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Sonoparasitology: An alternative approach to parasite detection in sheep
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Small Ruminant Research xxx (2016) xxx–xxx
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Sonoparasitology: An alternative approach to parasite detection in sheep K. Arsenopoulos a , G.C. Fthenakis b , E. Papadopoulos a,∗ a b
Laboratory of Parasitology and Parasitic Diseases, School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece Veterinary Faculty, University of Thessaly, 43100 Karditsa, Greece
a r t i c l e
i n f o
Article history: Available online xxx Keywords: Coenurus cerebralis Cysticercus Diagnosis Echinococcus Fasciola Hydatid cyst Parasite Parasitic disease Ultrasound
a b s t r a c t Objective of the present review is to describe in a systematic way potential uses of ultrasonographic examination in diagnosis of parasitic diseases of sheep and to comment upon its potential usefulness in the health management of flocks. The technique has been primarily employed for diagnosis of hydatid disease in live sheep, by imaging lesions in the liver and/or the lungs of affected animals; this can be of potential value in health management of flocks, as other methods used to diagnose the disease may not have increased diagnostic accuracy. Further, the technique has been used for diagnosis of Fasciola infection, during the ductal phase, as well as for diagnosis of coenurosis. It is concluded that sonoparasitology should be considered as a diagnostic possibility of valuable potential for application in sheep. © 2016 Elsevier B.V. All rights reserved.
1. Introduction 1.1. Preamble Diagnostic approaches in parasitic infections of sheep are mainly driven by the localisation of parasites into the animal, thus, in live animals, the ability to detect the adult parasite itself (e.g., ectoparasites) or its various reproductive forms (i.e., eggs, larvae, oocysts); for example, skin scrapings are examined for detection of arthropods, blood smears are evaluated for detection of protozoa and faecal samples are processed for detection of eggs or larvae of gastrointestinal or respiratory helminthes. When sheep harbour immature or larval forms of parasites, no reproductive elements are produced; therefore, detection of parasites becomes more complicated and laborious. In such cases, diagnosis of infection would be based on application of other methods, often molecular or immunological techniques searching for (i) parasite genetic material (e.g., parasite DNA) or antigenic factors (e.g., Fasciola hepatica coproantigen; Adela Valero et al., 2009) or (ii) host-specific antibodies (e.g., anti-Toxoplasma antibodies), inflammatory cells (e.g., increased proportion of blood eosinophils during trichostrongylid infections) or enzymes (e.g., blood aspartate aminotransferase or ␥-glutamyl
transferase concentration in cases of liver trematode infections) among others. There are limitations in these approaches, of which the most significant one is that these techniques provide only indirect evidence regarding presence of parasites. Ultrasonographic examination may be of use for providing evidence for presence of parasites in a host, by imaging parasites (or some form of theirs) within the body of a sheep (direct evidence). That way, it supports the diagnosis of a parasitic disease, in a way similar to the detection of mites in skin scrapings or of eggs of trichostrongylids in faecal samples. The idea behind this approach is that parasitic formations can be visible by recording the reflections of ultrasonic waves directed into potentially parasitised tissues of sheep. Alternatively, lesions characteristically caused by a parasite (indirect evidence) may also be imaged. The findings, considered together with results of the above indirect techniques, may provide confirmatory evidence about parasitic infection in sheep, as well as providing simultaneously information regarding the condition of the affected organ in the animal. Objective of the present review is to describe in a systematic way potential uses of ultrasonographic examination in diagnosis of parasitic diseases of sheep and to comment upon its potential usefulness in the health management of flocks.
∗ Corresponding author. E-mail address: [email protected] (E. Papadopoulos). http://dx.doi.org/10.1016/j.smallrumres.2016.12.007 0921-4488/© 2016 Elsevier B.V. All rights reserved.
