Enteric bacterial pathogen detection in southern sea otters (Enhydra lutris nereis) is associated with coastal urbanization and freshwater runoff
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Although protected for nearly a century, California's sea otters have been slow to recover, in part due to exposure to fecally-associated protozoal pathogens like Toxoplasma gondii and Sarcocystis neurona. However, potential impacts from exposure to fecal bacteria have not been systematically explored. Using selective media, we examined feces from live and dead sea otters from California for specific enteric bacterial pathogens (Campylobacter, Salmonella, Clostridium perfringens, C. difficile and Escherichia coli O157:H7), and pathogens endemic to the marine environment (Vibrio cholerae, V. parahaemolyticus and Plesiomonas shigelloides). We evaluated statistical associations between detection of these pathogens in otter feces and demographic or environmental risk factors for otter exposure, and found that dead otters were more likely to test positive for C. perfringens, Campylobacter and V. parahaemolyticus than were live otters. Otters from more urbanized coastlines and areas with high freshwater runoff (near outflows of rivers or streams) were more likely to test positive for one or more of these bacterial pathogens. Other risk factors for bacterial detection in otters included male gender and fecal samples collected during the rainy season when surface runoff is maximal. Similar risk factors were reported in prior studies of pathogen exposure for California otters and their invertebrate prey, suggesting that land-sea transfer and/or facilitation of pathogen survival in degraded coastal marine habitat may be impacting sea otter recovery. Because otters and humans share many of the same foods, our findings may also have implications for human health.
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Clostridia (e.g., Clostridium perfringens, Clostridioides difficile) are naturally present in the normal gut microbiome and fecal samples of asymptomatic marine mammals, fish, mollusks, and crustaceans, with ubiquitous distribution in freshwater and marine environments in water, sediment, sewage, and biota and on biological substrates.
“Clostridia (e.g., Clostridium perfringens, Clostridioides difficile) are naturally present in the normal gut microbiome and fecal samples of asymptomatic marine mammals, fish, mollusks, and crustaceans (McBee, 1960;Aschfalk and Müller, 2001;Miller et al., 2010;Morris et al., 2011), with ubiquitous distribution in freshwater and marine environments in water, sediment, sewage, and biota and on”
From Novel Lethal Clostridial Infection in Florida Manatees (Trichechus manatus latirostris): Cause of the 2013 Unusual Mortality Event in the Indian River Lagoon (2022) · cites this paper as Miller et al., 2010
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- [1]Abeyta C., Deeter F.G., Kaysner C.A., Stott R.F., Wekell M.M., Campylobacter jejuni in a Washington state shellfish growing bed associated with illness, J. Food Protect. (1993) 56: 323– 325 31091626
- [2]Altekruse S.F., Cohen M.L., Swerdlow D.L., Emerging foodborne diseases, Emerg. Infect. Dis. (1997) 3: 285– 293 9284372 PMC2627632
- [3]Aschfalk A., Müller W., Clostridium perfringens toxin types in hooded seals in the Greenland Sea, determined by PCR and ELISA, J. Vet. Med. (2001) 48: 765– 769 11846022
- [4]Bell J.A., Manning D.D., Reproductive failure in mink and ferrets after intravenous or oral inoculation of Campylobacter jejuni, Can. J. Vet. Res. (1990) 4: 432– 437 PMC1255689 2249178
- [5]Blake P.A., Vibrios on the half shell: what the walrus and carpenter didn’t know, Ann. Intern. Med. (1983) 99: 558– 559 6625388
- [6]Buck J.D., Wells R.S., Rhinehart H.L., Hansen L.J., Aerobic microorganisms associated with free-ranging bottlenose dolphins in coastal Gulf of Mexico and Atlantic Ocean waters, J. Wildl. Dis. (2006) 42: 536– 544 17092884
- [7]Cooley M., Carychao D., Crawford-Miksza L., Jay M.T., Myers C., Rose C.,, Incidence and tracking of Escherichia coli O157:H7 in a major produce production region in California, PLoS ONE (2007) 2: e1159 18174909 PMC2174234
- [8]Dabritz H.A., Atwill E.R., Gardner I.A., Miller M.A., Conrad P.A., Outdoor fecal deposition by free-roaming cats and attitudes of cat owners and nonowners toward stray pets, wildlife, and water pollution, J. Am. Vet. Med. Assoc. (2006) 229: 74– 81 16817717
