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Complex gill disorder (CGD): A histopathology workshop report


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A workshop was organised to share findings, experience and knowledge on the histopathology associated with gill diseases in sea water Atlantic salmon. An interesting extended discussion resulted in an agreed criteria for complex gill disorder (CGD)-type histopathology, which we hope will contribute in epidemiological studies, research projects and diagnostic reports.
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172, Bull. Eur. Ass. Fish Pathol., 39(4) 2019
Complex gill disorder (CGD): A
histopathology workshop report
P. Noguera1, A.B. Olsen2, J. Hoare3, K.I. Lie4, M.
Marcos-López3, T. T. Poppe5 and H. Rodger6
1 Marine Scotland Science, 375 Victoria Road, AB11 9DB Scotland; 2 Norwegian
Veterinary Institute, Thormøhlens gate 53C, 5006 Bergen, Norway; 3 Fish Vet Group Ltd.,
22 Carsegate Road, IV3 8EX Inverness, Scotland; 4 Fish Vet Group Norge, Hosveien
21 – 23, 0275 Oslo, Norway; Ireland; 5 PHARMAQ Analytiq AS, Harbialléen
2A, N-0213 Oslo, Norway; 6 VAI Consulting, Kinvara, Co. Galway
A workshop was organised to share ndings, experience and knowledge on the histopathology
associated with gill diseases in sea water Atlantic salmon. An interesting extended discussion re-
sulted in an agreed criteria for complex gill disorder (CGD)-type histopathology, which we hope
will contribute in epidemiological studies, research projects and diagnostic reports.
The growing issues of gill disease in the salmon
aquaculture industry in Europe have resulted
in a heightened focus on this area for diagnos-
ticians, clinicians and researchers working in
sh health, with the increased use of gross gill
scoring systems, as well as laboratory assays,
including light microscopy and molecular
There are a variety of terms being used to
describe gill pathology such as proliferative
gill disease (PGD), proliferative gill inam-
mation (PGI) (Kvellestad et al. 2005), complex
gill disease (CGD) (Herrero et al. 2018) and
amoebic gill disease (AGD) (Rodger 2014). In
order to clarify the histopathology criteria as-
sociated with these terms, a group of diagnostic
sh histopathologists convened for a one-day
workshop at the Scoish Aquaculture Innova-
tion Centre (SAIC), University of Stirling in
May 2019 to share their ndings, experience
and knowledge. As a result of this workshop,
the group was able to agree on criteria for the
above terms to enable their use in epidemiol-
ogy studies, research projects, and diagnostic
Drs. Patricia Noguera (Marine Scotland Science)
and Hamish Rodger (VAI Consulting) organised
the workshop with the much-appreciated assis-
tance and support of Caroline Grin and Robin
Shields from the SAIC. The diagnosticians who
participated were Drs. Trygve Poppe (Pharmaq
Analytiq, Norway), Mar Marcos-Lopez (Fish Vet
* Corresponding author’s e-mail:
Bull. Eur. Ass. Fish Pathol., 39(4) 2019 173
Group (FVG) UK & Ireland), Kai-Inge Lie (FVG
Norway), Anne Berit Olsen (NVI, Norway),
James Hoare (FVG UK), Patricia Noguera (MSS,
Scotland) and Hamish Rodger (VAI, Ireland).
Drs. Aaron Reeves and Annee Boerlage (SRUC,
Inverness), who are co-ordinating one of the
SAIC & industry funded gill projects, were
also present.
The workshop covered the reporting of dif-
ferent types of histopathology observed in the
various geographical regions associated with
gill disease mainly in sea water salmon, as well
as an extended discussion on the proposed
criteria for complex gill disorder (CGD)- type
histopathology as indicated below.
1. Complex gill disorder (CGD)-type
his topat hology. Signicant non-
specic, proliferative branchitis, which
cannot be aributed to a single known
aetiology (Figure 1.), and is characterised
Moderate to severe hyperplasia and fusion
of the lamellar epithelium, with variable
mucous cell hyperplasia and occasional
lacunae (pseudocysts).