Please cite this article in press as: Arsenopoulos, K., et al., Sonoparasitology: An alternative approach to parasite detection in sheep. Small Ruminant Res. (2016), http://dx.doi.org/10.1016/j.smallrumres.2016.12.007
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1.2. Use of ultrasonographic examination in humans and animal species other than sheep In humans, ultrasonographic examination has become part of the standard examination for diagnosis of hydatid disease (cystic echinococcosis) (Stojkovic et al., 2012; Craig et al., 2015), which affects primarily the liver and less often the lungs of patients (Derfoufi et al., 2012). Further, by using the technique, the lesions can be allocated into active, transitional or inactive, which would be of help in the therapeutic management of patients and the prognosis of the disease (Wuestenberg et al., 2014). Further, ultrasonographic examination has been employed in diagnosis of schistosomiasis (especially of the chronic form of the disease), which is responsible for periportal fibrosis in the liver and abnormalities in the urinary system; the findings of the examination are characteristic and use of the technique has led to minimising the frequency of liver biopsy for diagnostic purposes (Cerri et al., 1984), as well as to efficient monitoring of lesions in the urinary system (King et al., 2003). Other parasitic infections causing tissue lesions have also been readily diagnosed by use of ultrasonographic examination. These include Fasciola infections (Bassily et al., 1989; Aksoy et al., 2005; Koc et al., 2009), where it could also guide therapeutic management of the disease (Alatoom et al., 2008), schistosomiosis (DoehringSchwerdtfeger and Kardorff, 1995), lymphatic filariosis (Poltera and Zak, 1988; Mand et al., 2005) and liver abscesses associated with Ascaris infections (Javid et al., 1999; Richter et al., 2003). In animal species other than sheep, ultrasonographic examination can be of value as an adjunct to clinical examination in adult horses, used to detect intra-arterial changes associated with Strongylus vulgaris infections (Wallace et al., 1989a,b,c), as well as in foals, used to detect the characteristic intestinal dilation with intraluminal presence of ascarids associated with Parascaris equorum infection (Tatz et al., 2012; Nielsen et al., 2016). The method has also been used in calves to detect distended and thickened small intestine associated with Toxocara vitulorum infection (Van Der Steen et al., 2014) and in pigs for diagnosis of hepatic schistosomosis (Kardorff et al., 2003). Finally, in dogs and cats, use of the method has been made (among others) for diagnosis of Dioctophyme renale infection in kidneys (Rahal et al., 2014) and of peritoneal cestodosis (Venco et al., 2005).
2. Use of ultrasonography for diagnosis of parasitic diseases of sheep 2.1. Hydatid disease Hydatid disease (or cystic echinococcosis) is caused by hydatid cysts, the larval stage of Echinococcus granulosus. Apart from being a wide-spread zoonotic infection, the disease causes significant adverse financial consequences, due to reduced production by affected animals and the condemnation of affected tissue at abattoirs (Torgerson, 2003). No clearly defined approach is available for diagnosis of the disease in the field in live sheep. Various diagnostic methods have been proposed, e.g., serological examination (Lightowlers et al., 1984; Khabiri et al., 2006). However, use of these methods is hindered by reduced accuracy (e.g., due to potential cross-reactions with other pathogenic agents) and increased cost. As the disease is characterised by development of cystic formations in tissues of sheep (liver, lungs), it has been proposed that these might be detected by ultrasonographic examination. The potential usefulness of ultrasonographic examination for diagnosis of hydatid disease in sheep has been first discussed by Craig (1993). The liver and the lungs are the organs that should be
