Abstract
Thiamine deficiency complex (TDC) is a disorder resulting from the inability to acquire or retain thiamine (vitamin B1) and has been documented in organisms in aquatic ecosystems ranging from the Baltic Sea to the Laurentian Great Lakes. The biological mechanisms leading to TDC emergence may vary among systems, but in fishes, one common outcome is high mortality among early life stages. Here, we review the causes and consequences of thiamine deficiency in fishes and identify potential solutions. First, we examine the biochemical and physiological roles of thiamine in vertebrates and find that thiamine deficiency consistently results in impaired neurological function across diverse taxa. Next, we review natural producers of thiamine, which include bacteria, fungi, and plants, and suggest that thiamine is not currently limiting for most animal species inhabiting natural aquatic environments. A survey of historic occurrences of thiamine deficiency identifies consumption of a thiamine-degrading enzyme, thiaminase, as the primary explanation for low levels of thiamine in individuals and subsequent onset of TDC. Lastly, we review conservation and management strategies for TDC mitigation ranging from evolutionary rescue to managing for a diverse forage base. As recent evidence suggests occurrences of thiamine deficiency may be increasing in frequency, increased awareness and a better mechanistic understanding of the underlying causes associated with thiamine deficiency may help prevent further population declines.
Similar content being viewed by others
References
Amcoff P, Börjeson H, Lindeberg J, Norrgren L (1998) Thiamine concentrations in feral Baltic salmon exhibiting the M74 syndrome. In: McDonald DG, Fitzsimons JD, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. American Fisheries Society, Bethesda, pp 82–89
Amend DF, Pietsch JP (1972) Virucidal activity of two iodophors to salmonid viruses. J Fish Res Board Can 29:61–65
Ames BN, Elson-Schwab I, Silver EA (2002) High-dose vitamin therapy stimulates variant enzymes with decreased coenzyme binding affinity (increased K m): relevance to genetic disease and polymorphisms. Am J Clin Nutr 75:616–658
Balk L, Hägerroth P-Å, Åkerman G et al (2009) Wild birds of declining European species are dying from a thiamine deficiency syndrome. Proc Natl Acad Sci 106:12001–12006
Balk L, Hägerroth P-Å, Gustavsson H et al (2016) Widespread episodic thiamine deficiency in Northern Hemisphere wildlife. Sci Rep 6:38821
Bengtsson B-E, Hill C, Bergman Å et al (1999) Reproductive disturbances in Baltic fish: a synopsis of the FiRe project. Ambio 28:2–8
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Bettendorff L (2013) Thiamine. In: Zempleni J, Suttie JW, Gregory JF III, Stover PJ (eds) Handbook of vitamins, 5th edn. CRC Press, Boca Raton, pp 267–324
Bettendorff L, Hennuy B, Wins P, Schoffeniels E (1993) Thiamin and derivatives as modulators of rat brain chloride channels. Neuroscience 52:1009–1017
Bettendorff L, Lakaye B, Kohn G, Wins P (2014) Thiamine triphosphate: a ubiquitous molecule in search of a physiological role. Metab Brain Dis 29:1069–1082
Blakeslee CJ, Sweet SA, Galbraith HS, Honeyfield DC (2015) Thiaminase activity in native freshwater mussels. J Gt Lakes Res 41:516–519
Boś M, Kozik A (2000) Some molecular and enzymatic properties of a homogeneous preparation of thiaminase I purified from carp liver. J Protein Chem 19:75–84