Acute, subacute and/or chronic lamellar
inammation (may include either or both
granulocytic to lymphohistiocytic inltra-
Variable cellular degeneration and necrosis
Variable haemorrhage, hyperaemia and
Variable lament inammation
Variable hypertrophy and hyperplasia of
highly eosinophilic cells (alike chloride
and/ or degenerative epithelial cells)
Rare cartilage proliferation/dysplasia
Low to high numbers of the following agents
or evidence of their presence may be associated
with the above changes (Figure 2.):
Amoebae, epitheliocysts (Branchiomonas-
type, less than 10 μm in diameter and
densely basophilic), Gram-positive mi-
crosporidian spores within degenerate
cells or microvesicles, salmon gill pox
virus (apoptotic cells with nuclear central
clearing of chromatin), other pathogens
(e.g. Ichthyobodo sp., Tenacibaculum spp) or
damaged due harmful planktonic organ-
isms (e.g. jellysh).
This can be compared to the histopathology cri-
teria for other gill disease terms such as amoebic
gill disease and proliferative gill inammation
(PGI), which are outlined below:
2. Amoebic gill disease
his topat hology. (Clark & Nowak
1999, Munday et al. 2001) where there is
presence of all four ndings in the same
gill tissue:
Hyperplasia of gill epithelia
Lamellar fusion
Interlamellar lacunae in hyperplastic tissue
Presence of amoebae (eosinophilic para-
some) adjacent to gill surface (or in lacunae)
3. Proliferative gill inammation.
(Kvellestad et al. 2005) where there is
presence of all four ndings in the same
gill tissue:
Circulatory disturbances (haemorrhage,
thrombi, death of pillar cells)
Epithelial hyperplasia
Inammation in sub-epithelial & epithelial
Epithelial cell death
174, Bull. Eur. Ass. Fish Pathol., 39(4) 2019
Figure 1. General features of complex gill disorder (CGD)-type histopathology. Signicant, non-specic,
proliferative branchitis characterised by moderate to severe hyperplasia and fusion of the lamellar
epithelium (A, B, C) accompanied by occasional lacunae (pseudoc ysts) (C). Variable mucous cell hyperplasia
(D,E) and hyperplasia and hypertrophy of eosinophilic chloride-like cells along lamellae (E insert and F).
Acute, subacure and/or chronic lamellar and variable lament inammation may include both granulocytic
and lymphohistiocytic inltration (C,D,E,F,G). Variable cellular degeneration and necrosis (E,F,G), blood
congestion, haemorrhage, hyperaemia and t hrombosis (A, D, E, G), a nd rare cart ilage proliferation/dysplasia
(H) can also be observed.
Bull. Eur. Ass. Fish Pathol., 39(4) 2019 175
Figur e 2. Complex gill disorder (CGD)-type histopathology may be seen associated with low to high numbers
of one or more type of agents or evidence of their presence. Examples include amoebae (Neoparamoeba
perura ns) (A,B,C), microsporid ian (Desmozoon lepeopht herii) spores with in degenerate cells or m icrovesicles
(D), epitheliocysts (e.g. Branchiomonas-type, less than 10 μm in diameter and densely basophilic) (E), cell
changes associated with Salmon gill pox virus (ASPV) (apoptotic cells with central clearing of chromatin)
(F), and damaged associated to harmful plankton (e.g. jelly sh) (G, H).
176, Bull. Eur. Ass. Fish Pathol., 39(4) 2019
These can also be compared to the histopa-
thology of specic gill conditions where the
pathology is associated with, or has been dem-
onstrated to be, associated with one pathogen,
agent or factor alone.
We thank Drs. Alf Dalum (Pharmaq Analytic,
Norway) and Jorge del Pozo (University of
Edinburgh, UK) who while unable to aend
the meeting in person were also involved in
the post discussion of the nal report.