imaged for detection of hydatid cysts (Scott, 2017a,b), which appear as round hypoechoic structures located in those organs (Guarnera et al., 2001). However, various factors may influence the results of ultrasonographic examination. These include number, size (1.06.0 cm) and developmental status (active) of the cysts, parasitised organ and localisation of cysts therein, as well as pressure applied by cysts on surrounding tissues (Sagkan-Ozturk et al., 2015). Sage et al. (1998) have reported 55% sensitivity and 98% specificity of the technique (compared to post-mortem findings) for detection of hydatid cysts in the liver or lungs of sheep. In a later study, Lahmar et al. (2007) used the technique to examine sheep in the field and have reported that prevalence of liver lesions caused by the parasite amounted to 40%; the authors commented that ultrasonographic examination detected deep or superficial cysts only localised in the central or left part, in relation to the caudal vena cava, of the liver, hence up to one-third of cysts present in animals could be missed by using the technique. More recently, Dore et al. (2014) used more advanced technology equipment and reported >80% sensitivity and specificity of ultrasonographic examination (compared to post-mortem findings) for detection of hydatid cysts in the liver or lungs of sheep; rates increased to 100% if only active cysts (which were better imaged) were considered. It is noteworthy that Guarnera et al. (2001) have reported false positive results during examination of the liver for hydatid cysts, caused by imaging Cysticercus tenuicollis (the larval stage of Taenia hydatigena). Dore et al. (2014) have indicated that cysticerci were more often localised on the surface of the liver, which could help in their differentiation from hydatid cysts, present in the deeper parts of the organ. 2.2. Trematode infections of the liver Liver trematodes, e.g., Fasciola spp., Dicrocoelium dentriticum, may cause severe disease in sheep. In general, diagnosis of the infection may be performed readily by parasitological examination of faecal samples. Nevertheless, the technique has some constraints, because only adult parasites produce eggs (during parasitism by immature stages of Fasciola, which migrate through the liver [parenchymal phase of the disease], no eggs are produced) and number of eggs detected in faecal samples does not correlate directly with number of parasites in the liver (number of eggs produced by Fasciola or D. dentriticum is influenced by a variety of factors, e.g., immunological state of the host animal). Further, extent of liver damage may be detected to some degree by measuring blood concentrations of enzymes indicative of hepatic function (e.g., aspartate aminotransferase or ␥-glutamyl transferase). Gonzalo-Orden et al. (2003) in experimentally induced fasciolosis in sheep have indicated that ultrasonographic examination did not reveal specific lesions during the parenchymal phase of the infection. In contrast, the technique could be valuable for diagnosis of the infection during the ductal phase, as it showed the trematodes moving within the dilated duct imaged as structures of increased echogenicity; no specific lesions were evident during the parenchymal phase of the infection; further, findings characteristic of the disease: hepatomegaly and presence of multiple hyperechoic spots within the liver parenchyma, representing accumulations of inflammatory cells, could also be seen. Scott et al. (2005) have also performed ultrasonographic examination of the liver of sheep with mild fasciolosis, which revealed multiple hyperechoic dots in the parenchyma, giving a granular appearance in the texture of the organ; the findings corresponded to the most advanced changes as determined by the size of the abscesses and their relatively mature fibrous capsules, and areas of hepatic necrosis. In infections with Dicrocoelium dentriticum, mild to severe hepatitis is developed in affected sheep. Ultrasonographic examination of the liver revealed enlarged and occasionally calcified bile ducts in
Please cite this article in press as: Arsenopoulos, K., et al., Sonoparasitology: An alternative approach to parasite detection in sheep. Small Ruminant Res. (2016), http://dx.doi.org/10.1016/j.smallrumres.2016.12.007
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affected animals (Dore et al., 2014). These findings may contribute to presumed identification (false positive results) of hydatid cysts in the liver (Dore et al., 2014). 