Histopathological and ultrastructural observations of metacercarial infections of Diplostomum phoxini (Digenea) in the brain of minnows Phoxinus phoxinus

Abstract

The spatial distribution and histopathological changes induced by metacercariae of the digenean trematode Diplostomum phoxini (Faust, 1918) in the brains of European minnows Phoxinus phoxinus (L.) from the River Endrick, Scotland, were studied by light and electron microscopy. Postmortem examination of a sample of 34 minnows revealed that 50% (n = 17) of the population was infected with 13.7 ± 2.6 (mean ± SE; range 1 to 38) metacercariae per infected host. Serial histological sections of the infected minnow brains revealed that the metacercariae were unevenly distributed throughout the brain, with aggregations occurring in the cerebellum, the medulla oblongata and the optic lobes. In fish with highest intensities of infection, over 40% of the cerebellar area and about 30% of the medulla oblongata area were occupied by larvae. Metacercariae disrupt the integrity of brain tissue, with individuals being found in small pockets surrounded by cellular debris. Metacercariae were rarely encountered on the surface of the brain. Electron microscopic examination of infection sites revealed that the granular layer surrounding metacercariae was necrotic, exhibited nuclear degradation and was marked by vacuolation of the cytoplasm. Rodlet cells, the only inflammatory cell types recorded in this study, were found only in parasitized brains and in close proximity to the teguments of metacercariae. It is hypothesised that secretions released from the teguments of metacercariae are a counter response to protect the metacercariae from the fish brain's cellular defence mechanisms. KEY WORDS: Brain infection · Digenean trematode · Phoxinus phoxinus · Rodlet cells · Histopathology · Ultrastructure Resale or republication not permitted without written consent of the publisherDis Aquat Org 75: [51][52][53][54][55][56][57][58][59] 2007 gata and the optic lobes, centres of the brain that are responsible for host motor activity, sensory functions and vision (Barber et al. 2000, Shirakashi & Goater 2005. Until recently, metacercariae were generally regarded as immature, non-feeding and metabolically inactive stages waiting for transmission to the next/ definitive host (Bush et al. 2001, Poulin & Latham 2003. However, a recent study by Goater et al. (2005) demonstrated via experimental infection that the metacercariae of Ornithodiplostomum ptychocheilus Faust, 1917 in Pimephales promelas Rafinesque, 1820 undergo a series of complex developmental changes associated with their feeding on host brain tissue.A histological examination of Phoxinus phoxinus heads in the current study revealed the presence of rodlet cells only in infected brains, notably in the epithelium lining the ventricles of the optic lobes. It is believed that rodlet cells play a role within the piscine inflammatory response (Dezfuli et al. 2000, Manera & Dezfuli 2004, Reite 2005, Reite & Evensen 2006. We found rodlet cells only within the infected brain of a fish, and our findings are briefly compared with the information available on their presence in other f...

Personality differences in two minnow populations that differ in their parasitism and predation risk

“…Earlier studies have shown that brain-encysting trematodes have the potential to alter host behavior (e.g., Lafferty and Morris, 1996;Goater, 2002, 2005;Kekäläinen et al, 2014a). In the brain, D. phoxini metacercariae are known to aggregate mainly in the cerebellum, the optic lobes and the medulla oblongata (Barber and Crompton, 1997a), where they cause pathological damage in the brain tissue (e.g., necrosis and disruption in the integrity of brain tissue, Dezfuli et al, 2007). This may cause manipulative effects as a means of increased boldness and thus lead to increased predation by the definitive avian host.…”

Immune response to nematode larvae in the liver and pancreas of minnow, Phoxinus phoxinus (L.)

“…Rodlet cells are characterized by a thick fibrous capsule, a basal nucleus and the conspicuous rodlets (Manera & Dezfuli 2004). Evidence for the possible function of these cells as immune cells was provided in studies reporting an increase in their number in fish infected with protozoan (Leino 1996; Dezfuli, Giari, Simoni, Shinn & Bosi 2004) and metazoan parasites (Dezfuli, Arrighi, Domeneghini & Bosi 2000b; Dezfuli, Capuano, Simoni, Giari & Shinn 2007).…”

“…In infected liver and pancreas of minnow, an increased presence of RC, MC, neutrophils, macrophages and fibroblasts was observed. Occurrence of RCs in reactive foci as a result of infection with micro‐ and macro‐parasites was reviewed by Manera & Dezfuli (2004) and there have been further reports on this topic (Bosi, Shinn, Giari, Simoni, Pironi & Dezfuli 2005; Dezfuli et al. 2007, 2008a; Jordanova, Miteva & Rocha 2007).…”

Chronic Pathology and Longevity of Drepanocephalus spathans Infections in Juvenile Channel Catfish

“…Encystment in the luminal surfaces of the buccal cavity and the gill arch is not limited to D. spathans (Anderson and Cribb 1994;Olsen and Pierce 1997;Vélez-Hernández et al 1998;Mitchell et al 2000), and neither is encystment in the cranial cavity. Metacercaria have been reported from the brian ventricles (Mueller 1972); the interlobular infoldings, ventricular cavities, and external meninges (Siegmund et al 1997); the cerebellum, medulla oblongata, and optic lobes (Barber and Crompton 1997;Dezfuli et al 2007); the cranial fluid surrounding the brain (Johnston and Halton 1981); the neural tissue within and on the surface of 216 GRIFFIN ET AL. the brain (Heckman 1992); tissues of the optic tecta and valvula cerebelli (Sandland and Goater 2001); and the adipose tissue surrounding the brain (Zhokhov et al 2010).…”