Funding for travel to the workshop was
made available via SRUC, Inverness (Dr.
Aaron Reeves) and the University of Aber-
deen (Prof. Sam Martin) as part of SAIC &
industry funded projects on gill health. SAIC
is also gratefully acknowledged for support
for accommodation and meeting organisation.
Clark A and Nowak BF (1999). Field
investigations of amoebic gill disease in
Atlantic salmon, Salmo salar L., in Tasmania.
Journal of Fish Diseases 22, 433 – 443.
Herrero A, Thompson KD, Ashby A, Rodger
HD and Dalgleish MP (2018). Complex gill
disease: an emerging syndrome in farmed
Atlantic salmon (Salmo salar L.). Journal of
Comparative Pathology 163, 23 – 28.
Kvellestad A, Falk K, Nygaard SMR,
Flesjå K and Holm JA (2005). Atlantic
salmon paramyxovirus (ASPV)
infection contributes to proliferative gill
inammation (PGI) in seawater-reared
Salmo salar. Diseases of Aquatic Organisms
67, 47 – 54.
Munday BL, Zilberg D and Findlay V (2001).
Gill disease of marine sh caused by
infection with Neoparamoeba pemaquidensis.
Journal of Fish Diseases 24, 497 - 507.
Rodger HD (2014). Amoebic gill disease in
farmed salmon (Salmo salar) in Europe.
Fish Veterinary Journal 14, 16 - 26.
... .. (the types of specific gill diseases)'. When principal pathological changes are non-specific, either in combination with, or in the absence of, one or more of the seven distinctive types (including AGD), the type of gill disease is referred to as 'complex gill disease or disorder (CGD)' (Noguera et al. 2019). The terms CGD and multifactorial gill disease are often used interchangeably and are overlapping. ...
... The different terms that have been used to describe marine gill disease have led to confusion and make it difficult to compare between studies and areas. CGD as currently used, includes most other pathologies (Herrero et al. 2018;Noguera et al. 2019), but its boundaries are not well defined. A clear case definition would allow for a systematic estimation of prevalences across the salmon industry in different areas and countries and could aid epidemiological studies such as risk-factor analyses. ...
Full-text available
Gill disease of farmed Atlantic salmon (Salmo salar ) in the marine environment has emerged as a significant problem for the salmon aquaculture industry. Different types of marine salmon gill disease reported include amoebic gill disease (AGD), parasitic gill disease, viral gill disease, bacterial gill disease, zooplankton (cnidarian nematocyst)‐associated gill disease, harmful algal gill disease and chemical/toxin‐associated gill disease. The term ‘multifactorial gill disease’ is used when multiple distinguishable types of disease (as opposed to an obvious single primary type) are present. When gill disease is non‐specific, it is referred to as ‘complex gill disease’ (CGD) or ‘complex gill disorder’. These two terms are often used interchangeably and are overlapping. The significance of many infectious and non‐infectious agents that may be associated with CGD is often unclear. In this review, we summarise aspects of the different types of gill disease that are relevant to the epidemiology of gill disease and of CGD in particular. We also tabulate simultaneously occurring putative pathogens to explore the multifactorial nature of gill disease.
... Complex gill disorder (CGD) is a multifactorial and multiaetiological condition that is considered to be a consequence of the interaction of a number of factors including environment, management practices and pathogenic microorganisms in the marine stage of Atlantic salmon [6]. The histopathological criterion for CGD has recently been defined as a branchitis with additional histopathology of unknown aetiology [7]. The main infectious agents associated with cases of CGD in Atlantic salmon are Candidatus Branchiomonas cysticola, Desmozoon lepeophtherii and salmon gill poxvirus (SGPV) [8][9][10]. ...
