a study which seems to have been overlooked by the above authors, that pointed to the need for further investigation to validate and expand upon the histopathological impacts of T. vistulensis infections in European catfish. This current study highlights the impact of T. vistulensis on the gills of European catfish using histopathology methods and demonstrates its effects using advanced scanning electron microscope (SEM) techniques.
Materials and methods
Fish and parasite collection
European catfish naturally infected with T. vistulensis were obtained from a commercial fish farm in Hungary and transferred in oxygenated water to the Veterinary Medical Research Institute in Budapest, Hungary (HUN-REN VMRI). Then fish were kept in a flow-through tank system (60 L) and subsequently euthanised by severing the brain and the spinal cord posterior to the cranium. The gills were removed using surgical scissors and forceps and examined for the presence of parasites under a stereo microscope (Olympus SZ40, Olympus Optical, Tokyo, Japan). Parasites were removed and identified using standard procedures as described by Siwak (1932) and redescribed by Bychowsky and Nagibina (1957), Paladini et al. (2008) and Wan Sajiri et al. (2024). Heavily infected gill arches were preserved in 5% buffered formalin for histopathological investigation and scanning electron microscopy studies.
Histology
Formalin-fixed gill arches were processed using standard histology techniques: they were dehydrated in a graded ethanol series, cleared in xylene and embedded in paraffin, which was then sectioned using a Leica RM 2135 (Nussloch, Germany) microtome at 5 µm. The paraffin-embedded sections were placed on glass slides and dried at 40 °C for 24 h. After deparaffinizing in xylene and rehydration in a graded ethanol series, the sections were stained with haematoxylin and eosin (H&E) and mounted in a DPX histology medium. Stained sections were examined using different magnifications by an Olympus BX53 light microscope and photomicrographs were captured (Olympus DP74 digital camera).
Scanning electron microscope (SEM)
Preserved gills and parasites in formalin were prepared separately for SEM by dehydrating through the ascending concentrations of ethanol series and transferred to hexamethyldisilazane (Merck and Co., Darmstadt, Germany) as described by Wan Sajiri et al. (2024). The dehydrated specimens were placed on a carbon-conductive double-sided tape, mounted to an aluminium stub and sputter-coated with gold using a Leica EM ACE200 Vacuum Coater (Leica, Wetzlar, Germany). Prepared specimens were examined with an FEI Quanta 200 SEM (FEI Company, Hillsboro, Oregon, United States) at 3–8 kV acceleration voltage and images were taken using xT Microscope Control software.
Results
SEM of gills infected with T. vistulensis
The primary attachment apparatus of T. vistulensis is the opisthaptor (Fig. 1), equipped with haptoral sclerotized structures, whereas the prohaptor can facilitate temporary attachment. The parasites were commonly attached between two gill-lamellae exploiting completely their sharp, pointed dorsal and ventral anchors to penetrate as far as possible into the gill tissue of their hosts, which was further reinforced by the marginal hooklets that secured a firm attachment at the margin of the opisthaptor. The opisthaptor was commonly attached superficially (Fig. 1A) as well as basally to the filaments (Fig. 1B), causing deep concave cup-like depressions on the surface of the gill lamellae.
SEM of Thaparocleidus vistulensis (p) attachment on gills using opisthaptor (oh) causing concave cup-like deep hollows and deformation on the surface of the gill lamella of Silurus glanis (arrow). (A) superficial attachment; (B) deep attachment. Scale bars represents 100 μm
Citation: Acta Veterinaria Hungarica 73, 1; 10.1556/004.2025.01121
Histopathological effects of T. vistulensis infection on gills
The histopathological examination revealed significant cell proliferation and diffuse epithelial hyperplasia, leading to lamellar fusion and subsequently extravasated erythrocytes in the gill lamellae. In some cases, the epithelial disintegration led to desquamation and released erythrocytes were observed within the excess mucus between filaments in certain areas (Fig. 2). In heavily infected gills, a row or a cluster of filaments with club tips was commonly observed (Fig. 3) and free sera occasionally with coagulated blood cells between the gill filaments (Fig. 4). The presence of eosinophilic granular cells was commonly detected, particularly at the sites where the anchor of the parasite penetrated the gill lamellae (Fig. 5).