- [9]Davies C.M., Long J.A., Donald M., Ashbolt N.J., Survival of fecal microorganisms in marine and freshwater sediments, Appl. Environ. Microbiol. (1995) 61: 1888– 1896 7646026 PMC167451
- [10]Edwards D.D., McFeters G.A., Venkatesan M.I., Distribution of Clostridium perfringens and fecal sterols in a benthic coastal marine environment influenced by the sewage outfall from McMurdo station, Antarctica, Appl. Environ. Microbiol. (1998) 64: 2596– 2600 9647835 PMC106431
- [11]Higgins R., Bacteria and fungi of marine mammals: a review, Can. Vet. J. (2000) 41: 105– 116 10723596 PMC1476275
- [12]Hunter D.B., Prescott J.F., Hoover D.M., Hlywka G., Kerr J.A., Campylobacter colitis in ranch mink in Ontario, Can. J. Vet. Res. (1986) 50: 47– 53 3742356 PMC1255158
- [13]Jones K., Howard S., Wallace J.S., Intermittent shedding of thermophilic Campylobacters by sheep at pasture, J. Appl. Microbiol. (1999) 86: 531– 536 10196758
- [14]Kain K., Kelly M.T., Clinical features, epidemiology, and treatment of Plesiomonas shigelloides diarrhea, J. Clin. Microbiol. (1989) 27: 998– 1001 2745707 PMC267470
- [15]Kaysner C.A., Abeyta C. Jr, Wekell M.M., DePaola A. Jr, Stott R.F., Leitch J.M., Incidence of Vibrio cholerae from estuaries of the United States West Coast, Appl. Environ. Microbiol. (1987) 53: 1344– 1348 3606111 PMC203867
- [16]Kenyon J.E., Piexoto D.R., Austin B., Gillies D.C., Seasonal variation in numbers of Vibrio cholerae (non-O1) isolated from California coastal waters, Appl. Environ. Microbiol. (1984) 47: 1243– 1245 6742842 PMC240204
- [17]Knap A., Dewailly E., Furgal C., Galvin J., Baden D., Bowen R.E., et al., Indicators of ocean health and human health: developing a research and monitoring network, Environ. Health Perspect. (2002) 110: 839– 845 12204815 PMC1240980
- [18]Kulldorff M., Nagarwalla N., Spatial disease clusters: detection and inference, Stat. Med. (1995) 14: 799– 810 7644860
- [19]Kumar S., Shorenstein M.L., Niven N., Stroe M., Non-O1 Vibrio Cholerae gastroenteritis in Northern California, West. J. Med. (1984) 140: 783– 784 6730494 PMC1011101
- [20]Lipp E.K., Huq A., Colwell R.R., Effects of global climate on infectious disease; the cholera model, Clin. Microbiol. Rev. (2002) 15: 757– 770 12364378 PMC126864
- [21]Lisle J.T., Smith J.J., Edwards D.D., McFeters G.A., Occurrence of microbial indicators and Clostridium perfringens in wastewater, water column samples, sediments, drinking water and Weddell seal feces collected at McMurdo station, Antarctica, Appl. Environ. Microbiol. (2004) 70: 7269– 7296 15574926 PMC535152
- [22]Maugeri T.L., Carbone M., Fera M.T., Irrera G.P., Gugliandolo C., Distribution of potentially pathogenic bacteria as free living and plankton-associated in a marine coastal zone, J. Appl. Microbiol. (2004) 97: 354– 361 15239702
- [23]McLaughlin J.B., DePaola A., Bopp C.A., Martinek K.A., Napolilli N.P., Allison C.G., et al., Outbreak of Vibrio parahaemolyticus gastroenteritis associated with Alaskan oysters, N. Engl. J. Med. (2005) 353: 1463– 1470 16207848
- [24]Miller M.A., Gardner I.A., Packham A., Jessup D., Jameson R., Dodd E., Conrad P.A., Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection in southern sea otters (Enhydra lutris nereis), Int. J. Parasitol. (2002) 32: 997– 1006 12076629
- [25]Miller M.A., Miller W.A., Conrad P.A., James E.R., Melli A.C., Leutenegger C.M.,, Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters, Int. J. Parasitol. (2008) 34: 275– 284 18452923
- [26]Miller M.A., Conrad P.A., Harris M., Hatfield B., Langlois G., Jessup D.A.,, Localized epizootic of meningoencephalitis in southern sea otters (Enhydra lutris nereis) caused by Sarcocystis neurona, Vet. Parasitol. (in press) PMC4907795 20615616
- [27]Miller W.A., Atwill E.R., Gardner I.A., Miller M.A., Fritz H., Hedrick R.P.,, Clams (Corbicula fluminea) as bioindicators of fecal contamination with Cryptosporidium and Giardia spp. in freshwater ecosystems in California, Int. J. Parasitol. (2005) 35: 673– 684 15862580
- [28]Miller W.A., Miller M.A., Gardner I.A., Atwill E.R., Harris M., Ames J.,, New genotypes and factors associated with Cryptosporidium detection in mussels (Mytilus spp.) along the California coast, Int. J. Parasitol. (2005) 35: 1103– 1113 15993883
- [29]Miller W.A., Miller M.A., Gardner I.A., Atwill E.R., Byrne B.A., Jang S.,, Salmonella spp., Vibrio spp., Clostridium perfringens and Plesiomonas shigelloides in freshwater and marine invertebrates from coastal California ecosystems, Microb. Ecol. (2006) 52: 198– 206 16897302