Full-text available
Complex gill disorder (CGD) is an important condition in Atlantic salmon aquaculture, but the roles of the putative aetiological agents in the pathogenesis are uncertain. A longitudinal study was undertaken on two salmon farms in Scotland to determine the variations in loads of CGD-associated pathogens (Desmozoon lepeophtherii, Candidatus Branchiomonas cysticola, salmon gill pox virus (SGPV) and Neoparamoeba perurans) estimated by quantitative PCR. In freshwater, Ca. B. cysticola and SGPV were detected in both populations, but all four pathogens were detected on both farms during the marine stage. Candidatus B. cysticola and D. lepeophtherii were detected frequently, with SGPV detected sporadically. In the marine phase, increased N. perurans loads associated significantly (p < 0.05) with increases in semi-quantitative histological gill-score (HGS). Increased Ca. B. cysticola load associated significantly (p < 0.05) with increased HGS when only Farm B was analysed. Higher loads of D. lepeophtherii were associated significantly (p < 0.05) with increased HGS on Farm B despite the absence of D. lepeophtherii-type microvesicles. Variations in SGPV were not associated significantly (p > 0.05) with changes in HSG. This study also showed that water temperature (season) and certain management factors were associated with higher HGS. This increase in histological gill lesions will have a deleterious impact on fish health and welfare, and production performance.
... Thompson, Ashby, Rodger, & Dagleish, 2018;Noguera et al., 2019).However, the exact cause(s) and pathogenesis of a considerable proportion of gill disease cases are unknown (Boerlage et al., 2020).Microorganisms Ca. Branchiomonas cysticola, salmon gill poxvirus (SGPV), Neoparamoeba perurans (syn. ...
Full-text available
Gill disease is an important cause of economic losses, fish mortality and reduced animal welfare in salmonid farming. We performed a prospective cohort study, following groups of Atlantic salmon in Western Norway with repeated sampling and data collection from the hatchery phase and throughout the 1st year at sea. The objective was to determine if variation in pathogen prevalence and load, and zoo- and phytoplankton levels had an impact on gill health. Further to describe the temporal development of pathogen prevalence and load, and gill pathology, and how these relate to each other. Neoparamoeba perurans appeared to be the most important cause of gill pathology. No consistent covariation and no or weak associations between the extent of gill pathology and prevalence and load of SGPV, Ca. B. cysticola and D. lepeophtherii were observed. At sea, D. lepeophtherii and Ca. B. cysticola persistently infected all fish groups. Fish groups negative for SGPV at sea transfer were infected at sea and fish groups tested negative before again testing positive. This is suggestive of horizontal transmission of infection at sea and may indicate that previous SGPV infection does not protect against reinfection. Coinfections with three or more putative gill pathogens were found in all fish groups and appear to be the norm in sea-farmed Atlantic salmon in Western Norway.
... The criteria included were "lamellar hyperplasia" (0− 3), "lamellar fusion" (0− 3), "cellular hypertrophy" (0− 3), "cellular death" (0− 3), "lamellar oedema" (0− 3), "vascular changes" (0− 3), and "inflammation" (0− 3). These pathological changes in gills that are often associated with CGD (Noguera et al., 2019). The observed scores from these 7 criteria were aggregated to a single number that represented the histopathology score, see Table 2. ...