2.3. Coenurosis Diagnosis of coenurosis can be best achieved by a combination of history of the problem, findings of detailed clinical examination (Scott, 2012), elimination of other disorders with similar presentation (e.g., listeriosis, louping-ill, sarcocystosis, polioencephalomalacia, brain abscessation) (Giadinis et al., 2013) and evaluation of cerebrospinal fluid samples (Scott, 2012), as there is a consistent association between increased eosinophil concentration in cerebrospinal fluid and parasitic infection of the central nervous system (Doherty et al., 1989; Tschuor et al., 2006). In a relevant report, Doherty et al. (1989) have used ultrasonographic examination for detection of parasitic cysts in the brain. The technique had been performed after a small incision of the head bone was performed and the cerebral cortex was exposed; on caudal angulation, a large cavity full of fluid was revealed. The method was further used for treatment: the fluid was drained by means of a needle and the cyst was finally removed, which led to recovery of the animal 10 days later. 3. Use of ultrasonography for diagnosis of parasitic diseases in sheep health management The primary use of ultrasonography in parasitic diseases of sheep would be its value for diagnosis of hydatid disease (cystic echinococcosis) in live animals. The studies of Sage et al. (1998) and Dore et al. (2014) have indicated that ultrasonographic examination of sheep for detection of hydatid cysts can be useful (i.e., practical, cost-effective and relatively accurate), hence it may be used instead of or coupled with serological examination of animals under evaluation (Craig et al., 2015). The method may be applied for screening sheep to detect lesions of cystic echinococcosis. This can provide evidence regarding the value of preventive measures taken to control the disease in a flock (e.g., anthelmintic treatment of dogs, minimising potential infections from wild canids (Vasileiou et al., 2015) etc. Further, in case of animals of particular value (e.g., breeding rams), appropriate treatment may be initiated, although in general efficacy of such schemes is not always 100% (Ceballos et al., 2013). It is noteworthy that during ultrasonographic examination, the transducer is brought in contact with many sheep. Hence, there may be a danger for transmission of parasitic agents, if animals were infected. The possibility can arise with mange mites, e.g., Sarcoptes scabiei (Papadopoulos et al., 2000), Psoroptes ovis (Losson, 2012), which can survive in objects (including transducers of the ultrasonographic equipment) and be transmitted to other sheep in the farm (ones scanned after the infested ones) or even to other farms (if inappropriate cleaning of the transducer would be performed). 4. Concluding remarks Ultrasonographic examination has been employed successfully for diagnosis of parasitic infections of sheep. Routine use of the method for diagnosis of hydatid disease in live animals can be a possibility. It is concluded that sonoparasitology should be considered as a diagnostic possibility of valuable potential for application in sheep. Conflict of interest statement The authors have nothing to disclose.
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Please cite this article in press as: Arsenopoulos, K., et al., Sonoparasitology: An alternative approach to parasite detection in sheep. Small Ruminant Res. (2016), http://dx.doi.org/10.1016/j.smallrumres.2016.12.007
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Contents lists available at ScienceDirect
Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Sonoparasitology: An alternative approach to parasite detection in sheep K. Arsenopoulos a , G.C. Fthenakis b , E. Papadopoulos a,∗ a b
Laboratory of Parasitology and Parasitic Diseases, School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece Veterinary Faculty, University of Thessaly, 43100 Karditsa, Greece
a r t i c l e
i n f o
Article history: Available online xxx Keywords: Coenurus cerebralis Cysticercus Diagnosis Echinococcus Fasciola Hydatid cyst Parasite Parasitic disease Ultrasound
a b s t r a c t Objective of the present review is to describe in a systematic way potential uses of ultrasonographic examination in diagnosis of parasitic diseases of sheep and to comment upon its potential usefulness in the health management of flocks. The technique has been primarily employed for diagnosis of hydatid disease in live sheep, by imaging lesions in the liver and/or the lungs of affected animals; this can be of potential value in health management of flocks, as other methods used to diagnose the disease may not have increased diagnostic accuracy. Further, the technique has been used for diagnosis of Fasciola infection, during the ductal phase, as well as for diagnosis of coenurosis. It is concluded that sonoparasitology should be considered as a diagnostic possibility of valuable potential for application in sheep. © 2016 Elsevier B.V. All rights reserved.
