Cited by 330Aquaculture disease management and microbiotaStress Responses and CortisolReproductive biology and impacts on aquatic species

The DOI matches its Crossref record.

Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha)

Maule, A. G., Tripp, R. A., Kaattari, S. L., Schreck, C. B.·1989·Journal of Endocrinology

DOI 10.1677/joe.0.1200135

Open this paper in CoChat — free account

Abstract

We examined the effects of acute stress on the immune system and disease resistance of juvenile chinook salmon (Oncorhynchus tshawytscha) in laboratory and clinical trials. Immune function, as measured by the ability of lymphocytes from the anterior kidney to generate specific antibody-producing cells (APC) in vitro, was depressed 4 h after stress, when plasma cortisol levels were highest. At the same time, resistance to the fish pathogen, Vibrio anguillarum, was also depressed. Compared with controls, plasma cortisol and APC of stressed fish were unchanged after 24 h, and disease resistance was enhanced as evidenced by higher survival rate and longer mean time to death of mortalities. After 7 days, even though numbers of APC were depressed, plasma cortisol concentration and disease resistance did not differ from controls. This pattern was generally the same, independent of the type of stress applied: i.e. being held out of water in a dipnet for 30 s, manipulation during hatchery operations for 4 h, or transportation for 9 h. These and earlier findings suggest that similar endocrine-immune interactions operate in the mammalian and salmonid systems during acute stress. Journal of Endocrinology (1989) 120, 135–142