- [30]Mouriño-Pérez R.R., Worden A.Z., Azam F., Growth of Vibrio cholerae O1 in red tide waters off California, Appl. Environ. Microbiol. (2003) 69: 6923– 6931 14602656 PMC262290
- [32]Schlundt J., Toyofuku H., Jansen J., Herbst S.A., Emerging food-borne zoonoses, Rev. Sci. Tech. (2004) 23: 513– 533 15702717
- [33]Schulman F.Y., Montali R.J., Hauer P.J., Gastroenteritis associated with Clostridium perfringens type A in black-footed ferrets (Mustela nigripes), Vet. Pathol. (2003) 30: 308– 310 8333113
- [34]Skanavis C., Yanko W.A., Clostridium perfringens as a potential indicator for the presence of sewage solids in marine sediments, Mar. Pollut. Bull. (2001) 42: 31– 35 11382981
- [35]Smith W.A., Mazet J.K., Hirsh D.C., Salmonella in California wildlife species: prevalence in rehabilitation centers and characterization of isolates, J. Zoo Wildl. Med. (2002) 33: 228– 235 12462489
- [36]Steele C.M., Brown R.N., Botzler R.G., Prevalence of zoonotic bacteria among seabirds in rehabilitation centers along the Pacific Coast of California and Washington, USA, J. Wildl. Dis. (2005) 41: 735– 744 16456162
- [37]Stoddard R.A., Gulland F.M., Atwill E.R., Lawrence J., Jang S., Conrad P.A., Salmonella and Campylobacter spp. in Northern elephant seals, California, Emerg. Infect. Dis. (2005) 11: 1967– 1969 PMC3367645 16485493
- [38]Su Y.C., Liu C., Vibrio parahaemolyticus: a concern of seafood safety, Food Microbiol. (2007) 24: 549– 558 17418305
- [39]Thornton S.M., Nolan S., Gulland F.M., Bacterial isolates from California sea lions (Zalophus californianus), harbor seals (Phoca vitulina) and northern elephant seals (Mirounga angustirostris) admitted to a rehabilitation center along the central California coast, 1994–1995, J. Zoo Wildl. Med. (1998) 29: 171– 176 9732032
- [40]Venkateswaran K., Takai T., Navarro I.M., Nakano H., Hashimoto H., Siebeling R.J., Ecology of Vibrio cholerae non-O1 and Salmonella spp. and role of zooplankton in their seasonal distribution in Fukuyama coastal waters, Japan, Appl. Environ. Microbiol. (1989) 55: 1591– 1598 PMC202910 2764569
- [41]Williams C., Elnif J., Buddington R.K., The gastrointestinal bacteria of mink (Mustela vision L.): influence of age and diet, Acta Vet. Scand. (1998) 39: 473– 482 9926461 PMC8050671
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Landsberg, J. H., Tabuchi, M., Rotstein, D. S., Subramaniam, K., Rodrigues, T. C. S., Waltzek, T. B., Stacy, N. I., Wilson, P. W., Kiryu, Y., Uzal, F. A., et al. (2022) · Frontiers in Marine Science · doi:10.3389/fmars.2022.841857 · Cited by 20 · see citing works
- Authors
- Miller, M. A., Byrne, B. A., Jang, S. S., Dodd, E. M., Dorfmeier, E., Harris, M. D., Ames, J., Paradies, D., Worcester, K., Jessup, D. A., & Miller, W. A.
- Affiliations
- California Department of Fish and Wildlife (US)
- Veterinary Medical Teaching Hospital (US)
- University of California, Davis (US)
- Corresponding author
- Miller, Melissa A.
- Venue
- Veterinary Research
- Publisher
- EDP Sciences
- Published
- 2009-09-02
- Volume
- 41
- Issue
- 1
- Pages
- 01
- ISSN
- 0928-4249 (ISSN-L)
- 1297-9716
- PMC
- PMC2769548
- OpenAlex
- W2120072624
- Cited by
- 113
- References
- 0
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 14 · 2020: 13 · 2019: 11 · 2018: 7 · 2017: 5 · 2016: 7 · 2015: 7 · 2014: 9 · 2013: 6 · 2012: 9
- FWCI
- 6.55
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Veterinary Research (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Springer Link (Chiba Institute of Technology) (submittedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- California Department of Fish and Game
- Massachusetts Department of Fish and Game
- U.S. Fish and Wildlife Service
- U.S. Geological Survey
- Topics
- Physical Sciences › Environmental Science › Water Science and Technology › Fecal contamination and water quality
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Vibrio bacteria research studies
- Keywords
- southern sea otter, Enhydra lutris nereis, enteric bacterial pathogens, fecal bacteria, coastal urbanization, freshwater runoff, Campylobacter, Salmonella, Clostridium perfringens, Clostridium difficile, Escherichia coli O157:H7, Vibrio parahaemolyticus, Vibrio cholerae, Plesiomonas shigelloides, human health implications, California coast
- MeSH terms
- Animals, Bacterial Infections, California, Feces, Female, Male, Otters, Pacific Ocean, Risk Factors, Urbanization, Water Microbiology, Water Pollution, Ecosystem
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