1. Introduction 1.1. Preamble Diagnostic approaches in parasitic infections of sheep are mainly driven by the localisation of parasites into the animal, thus, in live animals, the ability to detect the adult parasite itself (e.g., ectoparasites) or its various reproductive forms (i.e., eggs, larvae, oocysts); for example, skin scrapings are examined for detection of arthropods, blood smears are evaluated for detection of protozoa and faecal samples are processed for detection of eggs or larvae of gastrointestinal or respiratory helminthes. When sheep harbour immature or larval forms of parasites, no reproductive elements are produced; therefore, detection of parasites becomes more complicated and laborious. In such cases, diagnosis of infection would be based on application of other methods, often molecular or immunological techniques searching for (i) parasite genetic material (e.g., parasite DNA) or antigenic factors (e.g., Fasciola hepatica coproantigen; Adela Valero et al., 2009) or (ii) host-specific antibodies (e.g., anti-Toxoplasma antibodies), inflammatory cells (e.g., increased proportion of blood eosinophils during trichostrongylid infections) or enzymes (e.g., blood aspartate aminotransferase or ␥-glutamyl
transferase concentration in cases of liver trematode infections) among others. There are limitations in these approaches, of which the most significant one is that these techniques provide only indirect evidence regarding presence of parasites. Ultrasonographic examination may be of use for providing evidence for presence of parasites in a host, by imaging parasites (or some form of theirs) within the body of a sheep (direct evidence). That way, it supports the diagnosis of a parasitic disease, in a way similar to the detection of mites in skin scrapings or of eggs of trichostrongylids in faecal samples. The idea behind this approach is that parasitic formations can be visible by recording the reflections of ultrasonic waves directed into potentially parasitised tissues of sheep. Alternatively, lesions characteristically caused by a parasite (indirect evidence) may also be imaged. The findings, considered together with results of the above indirect techniques, may provide confirmatory evidence about parasitic infection in sheep, as well as providing simultaneously information regarding the condition of the affected organ in the animal. Objective of the present review is to describe in a systematic way potential uses of ultrasonographic examination in diagnosis of parasitic diseases of sheep and to comment upon its potential usefulness in the health management of flocks.
∗ Corresponding author. E-mail address: [email protected] (E. Papadopoulos). http://dx.doi.org/10.1016/j.smallrumres.2016.12.007 0921-4488/© 2016 Elsevier B.V. All rights reserved.
Please cite this article in press as: Arsenopoulos, K., et al., Sonoparasitology: An alternative approach to parasite detection in sheep. Small Ruminant Res. (2016), http://dx.doi.org/10.1016/j.smallrumres.2016.12.007
G Model RUMIN-5365; No. of Pages 4
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1.2. Use of ultrasonographic examination in humans and animal species other than sheep In humans, ultrasonographic examination has become part of the standard examination for diagnosis of hydatid disease (cystic echinococcosis) (Stojkovic et al., 2012; Craig et al., 2015), which affects primarily the liver and less often the lungs of patients (Derfoufi et al., 2012). Further, by using the technique, the lesions can be allocated into active, transitional or inactive, which would be of help in the therapeutic management of patients and the prognosis of the disease (Wuestenberg et al., 2014). Further, ultrasonographic examination has been employed in diagnosis of schistosomiasis (especially of the chronic form of the disease), which is responsible for periportal fibrosis in the liver and abnormalities in the urinary system; the findings of the examination are characteristic and use of the technique has led to minimising the frequency of liver biopsy for diagnostic purposes (Cerri et al., 1984), as well as to efficient monitoring of lesions in the urinary system (King et al., 2003). Other parasitic infections causing tissue lesions have also been readily diagnosed by use of ultrasonographic examination. These include Fasciola infections (Bassily et al., 1989; Aksoy et al., 2005; Koc et al., 2009), where it could also guide therapeutic management of the disease (Alatoom et al., 2008), schistosomiosis (DoehringSchwerdtfeger and Kardorff, 1995), lymphatic filariosis (Poltera and Zak, 1988; Mand et al., 2005) and liver abscesses associated with Ascaris infections (Javid et al., 1999; Richter et al., 2003). In animal species other than sheep, ultrasonographic examination can be of value as an adjunct to clinical examination in adult horses, used to detect intra-arterial changes associated with Strongylus vulgaris infections (Wallace et al., 1989a,b,c), as well as in foals, used to detect the characteristic intestinal dilation with intraluminal presence of ascarids associated with Parascaris equorum infection (Tatz et al., 2012; Nielsen et al., 2016). The method has also been used in calves to detect distended and thickened small intestine associated with Toxocara vitulorum infection (Van Der Steen et al., 2014) and in pigs for diagnosis of hepatic schistosomosis (Kardorff et al., 2003). Finally, in dogs and cats, use of the method has been made (among others) for diagnosis of Dioctophyme renale infection in kidneys (Rahal et al., 2014) and of peritoneal cestodosis (Venco et al., 2005).