Integrity signals

Registry

Crossref · 10.1677/joe.0.1200135

Cites

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Sorted by citations

Items 101–200 of 330

Endocrine responses to environmental pollutants
Brown, J. A. (1993) · Springer eBooks · doi:10.1007/978-94-011-2304-4_11 · Cited by 66
Gene expression in the liver of rainbow trout, Oncorhynchus mykiss, during the stress response
Momoda, T. S., Schwindt, A. R., Feist, G. W., Gerwick, L. G., Bayne, C. J., & Schreck, C. B. (2007) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2007.06.002 · Cited by 70
Self-citation
Measurement of fecal glucocorticoids in parrotfishes to assess stress
Turner, J. W., Nemeth, R. S., & Rogers, C. S. (2003) · General and Comparative Endocrinology · doi:10.1016/s0016-6480(03)00196-5 · Cited by 64
“Stress in individual fish can compromise aspects of their immune function (Maule et al., 1989; Narnaware et al., 1994; Pickering, 1993), growth (McCormick et al.”
Background
Predicting salmon biomass remotely using a digital stereo-imaging technique
Beddow, T. A., Ross, L. G., & Marchant, J. A. (1996) · Aquaculture · doi:10.1016/s0044-8486(96)01384-1 · Cited by 62
Stress responses of Atlantic salmon (Salmo salar L.) elicited by water level reduction in rearing tanks
Einarsdóttir, I. E., & Nilssen, K. J. (1996) · Fish Physiology and Biochemistry · doi:10.1007/bf01875582 · Cited by 61
Effect of corticosteroids on viability and proliferation of the rainbow trout monocyte/macrophage cell line, RTS11
Pagniello, K., Bols, N. C., & Lee, L. E. J. (2002) · Fish & Shellfish Immunology · doi:10.1006/fsim.2001.0395 · Cited by 61
Effect of hyperoxygenation and low water flow on the primary stress response and susceptibility of Atlantic salmon Salmo salar L. to experimental challenge with IPN virus
Fridell, F., Gadan, K., Sundh, H., Taranger, G. L., Glette, J., Olsen, R. E., Sundell, K. S., & Evensen, Ø. (2007) · Aquaculture · doi:10.1016/j.aquaculture.2007.04.081 · Cited by 60
Influence of the tectal zone on the distribution of synaptic boutons in the brainstem of goldfish
Herrero, L., Corvisier, J., Hardy, O., & Torres, B. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19981123)401:3 · Cited by 13
Pathogenicity of vibrios in fish: An overview
Li, J., & Woo, N. Y. S. (2003) · Journal of Ocean University of China · doi:10.1007/s11802-003-0039-7 · Cited by 59
“High levels of circulating steroid hormones have been demonstrated to affect lymphocyte proliferation, decreasing the number of antibody-producing cells and other cellular functions of the immune system, and subsequent immunosuppression and further decrease of disease resistance may result (Maule et al., 1989; Anderso…”
Background
Effect of Dietary Vitamin C on Weight Gain, Tissue Ascorbate Concentration, Stress Response, and Disease Resistance of Channel Catfish Ictalurus punctatus1
Li, M. H., Wise, D. J., & Robinson, E. H. (1998) · Journal of the World Aquaculture Society · doi:10.1111/j.1749-7345.1998.tb00293.x · Cited by 59
Physiological Levels of Testosterone Kill Salmonid Leukocytesin Vitro
Slater, C. H., & Schreck, C. B. (1997) · General and Comparative Endocrinology · doi:10.1006/gcen.1996.6858 · Cited by 59
Self-citation
Genetic, Environmental, and Interaction Effects on Growth and Stress Response of Chinook Salmon (Oncorhynchus tshawytscha) Fry
Heath, D. D., Bernier, N. J., Heath, J. W., et al. (1993) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/f93-049 · Cited by 58
Zebrafish 20β-Hydroxysteroid Dehydrogenase Type 2 Is Important for Glucocorticoid Catabolism in Stress Response
Tokarz, J., Norton, W., Möller, G., de Angelis, M. H., & Adamski, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054851 · Cited by 56
“by diseases in adult fish [19–22].”
Effect of dietary cortisol on resistance of channel catfish to infection by Ichthyopthirius multifiliis and channel catfish virus disease
Davis, K. B., Griffin, B. R., & Gray, W. L. (2003) · Aquaculture · doi:10.1016/s0044-8486(02)00630-0 · Cited by 56
Seasonal changes in the immune activities of common carp (Cyprinus carpio)
Saha, N., Usami, T., & Suzuki, Y. (2002) · Fish Physiology and Biochemistry · doi:10.1023/b:fish.0000009275.25834.67 · Cited by 55
“F reduced antibodyproducing cells in salmonid fish (Maule et al. 1989).”
Background
Ontogeny of the stress response in chinook salmon, Oncorhynchus tshawytscha *
Feist, G. W., & Schreck, C. B. (2001) · Fish Physiology and Biochemistry · doi:10.1023/a:1019709323520 · Cited by 54
“Cortisol can have deleterious effects on immune function (Maule et al. 1989), and down-regulation of both endogenous cortisol and the ability to produce it during stress may be a mechanism to allow for proper development of the immune system.”
BackgroundSelf-citation
Combined effects of high stocking density and Piscirickettsia salmonis treatment on the immune system, metabolism and osmoregulatory responses of the Sub-Antarctic Notothenioid fish Eleginops maclovinus
Vargas‐Chacoff, L., Martínez, D. P., Oyarzún, R., et al. (2014) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2014.07.024 · Cited by 54
Innate and adaptive immune responses in migrating spring-run adult chinook salmon, Oncorhynchus tshawytscha