Breves G, Hoeller H, Harmeyer J, Martens H (1980) Thiamin balance in the gastrointestinal tract of sheep. J Anim Sci 51:1177–1181
Breves G, Brandt M, Hoeller H, Rohr K (1981) Flow of thiamin to the duodenum in dairy cows fed different rations. J Agric Sci 96:587–591
Brown SB, Honeyfield DC, Vandenbyllaardt L (1998) Thiamine analysis in fish tissues. In: McDonald G, Fitzsimons J, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and the Baltic Sea, vol 21. American Fisheries Society, Bethesda, Maryland, pp 73–81
Brown SB, Arts MT, Brown LR et al (2005a) Can diet-dependent factors help explain fish-to-fish variation in thiamine-dependent early mortality syndrome? J Aquat Anim Health 17:36–47
Brown SB, Fitzsimons JD, Honeyfield DC, Tillitt DE (2005b) Implications of thiamine deficiency in Great Lakes salmonines. J Aquat Anim Health 17:113–124
Brown SB, Honeyfield DC, Hnath JG et al (2005c) Thiamine status in adult salmonines in the Great Lakes. J Aquat Anim Health 17:59–64
Butterworth RF, Héroux M (1989) Effect of pyrithiamine treatment and subsequent thiamine rehabilitation on regional cerebral amino acids and thiamine-dependent enzymes. J Neurochem 52:1079–1084
Bylund G, Lerche O (1995) Thiamine therapy of M74 affected fry of Atlantic salmon Salmo salar. Bull Eur Assoc Fish Pathol 15:93–97
Carlson SM, Cunningham CJ, Westley PAH (2014) Evolutionary rescue in a changing world. Trends Ecol Evol 29:521–530
Carmody RN, Gerber GK, Luevano JM et al (2015) Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17:72–84
Carvalho PSM, Tillitt DE, Zajicek JL et al (2009) Thiamine deficiency effects on the vision and foraging ability of lake trout fry. J Aquat Anim Health 21:315–325
Casteels M, Sniekers M, Fraccascia P et al (2007) The role of 2-hydroxyacyl-CoA lyase, a thiamin pyrophosphate-dependent enzyme, in the peroxisomal metabolism of 3-methyl- branched fatty acids and 2-hydroxy straight-chain fatty acids. Biochem Soc Trans 35:876–880
Christie MR, Ford MJ, Blouin MS (2014) On the reproductive success of early-generation hatchery fish in the wild. Evol Appl 7:883–896
Chuang DT, Ku LS, Cox RP (1982) Thiamin-responsive maple-syrup-urine disease: decreased affinity of the mutant branched-chain alpha-keto acid dehydrogenase for alpha-ketoisovalerate and thiamin pyrophosphate. Proc Natl Acad Sci 79:3300–3304
Cooper JR, Pincus JH (1979) The role of thiamine in nervous tissue. Neurochem Res 4:223–239
Czesny S, Dettmers JM, Rinchard J, Dabrowski K (2009) Linking egg thiamine and fatty acid concentrations of Lake Michigan lake trout with early life stage mortality. J Aquat Anim Health 21:262–271
Depeint F, Bruce WR, Shangari N et al (2006) Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem Biol Interact 163:94–112
Dettmers JM, Goddard CI, Smith KD (2012) Management of alewife using Pacific salmon in the Great Lakes: whether to manage for economics or the ecosystem? Fisheries 37:495–501
Fisher CW, Lau KS, Fisher CR et al (1991) A 17-bp insertion and a Phe215 → Cys missense mutation in the dihydrolipoyl transacylase (E2) mRNA from a thiamine-responsive maple syrup urine disease patient WG-34. Biochem Biophys Res Commun 174:804–809
Fisher JP, Spitsbergen JM, Iamonte T et al (1995) Pathological and behavioral manifestations of the “Cayuga syndrome”, a thiamine deficiency in larval landlocked Atlantic salmon. J Aquat Anim Health 7:269–283