2. Use of ultrasonography for diagnosis of parasitic diseases of sheep 2.1. Hydatid disease Hydatid disease (or cystic echinococcosis) is caused by hydatid cysts, the larval stage of Echinococcus granulosus. Apart from being a wide-spread zoonotic infection, the disease causes significant adverse financial consequences, due to reduced production by affected animals and the condemnation of affected tissue at abattoirs (Torgerson, 2003). No clearly defined approach is available for diagnosis of the disease in the field in live sheep. Various diagnostic methods have been proposed, e.g., serological examination (Lightowlers et al., 1984; Khabiri et al., 2006). However, use of these methods is hindered by reduced accuracy (e.g., due to potential cross-reactions with other pathogenic agents) and increased cost. As the disease is characterised by development of cystic formations in tissues of sheep (liver, lungs), it has been proposed that these might be detected by ultrasonographic examination. The potential usefulness of ultrasonographic examination for diagnosis of hydatid disease in sheep has been first discussed by Craig (1993). The liver and the lungs are the organs that should be
imaged for detection of hydatid cysts (Scott, 2017a,b), which appear as round hypoechoic structures located in those organs (Guarnera et al., 2001). However, various factors may influence the results of ultrasonographic examination. These include number, size (1.06.0 cm) and developmental status (active) of the cysts, parasitised organ and localisation of cysts therein, as well as pressure applied by cysts on surrounding tissues (Sagkan-Ozturk et al., 2015). Sage et al. (1998) have reported 55% sensitivity and 98% specificity of the technique (compared to post-mortem findings) for detection of hydatid cysts in the liver or lungs of sheep. In a later study, Lahmar et al. (2007) used the technique to examine sheep in the field and have reported that prevalence of liver lesions caused by the parasite amounted to 40%; the authors commented that ultrasonographic examination detected deep or superficial cysts only localised in the central or left part, in relation to the caudal vena cava, of the liver, hence up to one-third of cysts present in animals could be missed by using the technique. More recently, Dore et al. (2014) used more advanced technology equipment and reported >80% sensitivity and specificity of ultrasonographic examination (compared to post-mortem findings) for detection of hydatid cysts in the liver or lungs of sheep; rates increased to 100% if only active cysts (which were better imaged) were considered. It is noteworthy that Guarnera et al. (2001) have reported false positive results during examination of the liver for hydatid cysts, caused by imaging Cysticercus tenuicollis (the larval stage of Taenia hydatigena). Dore et al. (2014) have indicated that cysticerci were more often localised on the surface of the liver, which could help in their differentiation from hydatid cysts, present in the deeper parts of the organ. 2.2. Trematode infections of the liver Liver trematodes, e.g., Fasciola spp., Dicrocoelium dentriticum, may cause severe disease in sheep. In general, diagnosis of the infection may be performed readily by parasitological examination of faecal samples. Nevertheless, the technique has some constraints, because only adult parasites produce eggs (during parasitism by immature stages of Fasciola, which migrate through the liver [parenchymal phase of the disease], no eggs are produced) and number of eggs detected in faecal samples does not correlate directly with number of parasites in the liver (number of eggs produced by Fasciola or D. dentriticum is influenced by a variety of factors, e.g., immunological state of the host animal). Further, extent of liver damage may be detected to some degree by measuring blood concentrations of enzymes indicative of hepatic function (e.g., aspartate aminotransferase or ␥-glutamyl transferase). Gonzalo-Orden et al. (2003) in experimentally induced fasciolosis in sheep have indicated that ultrasonographic examination did not reveal specific lesions during the parenchymal phase of the infection. In contrast, the technique could be valuable for diagnosis of the infection during the ductal phase, as it showed the trematodes moving within the dilated duct imaged as structures of increased echogenicity; no specific lesions were evident during the parenchymal phase of the infection; further, findings characteristic of the disease: hepatomegaly and presence of multiple hyperechoic spots within the liver parenchyma, representing accumulations of inflammatory cells, could also be seen. Scott et al. (2005) have also performed ultrasonographic examination of the liver of sheep with mild fasciolosis, which revealed multiple hyperechoic dots in the parenchyma, giving a granular appearance in the texture of the organ; the findings corresponded to the most advanced changes as determined by the size of the abscesses and their relatively mature fibrous capsules, and areas of hepatic necrosis. In infections with Dicrocoelium dentriticum, mild to severe hepatitis is developed in affected sheep. Ultrasonographic examination of the liver revealed enlarged and occasionally calcified bile ducts in