Dolan, B. P., Fisher, K. M., Colvin, M. E., et al. (2015) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2015.11.015 · Cited by 54
“Cortisol levels increase in fish, which is known to suppress immune function [4,24,25].”
BackgroundSelf-citation
Changes in serum protein and IgM concentration duringsmolting and early post-smolt period in vaccinated and unvaccinated Atlantic salmon (Salmo salar L.).
Melingen, G. O., Stefansson, S. O., Berg, A., et al. (1995) · Fish & Shellfish Immunology · doi:10.1016/s1050-4648(05)80015-4 · Cited by 54
Effect of High Dietary Carbohydrate on the Growth Performance and Physiological Responses of Juvenile Wuchang Bream, Megalobrama amblycephala
Zhou, C., Ge, X., Liu, B., et al. (2013) · Asian-Australasian Journal of Animal Sciences · doi:10.5713/ajas.2012.12659 · Cited by 53
“Fish fed with high carbohydrate diet are assumed to be under constant metabolic stress (Pieper and Pfeffer, 1980; Fletcher, 1981), which may lead to suppressed immune functions (Ellis, 1981; Maule et al., 1989; Wiik et al., 1989; Vielma et al., 2003; Kumar et al., 2005).”
Background
Fish Analgesia: Pain, Stress, Fear Aversion, or Nociception?
Weber, E. S. (2010) · Veterinary Clinics of North America Exotic Animal Practice · doi:10.1016/j.cvex.2010.09.002 · Cited by 53
Fish health challenge after stress. Indicators of immunocompetence
Balasch, J. C., MacKenzie, S. A., & Tort, L. (2005) · Contributions to science · doi:10.2436/cs.v0i0.323 · Cited by 53
Transcriptome analysis reveals carbohydrate-mediated liver immune responses in Epinephelus akaara
Yang, Y., Han, T., Xiao, J., Li, X., & Wang, J. (2018) · Scientific Reports · doi:10.1038/s41598-017-18990-8 · Cited by 50
The effect of large doses of vitamin C AND magnesium on stress responses in common carp, Cyprinus carpio
Dąbrowska, H., Dabrowski, K. R., Meyer‐Burgdorff, K. ‐., HANKE, W., & Günther, K. (1991) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(91)90150-b · Cited by 51
Low Levels of Environmental Ammonia Increase Susceptibility to Disease in Chinook Salmon Smolts
Ackerman, P. A., Wicks, B. J., Iwama, G. K., & Randall, D. J. (2006) · Physiological and Biochemical Zoology · doi:10.1086/504615 · Cited by 50
Optimal Stocking Density for Juvenile Winter Flounder Pseudopleuronectes americanus
Fairchild, E. A., & Howell, W. H. (2001) · Journal of the World Aquaculture Society · doi:10.1111/j.1749-7345.2001.tb00453.x · Cited by 50
A survey of microparasites present in adult migrating Chinook salmon (Oncorhynchus tshawytscha) in south‐western British Columbia determined by high‐throughput quantitative polymerase chain reaction
Bass, A. L., Hinch, S. G., Teffer, A. K., et al. (2017) · Journal of Fish Diseases · doi:10.1111/jfd.12607 · Cited by 49
Effects of stress on fish reproduction, gamete quality, and progeny☆☆Oregon Agricultural Experiment Station Technical Report Number 11578.
Schreck, C. B., Contreras‐Sánchez, W. M., & Fitzpatrick, M. S. (2001) · Elsevier eBooks · doi:10.1016/b978-0-444-50913-0.50005-9 · Cited by 49
Self-citation
Slow release cortisol implants result in impaired innate immune responses and higher infection prevalence following experimental challenge with infectious pancreatic necrosis virus in Atlantic salmon (Salmo salar) parr
Gadan, K., Marjara, I. S., Sundh, H., Sundell, K. S., & Evensen, Ø. (2012) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2012.01.004 · Cited by 48
Alteration of immune function endpoints and differential expression of estrogen receptor isoforms in leukocytes from 17β-estradiol exposed rainbow trout (Oncorhynchus mykiss)
Shelley, L. K., Osachoff, H. L., van Aggelen, G. C., et al. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.09.014 · Cited by 48
“While the effects of cortisol on overall immunocompetence is recognized [39,52], the relationship between circulating E2 concentrations and immune system function is not as well established and existing literature regarding effects at the cellular level is often contradictory.”
The effect of hyperoxygenation and reduced flow in fresh water and subsequent infectious pancreatic necrosis virus challenge in sea water, on the intestinal barrier integrity in Atlantic salmon, Salmo salar L.
Sundh, H., Olsen, R., Fridell, F., Gadan, K., Evensen, Ø., Glette, J., Taranger, G., Myklebust, R., & Sundell, K. S. (2009) · Journal of Fish Diseases · doi:10.1111/j.1365-2761.2009.01047.x · Cited by 48
Beyond mice and men: environmental change, immunity and infections in wild ungulates
Jolles, A. E., Beechler, B. R., & Dolan, B. P. (2014) · Parasite Immunology · doi:10.1111/pim.12153 · Cited by 50
Exposure to Increased Ambient Ultraviolet B Radiation has Negative Effects on Growth, Condition and Immune Function of Juvenile Atlantic Salmon (Salmo salar)
Jokinen, I. E., Markkula, E. S., Salo, H. M., Kuhn, P. S., Nikoskelainen, S., Arts, M. T., & Browman, H. I. (2008) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2008.00358.x · Cited by 46
“Chronic stress is an effective suppressor of immunity, and can lead to decreased immune competence in fish (54).”
Background
Physiological response to challenge tests in six stocks of coho salmon Oncorhynchus kisutch
McGeer, J. C. (2010) · Open Collections · doi:10.14288/1.0098613 · Cited by 47
The effects of stocking density on fish welfare
