Gill damage and delayed mortality of Northern shrimp (Pandalus borealis) after short time exposure to anti-parasitic veterinary medicine containing hydrogen peroxide

Bechmann, Renée Katrin; Arnberg, Maj; Gomiero, Alessio; Westerlund, Stig; Lyng, Emily; Berry, Mark; Ágústsson, Thorleifur; Jager, Tjalling; Burridge, L.E.

doi:10.1016/j.ecoenv.2019.05.045

Cited by 42 publications

(19 citation statements)

References 25 publications

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“…Fish encounter environmental oxidants during production, as several husbandry practices rely on the use of oxidative chemical compounds, such as during water disinfection [27] or disease treatment [9]. Application frequency may vary, from continuous to periodic, each depending on its intended use (i.e., disinfectant vs. therapy).…”

Section: Discussionmentioning

confidence: 99%

“…Exogenous ROS may come from various sources, and their impacts on redox status have consequences on cell viability, activation, proliferation, and organ function. Farmed fish encounter an increased flow of exogenous ROS several times during a lifetime, as many husbandry practices employ ROS-generating compounds either as a form of disinfectant or water treatment, or as a chemotherapeutant [7][8][9][10][11]. The antimicrobial activity of ROS towards opportunistic and pathogenic microorganisms underlines their use in providing fish with a favourable rearing environment [12].…”

Section: Introductionmentioning

confidence: 99%

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Oxidative Chemical Stressors Alter the Physiological State of the Nasal Olfactory Mucosa of Atlantic Salmon

et al. 2020

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The olfactory organs of fish have vital functions for chemosensory and defence. Though there have been some ground-breaking discoveries of their involvement in immunity against pathogens in recent years, little is known about how they respond to non-infectious agents, such as exogenous oxidants, which fish encounter regularly. To this end, we employed Atlantic salmon (Salmo salar) as a model to study the molecular responses at the nasal olfactory mucosa of a teleost fish when challenged with oxidants. Microarray analysis was employed to unravel the transcriptional changes at the nasal olfactory mucosa following two types of in vivo exposure to peracetic acid (PAA), a highly potent oxidative agent commonly used in aquaculture: Trial 1: periodic and low dose (1 ppm, every 3 days over 45 days) to simulate a routine disinfection; and Trial 2: less frequent and high dose (10 ppm for 30 min, every 15 days, 3 times) to mimic a bath treatment. Furthermore, leukocytes from the olfactory organ were isolated and exposed to PAA, as well as to hydrogen peroxide (H2O2) and acetic acid (AA)—the two other components of PAA trade products—to perform targeted cellular and molecular response profiling. In the first trial, microarrays identified 32 differentially expressed genes (DEG) after a 45-day oxidant exposure. Erythrocyte-specific genes were overly represented and substantially upregulated following exogenous oxidant exposure. In Trial 2, in which a higher dose was administered, 62 DEGs were identified, over 80% of which were significantly upregulated after exposure. Genes involved in immune response, redox balance and stress, maintenance of cellular integrity and extracellular matrix were markedly affected by the oxidant. All chemical stimuli (i.e., PAA, H2O2, AA) significantly affected the proliferation of nasal leukocytes, with indications of recovery observed in PAA- and H2O2-exposed cells. The migration of nasal leukocytes was promoted by H2O2, but not much by PAA and AA. The three chemical oxidative stressors triggered oxidative stress in nasal leukocytes as indicated by an increase in the intracellular reactive oxygen species level. This resulted in the mobilisation of antioxidant defences in the nasal leukocytes as shown by the upregulation of crucial genes for this response network. Though qPCR revealed changes in the expression of selected cytokines and heat shock protein genes following in vitro challenge, the responses were stochastic. The results from the study advance our understanding of the role that the nasal olfactory mucosa plays in host defence, particularly towards oxidative chemical stressors.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Oxidative Chemical Stressors Alter the Physiological State of the Nasal Olfactory Mucosa of Atlantic Salmon

et al. 2020

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“…Traditionally, H2O2 has been considered as posing a low environmental risk because it rapidly disassociates into water and oxygen and does not bioaccumulate in the environment (Kiemer, Black, 1997;Pedersen, Good, Pedersen, 2012). However, its excessive use in recent years has raised some serious concerns, and the frequency of treatment has been implicated in the development of resistance to the chemotherapeutant (Bechmann, Arnberg, Gomiero, Westerlund, Lyng, Berry, Agustsson, Jager, Burridge, 2019;Hjeltnes B, Bang-Jensen B, Bornø G, Haukaas A, S, 2019). These concerns are also prompted by a significant caveat about the lack of knowledge of the physiological consequences of peroxide use in salmon, as earlier approaches focused on the impacts on the causative agent and the disappearance of clinical signs.…”