Amoebic gill disease (AGD) and complex gill disease (CGD) are the most significant marine gill diseases in salmon aquaculture in Scotland. Little is published about diagnostic performance of tests to detect these diseases, making it difficult to interpret test results. We estimated diagnostic sensitivity (DSe) and specificity (DSp) of common tests for AGD (gross AGD score, qPCR for Neoparamoeba perurans, histopathology) and CGD (gross proliferative gill disease (PGD) score, gross total gill score, histopathology). Because specifications in our sampling protocol implemented to encourage consistency across the farms might affect diagnostic performance of histopathology (historically the reference standard for gill diseases), we used Bayesian latent class models without reference standard. Cases and non-cases were based on less, medium, and severe stringent case definitions, representing different cut-off levels for the different tests. Gross gill scores for both diseases were excellent in designating non-diseased fish, DSps were generally around 1. To detect CGD, DSe of gross total gill score and gross PGD score were between respectively 0.81 (0.73 – 0.91 lower to upper 95% credible interval) and 0.53 (0.46 – 0.64) for medium stringent case definitions, and to detect AGD the DSe for the gross AGD score was between 0.53 (0.48 - 0.57) and 0.14 (0.07 – 0.22) for respectively the less and severe stringent case definition. Thus, gross gill scores were medium to good in designating truly diseased fish, implying some false negatives are expected. For CGD the DSe for gross total gill scores were the highest, for AGD it was the qPCR test at a DSe of 0.92 (0.86 – 0.99). For both diseases, DSe was lowest for histopathology, e.g. 0.23 (0.16 – 0.30) for AGD and 0.1 (0.07 – 0.14) for CGD under medium stringent case definitions, perhaps due to collecting the second gill arch on the right rather than the worst affected arch, whilst PCR sampling and gross gill scoring included multiple (PCR) or all (gross scoring) gill arches. The diagnostic goals of these tests differ; gross gill scoring provides a low-cost presumptive diagnosis, PCR a non-lethal confirmation of the presence of a specific pathogen and histopathology provides information on the underlying aetiology of gill damage as well as the extent, severity, and chronology of gill disease. An effective gill health surveillance strategy is likely to incorporate multiple diagnostic tools used in a complementary manner.
... Sea lice are rated as amongst the most important pathogens for sustainable aquaculture (Jones et al., 2015) and management to reduce lice numbers is required with government intervention should loads indicate improvements in mitigation are required (Marine Scotland, 2019). Increases in lice numbers feed back to increased management (Noguera et al., 2019) or Pancreas Disease (Kilburn et al., 2012) cause substantial losses that are likely to increase with any potential reduction in biosecurity management (Wheatley et al. 1995), and with increased biomass (Anderson & May 1979;Moriarty et al., 2020), which has been permitted on a temporary basis (SEPA, 2020b). Any increase in mortality reduces economic resources available to the producer, and are an issue for fish welfare. ...
Full-text available
COVID-19 led to sudden changes in human activities, mainly due to restrictive measures required to supress the virus. We assess the preliminary evidence for impacts on animal health and welfare in Scottish aquaculture, a key economic activity in remoter areas of the country. We summarise the industry structure, explore pathways of vulnerability to aquatic animal disease within a One Health framework that may be accentuated by impacts of COVID-19, and use basic routine data collection on the key welfare indicators of salmon mortality and parasitic sea lice counts. The indicators were published on schedule and provide no evidence of gross impact on health and welfare, at least for salmon, during the period of intensive lockdown restrictions in Scotland. Longer term effects cannot be ruled out and we do not assess impacts on the economic or social aspects of aquaculture production.
... [1][2][3][4][5] Gill diseases can be caused by infectious and noninfectious agents, and multifactorial or complex gill pathology often occurs. 3,[5][6][7][8][9][10][11][12][13] Poor gill health can lead to direct mortalities, increased mortalities during bath treatments, economic losses, increased susceptibility to other diseases, and reduced performance and welfare. Among parasitic conditions, amoebic gill disease (AGD), caused by the marine ectoprotozoan Neoparamoeba perurans (syn. ...
Gill health is one of the main health challenges for Atlantic salmon (Salmo salar L.) mariculture worldwide, and amoebic gill disease (AGD), caused by the marine ectoprotozoan Neoparamoeba perurans, is currently one of the most significant diseases in terms of prevalence and economic impact. This review describes the host response of Atlantic salmon to the disease, focusing on the pathological changes, immune response, and mechanisms underlying the prominent epithelial proliferation and mucus hypersecretion occurring in affected fish. Health management strategies and risk factors are also discussed.