Baldwin, L. (2024) · PEARL (University of Plymouth) · doi:10.24382/bj18-fb35 · Cited by 46
Immunological alterations in juvenile Pacific herring, Clupea pallasi, exposed to aqueous hydrocarbons derived from crude oil
Kennedy, C. J., & Farrell, A. P. (2007) · Environmental Pollution · doi:10.1016/j.envpol.2007.09.003 · Cited by 44
Cellular responses of the skin and changes in plasma cortisol levels of trout (Oncorhynchus mykiss) exposed to acidified water
Iger, Y., Balm, P. H. M., & Bonga, S. E. W. (1994) · Cell and Tissue Research · doi:10.1007/bf00331371 · Cited by 44
Reference Intervals for Blood Biomarkers in Farmed Atlantic Salmon, Coho Salmon and Rainbow Trout in Chile: Promoting a Preventive Approach in Aquamedicine
Rozas‐Serri, M., Correa, R., Walker-Vergara, R., et al. (2022) · Biology · doi:10.3390/biology11071066 · Cited by 43
Onset of the primary stress in European sea bass Dicentrarhus labrax, as indicated by whole body cortisol in relation to glucocorticoid receptor during early development
Pavlidis, M. A., Karantzali, E., Fanouraki, E., Barsakis, C., Kollias, S., & Papandroulakis, N. (2010) · Aquaculture · doi:10.1016/j.aquaculture.2010.09.013 · Cited by 43
Vulnerability to predation and physiological stress responses of experimentally descaled juvenile chinook salmon,Oncorhynchus tshawytscha
Gadomski, D. M., Mesa, M. G., & Olson, T. M. (1994) · Environmental Biology of Fishes · doi:10.1007/bf00004937 · Cited by 43
“Physiological stress responses associated with descaling could affect survival by depressing immune competence and predisposing fish to disease ( Maule et al. 1989, Peters et al. 1988) or by altering aspects of performance, such as the ability to avoid predation (Sigismondi & Weber 1988, Olla & Davis 1989).”
Background
Coho salmon Oncorhynchus kisutch strain differences in disease resistance and non-specific immunity, following immersion challenges with Vibrio anguillarum
Balfry, S. K., Maule, A. G., & Iwama, G. K. (2001) · Diseases of Aquatic Organisms · doi:10.3354/dao047039 · Cited by 43
“Stress susceptibility has been associated with immunosuppression and a decreased ability to resist infections (Maule et al. 1989, Schreck 1996).”
BackgroundSelf-citation
Whole-body corticosteroid and plasma cortisol concentrations in larval and juvenile Atlantic cod Gadus morhua L. following acute stress
King, W., & Berlinsky, D. L. (2006) · Aquaculture Research · doi:10.1111/j.1365-2109.2006.01558.x · Cited by 42
Histone-like protein: a novel method for measuring stress in fish
Robinette, D. W., & Noga, E. J. (2001) · Diseases of Aquatic Organisms · doi:10.3354/dao044097 · Cited by 42
“Maule et al. (1989) observed that survival of chinook salmon after an experimental challenge with Vibrio anguillarum was higher when the challenge occurred 24 h after transport stress rather than immediately post-transport or 8 d posttransport, suggesting that some stressors may induce a transient…”
Androgens and immunocompetence in salmonids: Specific binding in and reduced immunocompetence of salmonid lymphocytes exposed to natural and synthetic androgens
Slater, C. H., Fitzpatrick, M. S., & Schreck, C. B. (1995) · Aquaculture · doi:10.1016/0044-8486(95)01062-9 · Cited by 42
Self-citation
Stress response in sea bream (Sparus aurata) held under crowded conditions and fed diets containing linseed and/or soybean oil
Ganga, R., Montero, D., Bell, J. G., et al. (2010) · Aquaculture · doi:10.1016/j.aquaculture.2010.11.050 · Cited by 41
“This could be explained by the inability of fish tissue to continue secreting the hormone or an adjustment of the fish to the somewhat mild, non-life threatening intensity of the stressor, as previously described and suggested for other species (Maule et al., 1989; Davis et al., 2002; Caipang et al., 2008).”
Background
Physiological Responses to Challenge Tests in Six Stocks of Coho Salmon (Oncorhynchus kisutch)
McGeer, J. C., Baranyi, L., & Iwama, G. K. (1991) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/f91-208 · Cited by 41
Influence of bacterial kidney disease on smoltification in salmonids: is it a case of double jeopardy?
Mesa, M. G., Maule, A. G., Poe, T. P., et al. (1999) · Aquaculture · doi:10.1016/s0044-8486(99)00012-5 · Cited by 41
Self-citation
The humoral immune system of anadromous fish
Zwollo, P. (2017) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2016.12.008 · Cited by 41
Effects of Steroids on the Antibody Producing Activity of Lymphocytes in Rainbow Trout
Hou, Y., Suzuki, Y., & Aida, K. (1999) · Fisheries Science · doi:10.2331/fishsci.65.850 · Cited by 40
Bacterial lipopolysaccharide (LPS) modulates corticotropin-releasing hormone (CRH) content and release in the brain of juvenile and adult tilapia (Oreochromis mossambicus; Teleostei)
Pepels, P. P. L. M., Bonga, S. E. W., & Balm, P. H. M. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.01316 · Cited by 41
“In fish, the acute-phase response and the susceptibility to bacterial infections are modulated by stress (Maule et al., 1989).”
Background
Measurement of fish size in atlantic salmon (salmo salar l.) cages using stereographic video techniques
Shieh, A., & Petrell, R. J. (1998) · Aquacultural Engineering · doi:10.1016/s0144-8609(97)00012-5 · Cited by 40
