HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Steele, C. M. Articles by Botzler, R. G. Search for Related Content PubMed PubMed Citation Articles by Steele, C. M. Articles by Botzler, R. G.

¹ Department of Wildlife, Humboldt State University, Arcata, California 95521, USA
³ Corresponding author (email: csteele{at}abrinc.com)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
ABSTRACT:   Many seabirds are rehabilitated annually by wildlife rehabilitation centers along the Pacific Coast, USA. Although various strains of zoonotic bacteria have been isolated from seabirds, risks to rehabilitators at these centers have not been well documented. From November 2001 through January 2003, we determined the prevalence of detectable enteric fauna by isolation and characterization of Gram-negative bacteria from cloacal swabs taken from 26 common murres (Uria aalge), 49 gulls (Larus spp.), and 14 other seabirds treated by rehabilitators in California and Washington (USA). At least 25 bacterial species were identified, including multiple strains of Escherichia coli, as well as Enterobacter cloacae, Citrobacter freundii, and Klebsiella pneumoniae. Antibiotic resistance was found in 13 of 19 bacterial isolates tested, including E. coli, K. pneumoniae, Acinetobacter baumanii, and Pseudomonas aeruginosa. Potential transfer of these bacteria poses a risk to wildlife rehabilitators and to seabirds in these centers, as well as to free-ranging birds.
  Key words:  Antibiotic resistance, rehabilitation centers, seabirds, zoonotic bacteria.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Each year, thousands of seabirds affected by oil contamination, injury, or illness are brought to rehabilitation centers along the Pacific Coast of the continental USA. These centers are staffed by veterinarians, technicians, and volunteers. The birds under the care of the centers are treated and, when possible, released back to the wild. Seabirds are particularly vulnerable to the effects of oil contamination (Jessup and Leighton, 1996); in larger oil spills, hundreds of seabirds may be treated at a center in a matter of days or weeks. Two of the most abundant avian groups on the Pacific Coast of the USA are common murres (Uria aalge) and gulls (Larus spp.) (Sibley, 2000). Common murres frequently are affected by oil during marine spills (Debacker et al., 1997), and both common murres and gulls routinely come into contact with humans at rehabilitation centers on the Pacific Coast (Smith et al., 2002).

Rehabilitation workers come into close contact with these birds, their feces and other body fluids, and soiled bedding materials. Animals stressed by illness, capture, and captivity are more likely to shed potentially pathogenic bacteria than are healthy, free-ranging birds (Smith et al., 2002). Because many enteric zoonotic bacteria are transmitted by the fecal-oral route, seabirds in rehabilitation centers may serve as sources of disease agents. Conversely, seabirds also may acquire pathogenic bacteria at rehabilitation centers, and once they are released back to the wild, they could spread potential pathogens to free-ranging seabird populations (Ziegerer et al., 2002).

Zoonotic Gram-negative bacteria previously isolated from seabird species include, but are not limited to, Salmonella spp., Campylobacter spp., and Yersinia spp. (Kapperud and Rosef, 1983). In humans, these bacteria can cause gastroenteritis, respiratory symptoms, septicemia, and even mortality; for example, the multiple and ubiquitous strains of Salmonella pose a considerable public health threat and are often associated with disease outbreaks (Velge et al., 2005).

The liberal use of antibiotics in medicine and animal husbandry over the course of decades has fostered the selection of resistant bacteria (Tomasz, 1994). The rise in multi-drug resistant pathogenic and commensal bacteria is of global concern, because it can lead to increased human and domestic animal healthcare costs and increased morbidity and mortality (Williams and Heymann, 1998). Ziegerer et al. (2002) found that the number of antibiotic-resistant strains of bacteria isolated from birds at Tufts University Veterinary Clinic (Grafton, Massachusetts, USA) increased while birds were in the clinic. To better assess the risks of exposure to zoonotic bacteria by rehabilitation workers, free-living wild birds, and birds brought to rehabilitation centers, it is essential to first establish the zoonotic bacteria carried by birds in rehabilitation centers as well as any antibiotic resistance carried in these bacteria.

Our objectives were to survey seabirds in rehabilitation centers to compare prevalences of enteric species between and among groups of common seabirds, as well as to compare bacterial species richness between rehabilitation centers (with an n value of at least six per bird family). In addition, we investigated the potential pathogenicity to humans of selected isolates of Escherichia coli by testing for the presence of toxin genes. Finally, we tested antibiotic resistance in isolates that were selected to represent a variety of bacterial species as well as possible variation in strains among host species. This information was used to assess which bacteria might pose a risk to rehabilitators working with seabirds and others birds in these centers, as well as free-living wild birds.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Seabirds were sampled at rehabilitation centers in California and Washington from November 2001 to January 2003 (Steele, 2003). Eighty-nine birds representing 16 species were sampled, with the highest numbers from the families Laridae and Alcidae (Table 1). Birds were sampled from the Humboldt Wildlife Care Center, Arcata, California (USA; 40.72359°N, 123.86225°W), in November and December 2001; the San Francisco Bay Oiled Wildlife Care and Education Center, Cordelia, California (38.24570°N, 122.00984°W), in January, April, May, and June of 2002; the Progressive Animal Welfare Society (PAWS) Wildlife Center, Lynwood, Washington (USA; 47.62691°N, 122.12881°W), in January, April, and August 2002, and January 2003; and the Los Angeles Oiled Bird Care and Education Center, San Pedro, California (33.733894°N, 118.291425°W), in July 2002. Any birds that had been treated with antibiotics were excluded from the study.