Fisher JP, Fitzsimons JD, Combs GF, Spitsbergen JM (1996) Naturally occurring thiamine deficiency causing reproductive failure in Finger Lakes Atlantic salmon and Great Lakes trout. Trans Am Fish Soc 125:167–178
Fisher JP, Brown SB, Wooster GW, Bowser PR (1998) Maternal blood, egg and larval thiamin levels correlate with larval survival in landlocked Atlantic salmon (Salmo salar). J Nutr 128:2456–2466
Fitzsimons JD (1995) The effect of B-vitamins on a swim-up syndrome in Lake Ontario lake trout. J Gt Lakes Res 21:286–289
Fitzsimons J, Brown SB (1998) Reduced egg thiamine levels in inland and Great Lakes lake trout and their relationship with diet. In: McDonald G, Fitzsimons JD, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. American Fisheries Society, Bethesda, pp 160–171
Fitzsimons JD, Huestis S, Williston B (1995) Occurrence of a swim-up syndrome in Lake Ontario lake trout in relation to contaminants and cultural practices. J Gt Lakes Res 21:277–285
Fitzsimons JD, Ketola G, Wooster GW, Brown SB (2001a) Use of a thiamine antagonist to induce Cayuga-Syndrome-like mortalities in larval Atlantic salmon. J Aquat Anim Health 13:151–157
Fitzsimons JD, Vandenbyllaardt L, Brown SB (2001b) The use of thiamine and thiamine antagonists to investigate the etiology of early mortality syndrome in lake trout (Salvelinus namaycush). Aquat Toxicol 52:229–239
Fitzsimons JD, Williston B, Amcoff P et al (2005a) The effect of thiamine injection on upstream migration, survival, and thiamine status of putative thiamine-deficient coho salmon. J Aquat Anim Health 17:48–58
Fitzsimons JD, Williston B, Zajicek JL et al (2005b) Thiamine content and thiaminase activity of ten freshwater stocks and one marine stock of alewives. J Aquat Anim Health 17:26–35
Fitzsimons JD, Williston B, Williston G et al (2007) Egg thiamine status of Lake Ontario salmonines 1995–2004 with emphasis on lake trout. J Gt Lakes Res 33:93–103
Fitzsimons JD, Brown SB, Williston B et al (2009) Influence of thiamine deficiency on lake trout larval growth, foraging, and predator avoidance. J Aquat Anim Health 21:302–314
Fitzsimons JD, Brown S, Brown L et al (2010) Increase in lake trout reproduction in Lake Huron following the collapse of alewife: relief from thiamine deficiency or larval predation? Aquat Ecosyst Health Manag 13:73–84
Fitzsimons JD, Wolgamood M, Madenjian CP, Bunnell DB (2012) Thiamine deficiency in aquatic food chains: the cumulative result of ecosystem disruption by clupeids? In: Norrgren L, Levengood J (eds) Ecology and animal health. Baltic University Press, Uppsala, pp 167–180
Fitzsimons JD, Brown SB, Brown LR et al (2013) Impacts of diet on thiamine status of Lake Ontario American eels. Trans Am Fish Soc 142:1358–1369
Fox GA, Allan LJ, Weseloh DV, Mineau P (1990) The diet of herring gulls during the nesting period in Canadian waters of the Great Lakes. Can J Zool 68:1075–1085
Fradin D, Bougneres P (2007) Three common intronic variants in the maternal and fetal thiamine pyrophosphokinase gene (TPK1) are associated with birth weight. Ann Hum Genet 71:578–585
Futia MH, Hallenbeck S, Noyes AD et al (2017) Thiamine deficiency and the effectiveness of thiamine treatments through broodstock injections and egg immersion on Lake Ontario steelhead trout. J Gt Lakes Res 43:352–358
Ghiasi S, Falahatkar B, Arslan M, Dabrowski K (2017) Physiological changes and reproductive performance of Sterlet sturgeon Acipenser ruthenus injected with thiamine. Anim Reprod Sci 178:23–30