Injuries from Non-Retention in Gillnet Fisheries Suppress Reproductive Maturation in Escaped Fish
Baker, M. R., Swanson, P., & Young, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069615 · Cited by 40
“There is extensive documentation on the reduced immunological capacities of fish experiencing acute [28] and chronic [29] exposure to stress.”
Background
Modulation of stress hormones in rainbow trout by means of anesthesia, sensory deprivation and receptor blockade
Gerwick, L. G., Demers, N. E., & Bayne, C. J. (1999) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/s1095-6433(99)00126-9 · Cited by 39
“held [13].”
The effects of stress on androgen production, spermiation response and sperm quality in high and low cortisol responsive domesticated male striped bass
Castranova, D. A., King, W., & Woods, L. C. (2005) · Aquaculture · doi:10.1016/j.aquaculture.2004.12.019 · Cited by 39
“While the generalized stress response is adaptive in the short term, chronic stress can be maladaptive and may lead to more serious consequences such as impaired growth (McCormick et al., 1998; Procarione et al., 1999), decreased resistance to disease ( Maule et al., 1989; Davis et al., 2002 )o r death (Noga et al., 1…”
Background
Capture-Related Stressors Impair Immune System Function in Sablefish
Lupes, S. C., Davis, M. W., Olla, B. L., & Schreck, C. B. (2005) · Transactions of the American Fisheries Society · doi:10.1577/t04-198.1 · Cited by 38
“These results are consistent with other studies in which salmonids were subjected to nonlethal aerial emersions as brief as 30 s (Maule et al. 1989), which caused a significant depression in immune function.”
ResultSelf-citation
Effects of mercuric chloride and sodium selenite on some immune responses of blue gourami, Trichogaster trichopterus (Pallus)
Low, K. W., & Sin, Y. M. (1998) · The Science of The Total Environment · doi:10.1016/s0048-9697(98)00061-8 · Cited by 38
WIND TURBINES CAUSE CHRONIC STRESS IN BADGERS (MELES MELES) IN GREAT BRITAIN
Agnew, R. C. N., Smith, V. J., & Fowkes, R. C. (2016) · Journal of Wildlife Diseases · doi:10.7589/2015-09-231 · Cited by 38
Using truss networks to estimate the biomass of Oreochromis niloticus, and to investigate shape Characteristics
Hockaday, S., Beddow, T. A., Stone, M., et al. (2000) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2000.tb02206.x · Cited by 37
White blood cell profiles of breeding American toads (Bufo americanus) relative to sex and body size
Forbes, M. R., McRuer, D. L., & Shutler, D. (2006) · Comparative Clinical Pathology · doi:10.1007/s00580-006-0623-5 · Cited by 36
“IS could take the form of reduced ability to produce leukocytes or their elements, thus resulting in a decrease in circulating leukocytes in the blood (Maule et al. 1988; Cooper et al. 1992; Maniero and Carey 1997; Hopster et al. 1998).”
Background
Aroclor 1254 exposure reduces disease resistance and innate immune responses in fasted Arctic charr
Maule, A. G., Jørgensen, E. H., Vijayan, M. M., & Killie, J.-E. A. (2004) · Environmental Toxicology and Chemistry · doi:10.1897/03-700.1 · Cited by 36
“Stress-induced elevated cortisol then reduced the disease resistance [29] of fed fish.”
BackgroundResultSelf-citation
Effect Of Anesthetics On Stress And The Innate Immune System Of Gilthead Seabream (Sparus Surata)
Ron, B., & Bressler, K. (2004) · Israeli Journal of Aquaculture - Bamidgeh · doi:10.46989/001c.20367 · Cited by 36
Effects of daily management stress on haematology and blood rheology of the gilthead seabream
PagÉes, T., Gómez, E., Súñer, O., et al. (1995) · Journal of Fish Biology · doi:10.1111/j.1095-8649.1995.tb01601.x · Cited by 36
Effects of didecyldimethylammonium chloride (DDAC) on the swimming performance, gill morphology, disease resistance, and biochemistry of rainbow trout (Oncorhynchus mykiss)
Wood, A. W., Johnston, B. D., Farrell, A. P., et al. (1996) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/f96-201 · Cited by 36
Cortisol profiles in sockeye salmon: Sample bias and baseline values at migration, maturation, spawning, and senescence
Baker, M. R., & Vynne, C. (2014) · Fisheries Research · doi:10.1016/j.fishres.2014.01.015 · Cited by 35
“, 1997; Wingfield and Ramenofsky, 1999), lower immune responses (Balm, 1997;Maule et al., 1989), increasemetabolic costs (Pankhurst andVanDerKraak,1997), and impair responses tophysical challenges (Davis, 2006).”
Background
Early response of salmonid head-kidney cells to stress hormones and toll-like receptor ligands
Ribera, J. M., Nipkow, M., Viergutz, T., Brunner, R. M., Bochert, R., Koll, R., Goldammer, T., Gimsa, U., & Rebl, A. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.11.058 · Cited by 35
Effect of acclimation temperature on the acute stress response in juvenile Atlantic cod, Gadus morhua L., and haddock, Melanogrammus aeglefinus L.
King, W., Buckley, L. J., & Berlinsky, D. L. (2006) · Aquaculture Research · doi:10.1111/j.1365-2109.2006.01623.x · Cited by 35
The synergistic interaction of thermal stress coupled with overstocking strongly modulates the transcriptomic activity and immune capacity of rainbow trout (Oncorhynchus mykiss)
Rebl, A., Korytář, T., Borchel, A., Bochert, R., Strzelczyk, J. E., Goldammer, T., & Verleih, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-71852-8 · Cited by 35