... As a result, fish exposed to Neoparamoeba perurans and then classified as clear of the AGD symptoms during the macroscopic gill scoring for AGD may in fact need to be re-classified at the level of histopathological examination (Wynne et al., 2008b). Further complexity to the diagnostic problems is added when the gill disease is multifactorial (Wise et al., 2008;Gjessing et al., 2019;Noguera et al., 2019). More broadly, the poor diagnostic and prognostic value of the PGD scores demonstrated in our study is consistent with the limited applicability of the gross morphology to diagnose complex diseases in livestock and humans, which typically need extensive histopathology and molecular profiling to confirm and prognosticate (Hoffmann et al., 2009;Ahmed and Abedalthagafi, 2016;Mobadersany et al., 2018). ...
Full-text available
The gill of teleost fish is a multifunctional organ involved in many physiological processes such as gas exchange, osmotic and ionic regulation, acid-base balance and excretion of nitrogenous waste. Due to its extensive interface with the environment, the gill plays a key role as a primary mucosal defense tissue against pathogens, as manifested by the presence of the gill-associated lymphoid tissue (GIALT). In recent years, the prevalence of multifactorial gill pathologies has increased significantly, causing substantial losses in Atlantic salmon aquaculture. The transition from healthy to unhealthy gill phenotypes and the progression of multifactorial gill pathologies, such as proliferative gill disease (PGD), proliferative gill inflammation (PGI) and complex gill disorder (CGD), are commonly characterized by epithelial hyperplasia, lamellar fusion and inflammation. Routine monitoring for PGD relies on visual inspection and non-invasive scoring of the gill tissue (gross morphology), coupled with histopathological examination of gill sections. To explore the underlying molecular events that are associated with the progression of PGD, we sampled Atlantic salmon from three different marine production sites in Scotland and examined the gill tissue at three different levels of organization: gross morphology with the use of PGD scores (macroscopic examination), whole transcriptome (gene expression by RNA-seq) and histopathology (microscopic examination). Our results strongly suggested that the changes in PGD scores of the gill tissue were not associated with the changes in gene expression or histopathology. In contrast, integration of the gill RNA-seq data with the gill histopathology enabled us to identify common gene expression patterns associated with multifactorial gill disease, independently from the origin of samples. We demonstrated that the gene expression patterns associated with multifactorial gill disease were dominated by two processes: a range of immune responses driven by pro-inflammatory cytokines and the events associated with tissue damage and repair, driven by caspases and angiogenin.
... AGD can be proactively managed by regular inspection of the gills of anaesthetized fish for gross AGD signs. A "gill index" is used internationally, with a scale from 0 = no lesions to 5 = extensive lesions, by examining all the hemibranch surfaces (Noguera et al., 2019). The gill index allows the farmer to plan treatments in a cost-effective manner (Taylor, Muller, Cook, Kube, & Elliott, 2009). ...
Full-text available
Neoparamoeba perurans is the causative agent of amoebic gill disease (AGD). Two loop‐mediated isothermal amplification (LAMP) assays targeting the parasite 18S rRNA and the Atlantic salmon EF1α, used as internal control, were designed. The N. perurans LAMP assay did not amplify close relatives N. pemaquidensis and N. branchiphila, or the host DNA. This assay detected 106 copies of the parasite 18S rRNA gene under 13 min and 103 copies under 35 min. Five “fast‐and‐dirty” DNA extraction methods were compared with a reference method and further validated by TaqMan™ qPCR. Of those, the QuickExtract buffer was selected for field tests. Seventy‐one non‐lethal gill swabs were analysed from AGD‐clinically infected Atlantic salmon. The pathogen was detected under 23 min in fish of gill score >2 and under 39 min for lower gill scores. About 1.6% of the tests were invalid (no amplification of the internal control). 100% of positives were obtained from swabs taken from fish showing gill score ˃3, but only ~50% of positives for lower gill scores. The present LAMP assay could be implemented as a point‐of‐care test for the on‐site identification of N. perurans; however, further work is required to improve its performance for lower scores.