Gibson GE, Zhang H (2002) Interactions of oxidative stress with thiamine homeostasis promote neurodegeneration. Neurochem Int 40:493–504
Gibson GE, Ksiezak-Reding H, Sheu K-FR et al (1984) Correlation of enzymatic, metabolic, and behavioral deficits in thiamin deficiency and its reversal. Neurochem Res 9:803–814
Goodrich JK, Waters JL, Poole AC et al (2014) Human genetics shape the gut microbiome. Cell 159:789–799
Goodrich JK, Davenport ER, Waters JL et al (2016) Cross-species comparisons of host genetic associations with the microbiome. Science 352:532–535
Green RG, Evans CA (1940) A deficiency disease of foxes. Science 92:154–155
Hansson S (2001) Stomach analyses of Baltic salmon from 1959–1962 and 1994–1997: possible relations between diet and yolk-sac-fry mortality (M74). J Fish Biol 58:1730–1745
Happel A, Pattridge R, Walsh M, Rinchard J (2017) Assessing diet compositions of Lake Ontario predators using fatty acid profiles of prey fishes. J Gt Lakes Res 43:838–845
Happel A, Jonas JL, McKenna PR et al (2018) Spatial variability of lake trout diets in Lakes Huron and Michigan revealed by stomach content and fatty acid profiles. Can J Fish Aquat Sci 75:95–105
Harbicht AB, Castro-Santos T, Gorsky D et al (2018) Environmental, anthropogenic, and dietary influences on fine scale movement patterns of Atlantic salmon through challenging waters. Can J Fish Aquat Sci. https://doi.org/10.1139/cjfas-2017-0476
Harper CG, Giles M, Finlay-Jones R (1986) Clinical signs in the Wernicke–Korsakoff complex: a retrospective analysis of 131 cases diagnosed at necropsy. J Neurol Neurosurg Psychiatry 49:341–345
Hashimoto Y, Arai S, Nose T (1970) Thiamine deficiency symptoms experimentally induced in the eel. Bull Jpn Soc Sci Fish 36:791–797
Hatheway CL (1990) Toxigenic clostridia. Clin Microbiol Rev 3(1):66–98
He JX, Ebener MP, Riley SC et al (2012) Lake trout status in the main basin of Lake Huron, 1973–2010. North Am J Fish Manag 32:402–412
Honeyfield DC, Hinterkopf JP, Brown SB (2002) Isolation of thiaminase-positive bacteria from alewife. Trans Am Fish Soc 131:171–175
Honeyfield DC, Hinterkopf JP, Fitzsimons JD et al (2005) Development of thiamine deficiencies and early mortality syndrome in lake trout by feeding experimental and feral fish diets containing thiaminase. J Aquat Anim Health 17:4–12
Honeyfield DC, Vandergoot CS, Bettoli PW et al (2007) Thiamine and fatty acid content of walleye tissue from three southern U.S. reservoirs. J Aquat Anim Health 19:84–93
Honeyfield D, Peters A, Jones M (2008) Thiamine and fatty acid content of Lake Michigan Chinook salmon. J Gt Lakes Res 34:581–589
Honeyfield DC, Daniels ME, Brown LR et al (2012) Survey of four essential nutrients and thiaminase activity in five Lake Ontario prey fish species. J Gt Lakes Res 38:11–17
Honeyfield D, Murphy J, Howard K et al (2016) An exploratory assessment of thiamine status in western Alaska Chinook salmon (Oncorhynchus tshawytscha). North Pac Anadromous Fish Comm Bull 6:21–31
Hornung MW, Miller L, Peterson RE et al (1998) Efficacy of thiamine, astaxanthin, β-carotene, and thyroxine treatments in reducing early mortality syndrome in Lake Michigan salmonid embryos. In: McDonald G, Fitzsimons JD, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. American Fisheries Society, Bethesda, pp 124–134
Houde ALS, Saez PJ, Wilson CC et al (2015) Effects of feeding high dietary thiaminase to sub-adult Atlantic salmon from three populations. J Gt Lakes Res 41:898–906