Light micrograph of a cross section of gills infested by Thaparocleidus vistulensis (p) showing lamellar proliferation, diffuse epithelial hyperplasia (hp), extravasated erythrocytes in the lamella capillaries (hollow arrow), excess mucus (star) and extravascular erythrocytes escaping from the circulatory system (arrow) and epithelial desquamation (red arrow). Haematoxylin and eosin (H&E) staining. Scale bar represents 100 μm
Citation: Acta Veterinaria Hungarica 73, 1; 10.1556/004.2025.01121
Light micrograph of a cross section of gills infested by Thaparocleidus vistulensis (p) illustrating clubbed filament tips with lamellar fusion (arrow). H&E staining. Scale bar represents 100 μm
Citation: Acta Veterinaria Hungarica 73, 1; 10.1556/004.2025.01121
Light micrograph of a cross section of gills infested by Thaparocleidus vistulensis (p), with serum coagulating between gill filaments (star). H&E staining. Scale bar represents 50 μm
Citation: Acta Veterinaria Hungarica 73, 1; 10.1556/004.2025.01121
Light micrograph of a cross section of gills infested by Thaparocleidus vistulensis (p) showing eosinophilic granular cell at the anchoring sites (arrow). H&E staining. Scale bar represents 20 μm
Citation: Acta Veterinaria Hungarica 73, 1; 10.1556/004.2025.01121
Infection by T. vistulensis caused depression of the epithelium due to anchor penetration, and in some cases, the parasite's body exerted pressure on the gill lamellae (Fig. 6A). The piercing of gill lamellae caused by anchors and marginal hooklets also led to rupture of epithelial tissue, loss of definitive cellular characteristics and lamellar integrity. Tissue debris and epithelial cells could be identified in the oral cavities and intestines of parasites (Fig. 6A). Sometimes, deeper anchor penetration affected the extracellular cartilaginous matrix, occasionally reaching the core of the matrix, touching the chondrocytes of the gill rays and causing distortion primarily in the extracellular cartilaginous matrix (Fig. 6B).
Light micrograph of a cross section of gills infested by Thaparocleidus vistulensis (p) showing dorsal anchors (da) penetrating basally between adjacent secondary lamellae. (A) Depression on lamellae due to T. vistulensis anchor and body (hollow arrow) and gill debris inside the parasite is highlighted (star); (B) Distortion of the extracellular cartilaginous matrix (arrow). H&E staining. Scale bars represent 20 μm
Citation: Acta Veterinaria Hungarica 73, 1; 10.1556/004.2025.01121
Discussion
This study extended the investigations of our previous paper (Wan Sajiri et al., 2024), that had highlighted the early development of the sclerotized anchor and identified critical characteristics of T. vistulensis, particularly in relation to the shape and size of the anchors and copulatory organs. Additionally, we have provided molecular data therein for the species for the first time. In this study, we investigated the effects of T. vistulensis infestation on the gills of European catfish through histopathological observation. While many of the histopathological effects have been thoroughly explored by Molnár (1980), we employed advanced microscopy techniques (i.e. SEM) and discussed additional findings, providing a more detailed analysis of the parasite's impact on gill structure.
T. vistulensis causes damage to the host gills when it attaches and feeds resulting in mechanical rupture and loss of gill tissue. The attachment of T. vistulensis, which typically anchors itself between the gill lamellae of the European catfish, is mainly achieved using the ventral and dorsal anchors and is further strengthened with the fixation of marginal hooklets. Various monopisthocotylans, for instance, Macrogyrodactylus clarii on Clarias gariepinus (Arafa et al., 2009), Cichlidogyrus spp. on Oreochromis niloticus (El-Naggar et al., 2001), Paradactylogyrus sp. on Labeo rohita (Kaur and Shrivastav, 2014), and Cichlidogyrus philander on Pseudocrenilabrus philander (Igeh and Avenant-Oldewage, 2020) insert their anchors into the interlamellar gill epithelium of their hosts. Anchors in some species may even penetrate and distort the extracellular cartilaginous matrix of the gills (Kaur and Shrivastav, 2014; Igeh and Avenant-Oldewage, 2020). Molnár (1980) found that Ancylodiscoides vistulensis (syn. T. vistulensis) attaches between two adjacent lamellae, on one side with the dorsal pair of anchors, and to the other side with the ventral pair. In the same study, the author has also reported that the anchors often sunk as deep as the cartilaginous supporting structure of the gill filament. Our study found similar dispositions to those reported by Molnár (1980). Additionally, we revealed that distortion of the gills occurred when the anchors penetrated deeply into the gill lamellae, reaching and distorting the (core) extracellular cartilaginous matrix. The SEM study supported the histopathological observation, which showed the opisthaptor of individuals T. vistulensis embedded entirely into the proliferating gills.