Transmission of pathogens increases with population density associated with larger populations within farms and higher number of farms within an area. These pathogens can also spill over (or back) into wild populations. Owing to transmission between, and from, farms many diseases are best managed at an area level. Current area management practice in Scotland was developed 20 years ago, but as aquaculture evolves, farm size and environmental exposure will change. To assess if potential aquaculture management changes require spatial disease management changes, three scenarios for particle spread to help inform on pathogen transmission are evaluated: (1) current farm distribution; (2) medium term development (farms in exposed coastal areas); and (3) long term development (offshore farms). Climatological output from a hydrodynamic model is used to drive movements of passive particles representing infectious pathogens released from these farms. The potential distribution of particles allows assessment on possible transmission of infection, around farm locations, subject to various modelling assumptions and limitations. Dispersal distances increased with time in all scenarios. For medium term development the average dispersal distance (3.0+/-1.3 km) was marginally larger than dispersal from existing sites (2.7+/-1.6 km) after 12 hours, whereas for the longer term development this was 4.8+/-2.9 km. These results indicate that short to medium term aquaculture expansion is consistent with existing disease management areas, at least from these models. However, offshore aquaculture may result in transmission distances for pathogens that exceed existing limits, therefore will likely require re-assessment of management areas, subject to consideration of all relevant epidemiological factors.
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Gill diseases may cause high mortalities in farmed Atlantic salmon. In seawater reared fish co-infections involving the epitheliocystis associated bacterium Ca. Branchiomonas cysticola, the microsporidian Desmozoon lepeophtherii, the causative agent of amoebic gill disease Paramoeba perurans and salmon gill poxvirus are common and histopathological lesions may be complex. Here, we report detection of these agents utilising multiplex real-time PCR and link their presence to histopathologically visible gill lesions by in situ hybridisation (ISH) utilising RNAscope®. We show that Ca. Branchiomonas cysticola infections may remain undetected if diagnostic investigations are restricted to histopathology alone. Further, positive in situ labelling of Ca. Branchiomonas cysticola was observed within epitheliocysts, but also in small foci within areas of inflammation and necrosis in which histologically detectable epitheliocysts were not visible. In situ labelling of D. lepeophtherii corresponded well with tissue distribution patterns previously associated with this microsporidian. Salmon gill poxvirus was associated with apoptotic gill epithelial cells, while Ca. Piscichlamydia salmonis could not be associated with pathological changes. The multiplex real-time PCRs utilised were rapid and sensitive diagnostic tools and the results corresponded well with ISH. This study shows that the agents involved in complex gill disease can be linked to lesions using ISH and suggests that Ca. B. cysticola plays a crucial role in the development of gill disease in the farming of salmon in Norway.
Full-text available
Amoebic gill disease (AGD) emerged in marine Atlantic salmon farming in France, Ireland and Scotland as the major infectious disease challenge dur- ing 2011 and 2012. The causal parasite, Neoparamoeba perurans, causes focal to multifocal gill hyperplasia and lamellar fusion leading to severely compromised gill physiology and function. Affected fish suffer respiratory distress, increased susceptibility to stress at movement or bathing (for lice treatment) and mortality. Fish can be monitored for the condition through weekly gross gill score assessment, complimented with laboratory tests such as gill smears, histopathology or RT-PCR. The disease can be treated with freshwater or hydrogen peroxide baths taking into account environmental conditions and degree of gill pathology.