Jacobs GR, Madenjian CP, Bunnell DB et al (2013) Chinook salmon foraging patterns in a changing Lake Michigan. Trans Am Fish Soc 142:362–372
Jenkins AH, Schyns G, Potot S et al (2007) A new thiamin salvage pathway. Nat Chem Biol 3:492–497
Ji YQ, Adelman IR (1998) Thiaminase activity in alewives and smelt in Lakes Huron, Michigan, and Superior. In: McDonald G, Fitzsimons JD, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. American Fisheries Society, Bethesda, pp 154–159
Ji YQ, Warthesen JJ, Adelman IR (1998) Thiamine nutrition, synthesis, and retention in relation to lake trout reproduction in the Great Lakes. In: McDonald G, Fitzsimons JD, Honeyfield DC (eds) Early life stage mortality syndrome in fishes of the Great Lakes and Baltic Sea. American Fisheries Society, Bethesda, pp 99–111
Jude DJ, Tesar FJ, Deboe SF, Miller TJ (1987) Diet and selection of major prey species by Lake Michigan salmonines, 1973–1982. Trans Am Fish Soc 116:677–691
Jurgenson CT, Begley TP, Ealick SE (2009) The structural and biochemical foundations of thiamin biosynthesis. Annu Rev Biochem 78:569–603
Karlsson L, Ikonen E, Mitans A, Hansson S (1999) The diet of salmon (Salmo salar) in the Baltic Sea and connections with the M74 syndrome. Ambio 28:37–42
Keinänen M, Uddström A, Mikkonen J et al (2012) The thiamine deficiency syndrome M74, a reproductive disorder of Atlantic salmon (Salmo salar) feeding in the Baltic Sea, is related to the fat and thiamine content of prey fish. ICES J Mar Sci 69:516–528
Ketola HG, Bowser PR, Wooster GA et al (2000) Effects of thiamine on reproduction of Atlantic salmon and a new hypothesis for their extirpation in Lake Ontario. Trans Am Fish Soc 129:607–612
Ketola HG, Chiotti TL, Rathman RS et al (2005) Thiamine status of Cayuge Lake rainbow trout and its influence on spawning migration. N Am J Fish Manag 25:1281–1287
King-Heiden TC, Mehta V, Xiong KM et al (2012) Reproductive and developmental toxicity of dioxin in fish. Mol Cell Endocrinol 354:121–138
Kitamura T, Seki N, Kihara A (2017) Phytosphingosine degradation pathway includes fatty acid α-oxidation reactions in the endoplasmic reticulum. Proc Natl Acad Sci 114:E2616–E2623
Koski P, Pakarinen M, Nakari T et al (1999) Treatment with thiamine hydrochloride and astaxanthine for the prevention of yolk-sac mortality in Baltic salmon fry (M74 syndrome). Dis Aquat Organ 37:209–220
Kraft CE, Angert ER (2017) Competition for vitamin B1 (thiamin) structures numerous ecological interactions. Q Rev Biol 92:151–168
Kraft CE, Gordon ER, Angert ER (2014) A rapid method for assaying thiaminase I activity in diverse biological samples. PLoS ONE 9:e92688
Kuno Y (1951) Bacillus thiaminolyticus, a new thiamin-decomposing bacterium. Proc Jpn Acad 27:362–365
Ladago BJ, Marsden JE, Evans AN (2016) Early feeding by lake trout fry. Trans Am Fish Soc 145:1–6
Lee B-J, Jaroszewska M, Dabrowski K et al (2009) Effects of vitamin B1 (thiamine) deficiency in lake trout alevins and preventive treatments. J Aquat Anim Health 21:290–301
Lepak JM, Kraft CE, Honeyfield DC, Brown SB (2008) Evaluating the effect of stressors on thiaminase activity in alewife. J Aquat Anim Health 20:63–71
Lim C, Yildirim-Aksoy M, Barros MM, Klesius P (2011) Thiamin requirement of Nile tilapia, Oreochromis niloticus. J World Aquac Soc 42:824–833
Lukienko PI, Mel’nichenko NG, Zverinskii IV, Zabrodskaya SV (2000) Antioxidant properties of thiamine. Bull Exp Biol Med 130:874–876