T. vistulensis can cause lesions and Molnár (1980) has extensively discussed the histopathological changes caused by T. vistulensis on the gills of the European catfish, including epithelial cell proliferation, diffuse epithelial hyperplasia of gill filaments and capillary haemorrhages, which are all in agreement with our observations. The tissue damage we observed predominantly occurs in areas where the anchors penetrate the gills, causing rupture of the epithelial tissue and definitive cellular changes. This pathology is caused by the pressure and compression created by the penetration of the anchors and marginal hooklets into the gill epithelium and the contact between the parasite's body and the secondary gill lamellae. Arafa et al. (2009), and Igeh and Avenant-Oldewage (2020) have documented similar compression in the gills of C. gariepinus infected with M. clarii and P. philander infected with C. philander. Arafa et al. (2009) have noted that attachment by the haptor caused neighbouring gill lamellae to be compressed and tightly packed, leading to an abnormal appearance of the gills. Our SEM findings revealed an atypical appearance of the gills, characterized by deep concave cup-like hollow surface deformations. The indentation formed by the opisthaptor on the gill lamellae may exert pressure on the blood vessel walls, potentially causing stasis and rupture. The destruction of lamellae and clubbing would diminish the gill surface area available for gaseous exchange and decrease the fish's respiratory capacity.
The pathological changes observed in this study also resemble those documented by Molnár (1972) (Dactylogyrus lamellatus infecting C. idella), Buchmann (2012) (Pseudodactylogyrus anguillae and P. bini infecting A. Anguilla), Molnár et al. (2016) (Ancyrocephalus paradoxus infecting S. lucioperca), Arya and Singh (2020) (Mizelleus indicus infecting Wallago attu) and Igeh and Avenant-Oldewage (2020) (C. philander infecting P. philander), who also reported hyperplasia of the epithelial cells and the subsequent fusion of lamellae, which represent a key feature of the parasitic infection. The intensive proliferation of interlamellar epithelia thickened the secondary lamellae with damaged capillaries deeply embedded in the hyperplastic tissue. Clubbing at the tip of filaments of heavily infected gills was also observed where a row or group of filaments was affected. Clubbing manifested as extensive epithelial hyperplasia, infiltrated with numerous epithelioid cells and varying numbers of small mononuclear cells. These histopathological changes proved to be less frequent and severe than Molnár (1980) had reported, where several filaments were fused. Buchmann (2012) has also observed analogous pathological host responses in A. anguilla infected with P. anguillae and P. bini, including hyperplasia of mucous cells and gill epithelial cells, excess mucus production and fusion of gill lamellae resulting in clubbing of filaments. These gill changes result from the host's defence mechanisms (Reda and El-Naggar, 2003; Vankara et al., 2022).
While most authors have stated the increase in the number of mucus cells (Buchmann, 2012; Arya and Singh, 2020; Igeh and Avenant-Oldewage, 2020; Vankara et al., 2022) and goblet cells (Reda and El-Naggar, 2003; Molnár et al., 2016) in response to monogenean infection around the infected tissue filaments, our observations revealed that, although mucus cells are present in the space between the filaments, goblet cells seemed to be noticeably absent. This phenomenon is consistent with the findings of Molnár (1980), who had observed the disappearance of goblet cells. Typically, when parasitic infection occurs on the host, the immune system often triggers an inflammatory response, including activation of the mucus and goblet cells. The infection may trigger these cells to produce more mucins that act as a barrier to protect the epithelial surfaces from further damage and expel the parasites (Gomez et al., 2013). However, the absence of goblet cells was not evident in the present study. We hypothesized that some parasite-produced substances may specifically impede the function or regeneration of the goblet cells, resulting in their depletion or disappearance in the infected area (Xian et al., 1999) or consequence of the host's immune response (Bergstrom et al., 2008). Further exploratory research is required to clarify the underlying process and understand the fundamental mechanisms that define goblet cell dynamics in the gills of European catfish. However, we agreed that the mucoid material observed mainly originates from the cytoplasmic remnants of disrupted cells and the destroyed vascular network, as previously described by Paperna (1964) and Molnár (1972). On the other hand, our observations differed somewhat from those of Molnár (1980), especially with regard to eosinophilic granular cells. While he had not demonstrated an increase in the amount of these cells, our observation indicated their enrichment, especially at the anchoring sites of T. vistulensis.
Acknowledgements
The authors are indebted to Ms. Györgyi Pataki for the histological slides. The authors express their gratitude to Dr. Sebastian Kjeldgaard-Nintemann for his assistance with SEM. Also, thanks to Ms. Virág Marek for maintaining fish in the laboratory. This project was funded by the European Union's Horizon 2020 research and innovation program under Marie Sklodowska-Curie grant agreement No. 956481.
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