Seasonal changes in cortisol sensitivity and glucocorticoid receptor affinity and number in leukocytes of coho salmon
Maule, A. G., Schreck, C. B., & Sharpe, C. S. (1993) · Fish Physiology and Biochemistry · doi:10.1007/bf00004605 · Cited by 34
Self-citation
Revisiting the Teleost Thymus: Current Knowledge and Future Perspectives
Barraza, F., Montero, R., Wong‐Benito, V., Valenzuela, H., Godoy‐Guzmán, C., Guzmán, F., Köllner, B., Wang, T., Secombes, C. J., Maisey, K. R., et al. (2020) · Biology · doi:10.3390/biology10010008 · Cited by 38
The inhibitory effect of environmental ammonia on Danio rerio LPS induced acute phase response
Gonçalves, A. F., Páscoa, I., Neves, J. V., Coimbra, J., Vijayan, M. M., Rodrigues, P., & Wilson, J. M. (2011) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2011.04.008 · Cited by 33
Susceptibility to furunculosis, cold water vibriosis, and infectious pancreatic necrosis (IPN) in post-smolt Atlantic salmon (Salmo salar L.) as a function of smolt status by seawater transfer
Eggset, G., Mortensen, A., Johansen, L., et al. (1997) · Aquaculture · doi:10.1016/s0044-8486(97)00178-6 · Cited by 32
The effect of feeding level and rearing density on growth, feed conversion and survival in chinook salmon (Oncorhynchus tshawytscha) reared in salt water
Mazur, C. F., Tillapaugh, D., Brett, J. R., et al. (1993) · Aquaculture · doi:10.1016/0044-8486(93)90129-m · Cited by 31
Management of Stress in Fish for Sustainable Aquaculture Development
Akinrotimi, O. A. (2011) · Cited by 30
Streptococcus agalactiaeVaccination and Infection Stress in Nile Tilapia,Oreochromis niloticus
Evans, J. J., Klesius, P. H., Shoemaker, C. A., et al. (2005) · Journal of Applied Aquaculture · doi:10.1300/j028v16n03_07 · Cited by 30
“Maule et al. (1989) found that acute handling stress suppressed antibody producing cells of the head kidney and lowered disease resistance to Vibrio anguillarum infection in chinook salmon.”
Background
Effect of Aloe vera extract on the improvement of the respiratory activity of leukocytes of matrinxã during the transport stress
Zanuzzo, F. S., Biller-Takahashi, J. D., & Urbinati, E. C. (2012) · Revista Brasileira de Zootecnia · doi:10.1590/s1516-35982012001000023 · Cited by 29
“Stress alters the immune function and increases susceptibility to diseases in fish (Maule et al., 1989; Jeney et al., 1997; Ramsay et al., 2009).”
Background
Timing of intraperitoneal administration of β‐1,3/1,6 glucan to rainbow trout, Oncorhynchus mykiss (Walbaum), affects protection against the microsporidian Loma salmonae
Guselle, N. J., Markham, R. J. F., & Speare, D. J. (2007) · Journal of Fish Diseases · doi:10.1111/j.1365-2761.2007.00781.x · Cited by 28
Location-specific consequences of beach seine and gillnet capture on upriver-migrating sockeye salmon migration behavior and fate
Bass, A. L., Hinch, S. G., Patterson, D. A., et al. (2018) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/cjfas-2017-0474 · Cited by 28
“…a need for additional recovery time and indicative of a more severe physiological impact (Jain et al. 1998; Donaldson et al. 2010, 2011) that could have long-term consequences in the form of increased consumption of stored energy and impaired immune defense (Maule et al. 1989; Lupes et al. 2006).”
Background
Distribution and Habitat Associations of Radio‐Tagged Adult Lost River Suckers and Shortnose Suckers in Upper Klamath Lake, Oregon
Banish, N. P., Adams, B. J., Shively, R. S., et al. (2009) · Transactions of the American Fisheries Society · doi:10.1577/t07-252.1 · Cited by 28
“Crowded conditions may have compromised fish health by reducing immune function (Maule et al. 1989), thus causing mortality.”
Background
Group size structure affects patterns of aggression in larval salamanders
Brunkow, P. E., & Collins, J. P. (1998) · Behavioral Ecology · doi:10.1093/beheco/9.5.508 · Cited by 28
“Aggressive behavior can increase stress hormone levels in aggressors as well as in recipients (Abbott, 1987; Fairbanks and McGuire, 1986; Knapp and Moore, 1995; Packer et al, 1995), and raised stress hormone levels can induce metamorphosis in amphibians (Hayes, 1995) and lower resistance to disease in fish ( Maule et…”
Background
Can we get the upper hand on viral diseases in aquaculture of Atlantic salmon?
Robertsen, B. (2011) · Aquaculture Research · doi:10.1111/j.1365-2109.2010.02671.x · Cited by 27
The Effect of AQUI‐S® Sedation on Primary, Secondary, and Tertiary Stress Responses during Salmon Smolt, Salmo salar L., Transport and Transfer to Sea
Iversen, M. H., & Eliassen, R. A. (2009) · Journal of the World Aquaculture Society · doi:10.1111/j.1749-7345.2009.00244.x · Cited by 27
Pathogen loads, clearance and plasma cortisol response in channel catfish, Ictalurus punctatus (Rafinesque), following challenge with Edwardsiella ictaluri
Bilodeau, A. L., Small, B. C., & Wolters, W. R. (2003) · Journal of Fish Diseases · doi:10.1046/j.1365-2761.2003.00481.x · Cited by 27
Effects of a homeopathic complex on the performance and cortisol levels in Nile tilapia (Oreochromis niloticus)
Merlini, L. S., Vargas, L. D., Piau, R., Ribeiro, R. P., & Merlini, N. B. (2014) · Homeopathy · doi:10.1016/j.homp.2013.08.005 · Cited by 26