Lundström J, Börjeson H, Norrgren L (1999a) Histopathological studies of yolk-sac fry of Baltic salmon (Salmo salar) with the M74 syndrome. Ambio 28:16–23
Lundström J, Carney B, Amcoff P et al (1999b) Antioxidative systems, detoxifying enzymes and thiamine levels in Baltic salmon (Salmo salar) that develop M74. Ambio 28:24–29
Mac MJ, Edsall CC, Seelye JG (1985) Survival of lake trout eggs and fry reared in water from the upper Great Lakes. J Gt Lakes Res 11:520–529
Mac MJ, Schwartz TR, Edsall CC, Frank AM (1993) Polychlorinated biphenyls in Great Lakes lake trout and their eggs: relations to survival and congener composition 1979–1988. J Gt Lakes Res 19:752–765
MacCallum WR, Regier HA (1970) Distribution of smelt, Osmerus mordax, and the smelt fishery in Lake Erie in the early 1960’s. J Fish Board Can 27:1823–1846
Madenjian CP, Fahnenstiel GL, Johengen TH et al (2002) Dynamics of the Lake Michigan food web, 1970–2000. Can J Fish Aquat Sci 59:736–753
Marcquenski S, Brown S (1997) Early mortality syndrome (EMS) in salmonid fishes from the Great Lakes. In: Rolland RM, Gilbertson M, Peterson RE (eds) Chemically induced alterations in functional development and reproduction of fishes. SETAC Press, Pensacola, pp 135–152
Marsden JE, Hauser M (2009) Exotic species in Lake Champlain. J Gt Lakes Res 35:250–265
Marsden JE, Kozel CL, Chipman BD (2018) Recruitment of lake trout in Lake Champlain. J Gt Lakes Res 44:166–173
Miller RR (1957) Origin and dispersal of the alewife, Alosa pseudoharengus, and the gizzard shad, Dorosoma cepedianum, in the Great Lakes. Trans Am Fish Soc 86:97–111
Miller TJ, Crowder LB, Rice JA, Marschall EA (1988) Larval size and recruitment mechanisms in fishes: toward a conceptual framework. Can J Fish Aquat Sci 45:1657–1670
Mimouni-Bloch A, Goldberg-Stern H, Strausberg R et al (2014) Thiamine deficiency in infancy: long-term follow-up. Pediatr Neurol 51:311–316
Monteverde DR, Gómez-Consarnau L, Cutter L et al (2015) Vitamin B1 in marine sediments: pore water concentration gradient drives benthic flux with potential biological implications. Front Microbiol 6:434
Nabokina SM, Said HM (2012) A high-affinity and specific carrier-mediated mechanism for uptake of thiamine pyrophosphate by human colonic epithelial cells. AJP Gastrointest Liver Physiol 303:G389–G395
Nishimune T, Watanabe Y, Okazaki H, Akai H (2000) Thiamin is decomposed due to Anaphe spp. entomophagy in seasonal ataxia patients in Nigeria. J Nutr 130:1625–1628
Nott A, Meislin SH, Moore MJ (2003) A quantitative analysis of intron effects on mammalian gene expression. RNA 9:607–617
Nylund A, Hovland T, Hodneland K et al (1994) Mechanisms for transmission of infectious salmon anaemia (ISA). Dis Aquat Organ 19:95–100
Ottinger CA, Honeyfield DC, Densmore CL, Iwanowicz LR (2012) Impact of thiamine deficiency on T-cell dependent and T-cell independent antibody production in lake trout. J Aquat Anim Health 24:258–273
Palace VP, Brown SB, Baron CL et al (1998) An evaluation of the relationships among oxidative stress, antioxidant vitamins and early mortality syndrome (EMS) of lake trout (Salvelinus namaycush) from Lake Ontario. Aquat Toxicol 43:195–208
Pankhurst NW, Sorensen PW (1984) Degeneration of the alimentary tract in sexually maturing European Anguilla anguilla (L.) and American eels Anguilla rostrata (LeSueur). Can J Zool 62:1143–1149
Park LCH, Zhang H, Sheu K-FR et al (1999) Metabolic impairment induces oxidative stress, compromises inflammatory responses, and inactivates a key mitochondrial enzyme in microglia. J Neurochem 72:1948–1958