Please cite this article in press as: Arsenopoulos, K., et al., Sonoparasitology: An alternative approach to parasite detection in sheep. Small Ruminant Res. (2016), http://dx.doi.org/10.1016/j.smallrumres.2016.12.007
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affected animals (Dore et al., 2014). These findings may contribute to presumed identification (false positive results) of hydatid cysts in the liver (Dore et al., 2014). 2.3. Coenurosis Diagnosis of coenurosis can be best achieved by a combination of history of the problem, findings of detailed clinical examination (Scott, 2012), elimination of other disorders with similar presentation (e.g., listeriosis, louping-ill, sarcocystosis, polioencephalomalacia, brain abscessation) (Giadinis et al., 2013) and evaluation of cerebrospinal fluid samples (Scott, 2012), as there is a consistent association between increased eosinophil concentration in cerebrospinal fluid and parasitic infection of the central nervous system (Doherty et al., 1989; Tschuor et al., 2006). In a relevant report, Doherty et al. (1989) have used ultrasonographic examination for detection of parasitic cysts in the brain. The technique had been performed after a small incision of the head bone was performed and the cerebral cortex was exposed; on caudal angulation, a large cavity full of fluid was revealed. The method was further used for treatment: the fluid was drained by means of a needle and the cyst was finally removed, which led to recovery of the animal 10 days later. 3. Use of ultrasonography for diagnosis of parasitic diseases in sheep health management The primary use of ultrasonography in parasitic diseases of sheep would be its value for diagnosis of hydatid disease (cystic echinococcosis) in live animals. The studies of Sage et al. (1998) and Dore et al. (2014) have indicated that ultrasonographic examination of sheep for detection of hydatid cysts can be useful (i.e., practical, cost-effective and relatively accurate), hence it may be used instead of or coupled with serological examination of animals under evaluation (Craig et al., 2015). The method may be applied for screening sheep to detect lesions of cystic echinococcosis. This can provide evidence regarding the value of preventive measures taken to control the disease in a flock (e.g., anthelmintic treatment of dogs, minimising potential infections from wild canids (Vasileiou et al., 2015) etc. Further, in case of animals of particular value (e.g., breeding rams), appropriate treatment may be initiated, although in general efficacy of such schemes is not always 100% (Ceballos et al., 2013). It is noteworthy that during ultrasonographic examination, the transducer is brought in contact with many sheep. Hence, there may be a danger for transmission of parasitic agents, if animals were infected. The possibility can arise with mange mites, e.g., Sarcoptes scabiei (Papadopoulos et al., 2000), Psoroptes ovis (Losson, 2012), which can survive in objects (including transducers of the ultrasonographic equipment) and be transmitted to other sheep in the farm (ones scanned after the infested ones) or even to other farms (if inappropriate cleaning of the transducer would be performed). 4. Concluding remarks Ultrasonographic examination has been employed successfully for diagnosis of parasitic infections of sheep. Routine use of the method for diagnosis of hydatid disease in live animals can be a possibility. It is concluded that sonoparasitology should be considered as a diagnostic possibility of valuable potential for application in sheep. Conflict of interest statement The authors have nothing to disclose.
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Please cite this article in press as: Arsenopoulos, K., et al., Sonoparasitology: An alternative approach to parasite detection in sheep. Small Ruminant Res. (2016), http://dx.doi.org/10.1016/j.smallrumres.2016.12.007