Short-term stressors and corticosterone effects on immunity in male toads (Rhinella icterica): A neuroimmune-endocrine approach
Titon, S. C. M., Titon, B., Gomes, F. R., & Assis, V. R. (2021) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2021.100230 · Cited by 26
“…following acute stress and treatment with low CORT doses have been previously described for birds (Gao and Deviche, 2019; Shini et al., 2010) and fishes (Maule et al., 1989); demonstrating impaired immune function and reactivity can also be observed following acute physiological increases in CORT.”
Background
Long-term welfare effects of repeated warm water treatments on Atlantic salmon (Salmo salar)
Moltumyr, L., Nilsson, J., Madaro, A., et al. (2021) · Aquaculture · doi:10.1016/j.aquaculture.2021.737670 · Cited by 26
Stereo Vison and Mask-RCNN Segmentation Based 3D Points Cloud Matching for Fish Dimension Measurement
Huang, K., Li, Y., Suo, F., et al. (2020) · Chinese Control Conference (CCC) · doi:10.23919/ccc50068.2020.9188604 · Cited by 25
“This process is invasive, time-consuming, labor intensive and has negative effects on the growth of fishes leading to significantly lower feed intake and growth rate [3].”
Background
Effect of PRL, GH and cortisol on the serum complement and IgM levels in gilthead seabream (Sparus aurata L.)
Cuesta, A., Laiz‐Carrión, R., Arjona, F. J., et al. (2005) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2005.05.010 · Cited by 25
Gelatinized to non‐gelatinized starch ratio in the diet of Labeo rohita: effect on digestive and metabolic response and on growth
Kumar, V., Sahu, N. P., Pal, A. K., et al. (2007) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/j.1439-0396.2007.00739.x · Cited by 25
Carbohydrate utilization in black seabream: Effects of the carbohydrate sources on growth, insulin signalling pathway and hepatic glucose metabolism
Taj, S., Irm, M., Jin, M., et al. (2020) · Aquaculture Nutrition · doi:10.1111/anu.13150 · Cited by 25
Effect of Nanophyetus salmincola and Bacterial Co-Infection on Mortality of Juvenile Chinook Salmon
Roon, S. R., Alexander, J. D., Jacobson, K. C., et al. (2015) · Journal of Aquatic Animal Health · doi:10.1080/08997659.2015.1094150 · Cited by 25
“Jacobson et al. (2003) challenged juvenile Chinook Salmon following acclimatization to saltwater, a physiological change that can contribute to a greater immunocompromised state (Maule et al. 1989; Tort 2011) and might have altered the effect N. salmincola had on the host.”
Background
Performance of juvenile steelhead trout (Oncorhynchus mykiss) produced from untreated and cryopreserved milt
Hayes, M. C., Rubin, S. P., Hensleigh, J. E., et al. (2005) · Aquaculture · doi:10.1016/j.aquaculture.2005.04.035 · Cited by 24
Effects of rearing stress on Atlantic salmon (Salmo salarL.) antibody response to a non-pathogenic antigen
Einarsdóttir, I. E., Nilssen, K. J., & Iversen, M. H. (2000) · Aquaculture Research · doi:10.1046/j.1365-2109.2000.00506.x · Cited by 24
Leucocyte populations and responses to immunization and photoperiod manipulation in Atlantic salmon (Salmo salar L.) 0+ smolt
Melingen, G. O., Pettersen, E. F., & Wergeland, H. I. (2002) · Aquaculture · doi:10.1016/s0044-8486(01)00866-3 · Cited by 24
Effects of dietary carbohydrate-to-lipid ratio on the growth performance and feed utilization of juvenile turbot (Scophthalmus maximus)
Miao, S., Nie, Q., Miao, H., et al. (2016) · Journal of Ocean University of China · doi:10.1007/s11802-016-2934-8 · Cited by 23
Rates of cortisol increase and decrease in channel catfish and sunshine bass exposed to an acute confinement stressor
Davis, K. B., & Small, B. C. (2006) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2006.01.003 · Cited by 25
“Recent evidence, however, suggests that plasma cortisol may have both positive and negative effects on immune function and disease resistance (Maule et al., 1989; Dhabhar and McEwen, 2001).”
Background
Aphanomyces invadansin Atlantic Menhaden along the East Coast of the United States
Blazer, V. S., Lilley, J. H., Schill, W. B., Kiryu, Y., Densmore, C. L., Panyawachira, V., & Chinabut, S. (2002) · Journal of Aquatic Animal Health · doi:10.1577/1548-8667(2002)014 · Cited by 57
Transportation and Handling
Wedemeyer, G. A. (1996) · Developments in aquaculture and fisheries science · doi:10.1016/s0167-9309(96)80015-9 · Cited by 23
Survey of Pathogens in Hatchery Chinook Salmon with Different Out-Migration Histories through the Snake and Columbia Rivers
Gaest, A. L. V., Dietrich, J. P., Thompson, D. E., Boylen, D. A., Strickland, S. A., Collier, T. K., Loge, F. J., & Arkoosh, M. R. (2011) · Journal of Aquatic Animal Health · doi:10.1080/00028487.2011.572023 · Cited by 22
“Differences in the hatchery rearing environment such as disease outbreaks and resulting antibiotic treatments, or size at release, can influence disease resistance (Maule et al. 1989; Salonius and Iwama 1993).”
The immunomodulatory effects of the dimer of lysozyme (KLP-602) in carp (Cyprinus carpio L)—in vivo study
Rymuszka, A., Studnicka, M., Siwicki, A. K., et al. (2004) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2004.07.005 · Cited by 22
Untitled work
(2002) · doi:10.1577/1548-8659(2002)131
Self-citation