Pettersson A, Lignell Å (1999) Astaxanthin deficiency in eggs and fry of Baltic salmon (Salmo salar) with the M74 syndrome. Ambio 28:43–47
Quinn TP (2005) The behavior and ecology of Pacific salmon and trout, 1st edn. University of Washington Press, Seattle
Ray BA, Hrabik TR, Ebener MP et al (2007) Diet and prey selection by Lake Superior lake trout during spring, 1986–2001. J Gt Lakes Res 33:104–113
Richter CA, Evans AN, Wright-Osment MK et al (2012) Paenibacillus thiaminolyticus is not the cause of thiamine deficiency impeding lake trout (Salvelinus namaycush) recruitment in the Great Lakes. Can J Fish Aquat Sci 69:1056–1064
Riley SC, Evans AN (2008) Phylogenetic and ecological characteristics associated with thiaminase activity in Laurentian Great Lakes fishes. Trans Am Fish Soc 137:147–157
Riley SC, He JX, Johnson JE et al (2007) Evidence of widespread natural reproduction by lake trout Salvelinus namaycush in the Michigan waters of Lake Huron. J Gt Lakes Res 33:917–921
Riley SC, Rinchard J, Honeyfield DC et al (2011) Increasing thiamine concentrations in lake trout eggs from Lakes Huron and Michigan coincide with low alewife abundance. N Am J Fish Manag 31:1052–1064
Roseman EF, Schaeffer JS, Bright E, Fielder DG (2014) Angler-caught piscivore diets reflect fish community changes in Lake Huron. Trans Am Fish Soc 143:1419–1433
Said HM, Ortiz A, Subramanian VS et al (2001) Mechanism of thiamine uptake by human colonocytes: studies with cultured colonic epithelial cell line NCM460. AJP Gastrointest Liver Physiol 281:G144–G150
Sannino DR, Dobson AJ, Edwards K et al (2018a) The Drosophila melanogaster gut microbiota provisions thiamine to its host. mBio 9:e00155-18
Sannino DR, Kraft CE, Edwards KA et al (2018b) Thiaminase I provides a growth advantage by salvaging precursors from environmental thiamin and its analogs in Burkholderia thailandensis. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01268-18)
Sechi G, Serra A (2007) Wernicke’s encephalopathy: new clinical settings and recent advances in diagnosis and management. Lancet Neurol 6:442–455
Skea JC, Symula J, Miccoli J (1985) Separating starvation losses from other early feeding fry mortality in steelhead trout Salmo gairdneri, Chinook salmon Oncorhynchus tshawytscha, and lake trout Salvelinus namaycush. Bull Environ Contam Toxicol 35:82–91
Stewart DJ, Kitchell JF, Crowder LB (1981) Forage fishes and their salmonid predators in Lake Michigan. Trans Am Fish Soc 110:751–763
Sutherland WJ, Butchart SHM, Connor B et al (2018) A 2018 horizon scan of emerging issues for global conservation and biological diversity. Trends Ecol Evol 33:47–58
Swedberg DV, Peck JW (1984) Food of young-of-the-year lake trout (Salvelinus namaycush) in Presque Isle Harbor, Lake Superior. J Gt Lakes Res 10:280–285
Sylvander P, Häubner N, Snoeijs P (2013) The thiamine content of phytoplankton cells is affected by abiotic stress and growth rate. Microb Ecol 65:566–577
Tillitt DE, Zajicek JL, Brown SB et al (2005) Thiamine and thiaminase status in forage fish of salmonines from Lake Michigan. J Aquat Anim Health 17:13–25
Tillitt DE, Cook PS, Giesy JP et al (2008) Reproductive impairment of Great Lakes lake trout by dioxin-like chemicals. In: Di Giulio RT, Hinton DE (eds) The toxicology of fishes. CRC Press, Boca Raton, FL, pp 819–876