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Amoebic gill disease (AGD) of maricultured salmonids, turbot, Scophthalmus maximus (L.), European seabass, Dicentrarchus labrax (L.), and sharpsnout seabream, Diplodus puntazzo (Cetti), caused by Neoparamoeba pemaquidensis has been reported from Australia (Tasmania), Ireland, France, Chile, North America (Washington State and California) and Spain. Of the salmonids, Atlantic salmon, Salmo salar L., appears to be the most susceptible with rainbow trout, Oncorhynchus mykiss (Walbaum), also suffering significant disease. Only minor outbreaks have been reported in coho, O. kisutch (Walbaum), and chinook salmon, O. tshawytscha (Walbaum). The disease now accounts for 10–20% of production costs of Atlantic salmon in Tasmania and has lead to temporary abandonment of culture of this species in parts of Spain. It is of lesser, but still significant, importance in other countries. Much is known about the pathology of AGD but the pathophysiology of the disease is poorly understood. There is evidence that non-specific immunity is involved in fish acquiring resistance to AGD, but no unequivocal evidence exists for protection as a result of specific immune responses. To date, for salmonids, the only effective treatment for AGD is a freshwater bath. Control procedures based on modification of management strategies have been minimal and virtually unresearched.
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Proliferative gill inflammation (PGI) causes significant losses in farmed Atlantic salmon Salmo salar L. in Norway, especially during the first months following seawater transfer. The aetiology is apparently multifactorial, including infection with chlamydia-like bacteria and Atlantic salmon paramyxovirus (ASPV). In the present study, gills from diseased fish from 3 farms on the western coast of Norway were sampled. The pathological changes were briefly described and the aetiological significance of ASPV studied by immunofluorescent staining of cryosections and by immunohistochemistry on sections of formalin-fixed and paraffin-embedded tissue. The pathological changes were macroscopically characterized by palour of the gills, and histologically by inflammation, circulatory disturbances, cell death and epithelial cell proliferation. ASPV was demonstrated in fish from all farms studied, as immunostaining consistent with ASPV was obtained in lamellar epithelial and endothelial cells of pathologically altered tissues. It is concluded that ASPV is at least a contributing cause of PGI. As far as we know, this is the first demonstration of fish disease related to infection with a paramyxovirus.
Gill disorders have become a significant problem during the marine phase of farming Atlantic salmon (Salmo salar L.). The term complex gill disease (CGD) includes a wide range of clinical gill disease presentations generally occurring from the end of summer to early winter on marine Atlantic salmon farms. The gross and histological lesions observed are the resultant culmination of exposure to a mixture of environmental insults, pathogenic organisms and farm management practices. None of the three principal agents purportedly associated with CGD (Desmozoon lepeophtherii, salmon gill poxvirus or Candidatus Branchiomonas cysticola) have been cultured successfully in-vitro, so individual in-vivo challenge studies to identify their pathogenesis have not been possible. Studies of cohabitation of single pathogen-infected fish with naïve fish, and epidemiological investigations are required urgently to elucidate the roles of these pathogens and other factors in CGD.
Amoebic gill disease (AGD) is the most serious health problem in Atlantic salmon cultured in Tasmania. Our field investigation examined prevalence of AGD during 2 years, every year for up to 7 months after transfer to sea water. The relationship between environmental factors and AGD prevalence was determined. Additionally, effects of adding levamisole to freshwater baths were investigated in a field trial. AGD was recorded on all farms, except for farm A, which did not move salmon from a brackish site to a full-salinity site during the study. The prevalence showed a bimodal distribution with the first larger peak in summer (usually in January) and the second smaller peak in autumn (between March and May). During both years the prevalence of AGD was significantly greater in January than any other month. Sampling month and the interaction between farm and month had a statistically significant effect on AGD prevalence. AGD was recorded at a minimum temperature of 10.6 °C and minimum salinity of 7.2 ppt. There was a positive relationship between the time since the freshwater bath and the prevalence of AGD for the first 30 days after the bath, with a dramatic increase in the AGD prevalence about 3 weeks after the bath. After 30 days, there was no statistically significant relationship between AGD prevalence and days since the last bath, except for the second bath. The addition of levamisole to the freshwater bath did not significantly increase the time between treatments. The relationship between diagnosis on the basis of gross signs and histological diagnosis was significant, however, the gross diagnosis was unreliable within the lower range, with 31.8% false negatives and 15.9% false positives and kappa value of 0.2742.