Authors: Maule, A. G., Tripp, R. A., Kaattari, S. L., & Schreck, C. B.
Affiliations: Oregon State University (US)
ORCID: Tripp, R. A.
Venue: Journal of Endocrinology
Publisher: Bioscientifica
Published: 1989-01-01
Volume: 120
Issue: 1
Pages: 135-142
ISSN: 0022-0795 (ISSN-L)
1479-6805
DOI: 10.1677/joe.0.1200135
OpenAlex: W2035540083
Cited by: 330
References: 0
Citations by year: 2026: 3 · 2025: 4 · 2024: 3 · 2023: 3 · 2022: 7 · 2021: 8 · 2020: 9 · 2019: 7 · 2018: 6 · 2017: 6 · 2016: 5 · 2015: 8 · 2014: 14 · 2013: 6 · 2012: 13
FWCI: 2.31
Type: journal article
Language: en
Open access: closed
Locations: Journal of Endocrinology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords: acute stress, Oncorhynchus tshawytscha, immune function, disease resistance, cortisol, antibody-forming cells, Vibrio anguillarum, endocrine-immune interaction, fish handling stress, hatchery operations, transport stress
MeSH terms: Acute Disease, Animals, Antibody-Producing Cells, Cell Count, Hydrocortisone, Immunity, Innate, Salmon, Stress, Physiological, Time Factors, Vibrio Infections

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha)

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cited by

Related

Metadata

Record

About these checks