Tillitt DE, Riley SC, Evans AN et al (2009) Dreissenid mussels from the Great Lakes contain elevated thiaminase activity. J Gt Lakes Res 35:309–312
Timpson NJ, Forouhi NG, Brion M-J et al (2010) Genetic variation at the SLC23A1 locus is associated with circulating concentrations of l-ascorbic acid (vitamin C): evidence from 5 independent studies with > 15,000 participants. Am J Clin Nutr 92:375–382
U.S. Department of Agriculture, Agricultural Research Service. 2018. USDA National Nutrient Database for Standar Reference, Legacy. Version Current: April 2018. Nutrient Data Laboratory Home Page. http://www.ars.usda.gov/nutrientdata. Accessed 25 July 2018
Waples RS (1990) Conservation genetics of Pacific salmon. II. Effective population size and the rate of loss of genetic variability. J Hered 81:267–276
Werner RM, Rook B, Greil R (2006) Egg-thiamine status and occurrence of early mortality syndrome (EMS) in Atlantic salmon from the St. Marys River, Michigan. J Gt Lakes Res 32:293–305
Weseloh DV, Ewins PJ, Struger J et al (1995) Double-crested cormorants of the Great Lakes: changes in population size, breeding distribution and reproductive output between 1913 and 1991. Colon Waterbirds 18:48
Whitfield KC, Bourassa MW, Adamolekun B et al (2018) Thiamine deficiency disorders: diagnosis, prevalence, and a roadmap for global control programs: thiamine deficiency-intervention roadmap. Ann N Y Acad Sci. https://doi.org/10.1111/nyas.13919
Widmann M, Radloff R, Pleiss J (2010) The Thiamine diphosphate dependent Enzyme Engineering Database: a tool for the systematic analysis of sequence and structure relations. BMC Biochem 11:9
Wistbacka S, Bylund G (2008) Thiaminase activity of Baltic salmon prey species: a comparision of net- and predator-caught samples. J Fish Biol 72:787–802
Wistbacka S, Heinonen A, Bylund G (2002) Thiaminase activity of gastrointestinal contents of salmon and herring from the Baltic Sea. J Fish Biol 60:1031–1042
Wolf LE (1942) Fish-diet disease of trout: a vitamin deficiency produced by diets containing raw fish. New York State Conservation Department, Bureau of Fish Culture
Wolgamood M, Hnath JG, Brown SB et al (2005) Temporal and spatial variation of early mortality syndrome in salmonids from Lakes Michigan and Huron. J Aquat Anim Health 17:65–76
Wooster GA, Bowser PR, Brown SB, Fisher JP (2000) Remediation of Cayuga Syndrome in landlocked Atlantic salmon Salmo salar using egg and sac-fry bath treatments of thiamine-hydrochloride. J World Aquac Soc 31:149–157
Zajicek JL, Tillitt DE, Honeyfield DC et al (2005) A method for measuring total thiaminase activity in fish tissues. J Aquat Anim Health 17:82–94
Funding
Avril Harder and Mark Christie were supported by funding from the Biological Sciences and Forestry and Natural Resources departments at Purdue University. Donald Tillitt and Cathy Richter were supported by the U.S. Geological Survey Ecosystems Mission Area.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Disclaimer Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government. The findings and conclusions in the article are those of the authors and do not necessarily represent the views of the USFWS.
Rights and permissions
About this article
Cite this article
Harder, A.M., Ardren, W.R., Evans, A.N. et al. Thiamine deficiency in fishes: causes, consequences, and potential solutions. Rev Fish Biol Fisheries 28, 865–886 (2018). https://doi.org/10.1007/s11160-018-9538-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11160-018-9538-x