Section: Introductionmentioning

confidence: 99%

Crowding reshapes the mucosal but not the systemic response repertoires of Atlantic salmon to peracetic acid

et al. 2021

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Knowledge of the impact of aquaculture chemotherapeutants on fish physiology is scarce. This is particularly relevant for peracetic acid (PAA), a widely used oxidative disinfectant in aquaculture. The chemical behaviour in water is well studied but knowledge about the physiological consequences for fish is limited. The present study investigated the transcriptomics, morphology, and physiology of Atlantic salmon (Salmo salar) responses to PAA and explored how crowding prior to exposure influenced these responses. Post-smolts were subjected to crowding by reducing the water volume thereby increasing the density for 1 h before they were exposed to 4.8 ppm PAA for 30 minutes. The exposed fish were allowed to recover for 2 weeks (w), with samplings carried out at 4 h and 2 w postexposure (p.e.). There were four treatment groups in total: no crowding/control; no crowding/PAA; crowding/control; and crowding/PAA. The physiological changes were documented at the mucosal (i.e., skin and gills) and systemic (i.e., plasma) levels. The overall external welfare score was in good status in all experimental groups. The treatments did not dramatically affect the number of mucous cells in both the skin and the gills. Branchial histomorphology was in a fairly good condition, despite the increased occurrence of epithelial lifting in the crowded groups at 2 w p.e. The gill transcriptome was affected by crowding, PAA, and their combinations more than the skin, as manifested by the number of differentially expressed genes (DEG) in the former. In general, individual stimuli and their combinations elicited strong transcriptional responses in the gills at 4 h p.e. and a marked recovery was observed 2 w thereafter. Crowding altered the dynamics of transcriptional response to PAA especially at 4 h p.e. and the two mucosal tissues demonstrated a contrasting profilea higher number of DEGs in the gills without crowding history, while higher skin DEGs were observed in the group subjected to crowding prior to exposure. Plasma metabolomics identified 639 compounds, and the metabolomic changes were affected mainly by crowding and sampling time, and not by PAA exposure. The results revealed the ability of salmon to mobilise physiological countermeasures to PAA exposure that were differentially influenced by crowding, and that such an effect was remarkably exhibited at the mucosa rather than in the circulating metabolome.

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“…However, a significant mortality occurred during the 24 h post-exposure period, resulting in LC 50 values of 174.1 mg/L and 77.5 mg/L for rock pool shrimp and chameleon shrimps respectively, classifying these species as highly sensitive. In the study by Bechmann et al ( 2019 ), the Northern shrimp ( Pandalus borealis ) was exposed to 15 mg/L H 2 O 2 for 1 h. The very low acute mortality observed immediately after exposure did however increase during the post-exposure period (7 days) but as the total mortality never exceeded 30%, no LC 50 could be calculated. Damage on the gills was observed in the shrimps exposed to H 2 O 2 and suggested as the major cause of the delayed mortality (Bechmann et al 2019 ).…”

Section: Resultsmentioning

confidence: 99%

“…A bath treatment involves the release of a large volume of H 2 O 2 containing waste water and the chemical can potentially be dispersed over a wide area (Burridge et al 2010 , 2014 , Parsons et al 2020 , Refseth et al 2017 ). Therefore, there is a growing concern about the possible toxic effects of H 2 O 2 on non-target aquatic invertebrate species living in the vicinity of fish farms, and specifically crustaceans which has been proven as particularly vulnerable (Smit et al 2008 ; Burridge et al 2014 ; Van Geest et al 2014 ; Gebauer et al 2017 ; Hansen et al 2017 ; Bechmann et al 2019 ; Escobar-Lux et al 2019 ).…”

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confidence: 99%

The Acute and Delayed Mortality of the Northern Krill (Meganyctiphanes norvegica) When Exposed to Hydrogen Peroxide

Escobar-Lux

Samuelsen

2020

Bull Environ Contam Toxicol

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Bath treatment pharmaceuticals used to control sea lice infestations in the salmonid industry, such as hydrogen peroxide (H2O2), are released directly into the environment where non-target organisms are at risk of exposure. The aim of this study was to determine the threshold concentrations for mortality of the Northern krill, Meganyctiphanes norvegica, a major component of the north Atlantic marine ecosystem. To assess the lethal effects of H2O2, we carried out a series of 1 h acute toxicity tests and assessed mortality through a 48 h post-exposure period. One-hour exposure to 170 mg/L, corresponding to 10% of the recommended H2O2 treatment, caused 100% mortality and a subsequent acute median-lethal concentration LC50 value of 32.5 mg/L. Increased mortality was observed with time in all exposed groups, resulting in successively lower LC50 values during the post-exposure period. The suggested H2O2 concentrations have the potential of causing negative effects to the Northern krill.

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Gill damage and delayed mortality of Northern shrimp (Pandalus borealis) after short time exposure to anti-parasitic veterinary medicine containing hydrogen peroxide

Cited by 42 publications

References 25 publications

Oxidative Chemical Stressors Alter the Physiological State of the Nasal Olfactory Mucosa of Atlantic Salmon

Oxidative Chemical Stressors Alter the Physiological State of the Nasal Olfactory Mucosa of Atlantic Salmon

Crowding reshapes the mucosal but not the systemic response repertoires of Atlantic salmon to peracetic acid

The Acute and Delayed Mortality of the Northern Krill (Meganyctiphanes norvegica) When Exposed to Hydrogen Peroxide

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