A fecal suspension in 1.0 ml sterile saline (0.85% NaCl) was made for each Cultureswab. The suspension was plated onto four different culture media. The initial isolation media used were MacConkey agar (Difco, Becton Dickinson and Company), Levine EMB agar (BBL, Becton Dickinson and Company), trypticase soy agar with 0.5% yeast extract (TSA/YE; Difco, Becton Dickinson and Company), and tetrathionate broth with iodine (Difco, Becton Dickinson and Company). All plates were examined after 24, 48, and 72 hr of incubation at 37 C in an aerobic chamber. After 24 hr, subcultures were made from the tetrathionate broth onto Salmonella-Shigella agar (BBL, Becton Dickinson and Company). Representatives of all distinct colony types were Gram stained and subcultured for purity onto a TSA/ YE plate. We stored each purified isolate on TSA/YE slants at 4 C.

Each isolate was inoculated into Kligler’s Iron Agar (Difco, Becton Dickinson and Company) and SIM medium (BBL, Becton Dickinson and Company) to test for hydrogen sulfide production, glucose and lactose fermentation, indole production, and motility. Capacity to grow on MacConkey agar was tested for all isolates not originally cultured from MacConkey agar. Representative Gram-negative isolates of all distinct organisms were identified using the API-20E differentiation system (BioMérieux Vitek, Inc., Hazelwood, Missouri, USA). Growth at 42 C was used to confirm the identification of Pseudomonas aeruginosa and Acinetobacter baumanii (Anonymous, 1992).

Initial typing of Salmonella spp. isolates was performed at the Veterinary Medical Teaching Hospital at the University of California in Davis, California (Smith et al., 2002). Salmonella spp. serotyping was performed by the National Animal Disease Laboratory (Ames, Iowa, USA) (Edwards and Ewing, 1986).

Prevalences (number of birds infected/number of birds examined) of bacteria isolated were compared between groups of birds with a Fisher Exact test using Number Cruncher Statistical Systems statistical software (Hintze, 2001). We used a two-way general linear model analysis of variance (ANOVA) to examine differences in species richness of bacteria isolated from common murres and gulls and between two rehabilitation centers: San Francisco Bay Oiled Wildlife Care and Education Center and the PAWS Wildlife Center. P values of 0.05 or less were considered significant. Species richness values were square-root transformed for normality.

Forty-eight E. coli isolates were selected by their API 20E codes to represent the variability within isolates recovered from all the birds, as well as between species of birds. These were tested for the presence of the following toxin genes at the Gastroenteric Disease Center at Pennsylvania State University (University Park, Pennsylvania, USA): presence of shiga-toxin I and II (Witham et al., 1996), heat-stable toxin a, heat-stable toxin b, and heat-labile toxin (Ojeniyi et al., 1994), entero-attaching and effacing gene (EAE) (Gannon et al., 1993), and cytotoxic necrotizing factor 1 and 2 (Blanco et al., 1996). Strains positive for toxin genes were checked for the presence of alpha intimin (Reid et al., 1999) and were serotyped (Orskov et al., 1977).

Nineteen isolates from 15 birds were tested for resistance against 16 antibiotics by IDEXX Veterinary Services (Sacramento, California, USA) on an automated system (VITEK, BioMérieux Vitek, Inc.) using MIC breakpoints established by the National Committee for Clinical Laboratory Standards (Aucoin, 2000). Isolates of E. coli, K. pneumoniae, Enterobacter cloacae, A. baumanii, Ps. aeruginosa, and Salmonella spp. were tested against the antibiotics amikacin, augmentin, ampicillin, carbenicillin, ceftazidime, ceftiofur, cephalothin, chloramphenicol, ciprofloxacin, enrofloxacin, gentamicin, piperacillin, tetracycline, ticarcillin, tobramycin, and tribrissen.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Gram-negative enteric bacteria were isolated from 86 of 89 birds (97%) (Table 2). A mean (±SD) of 2.64 (±1.34) different bacterial species was isolated per bird, with a maximum of six isolated from four different birds, two Western gulls (Larus occidentalis) and two pied-billed grebes (Podilymbus podiceps) from Cordelia. The most frequently isolated species of bacteria, E. coli, was cultured from 79 birds. The next five most frequently isolated bacteria, in decreasing order of frequency, were Proteus spp., K. pneumoniae, Citrobacter freundii, Escherichia fergusonii, and A. baumanii (Table 2). Salmonella enterica serotype Newport was isolated from one Western gull from Cordelia.

Mean (±SD) species richness values of bacteria found in gulls and common murres combined by rehabilitation centers were 2.79 (±1.03) at Cordelia (gulls, n=12; common murres, n=19) and 2.29 (±1.04) at Lynwood (gulls, n=27; common murres, n=6). Mean species richness of bacteria for gulls in both centers combined was 2.58 (±1.46), and for common murres it was 2.69 (±1.01). Based on a general linear-model ANOVA, these differences were not significant (df=62, P=0.09).

The EAE gene was present in six of 48 E. coli isolates tested from gulls and murres, and the alpha intimin gene was present in three isolates originally recovered from a common murre and Western gull from Cordelia and an unidentified species of gull from Lynwood. One type O57 was isolated from a herring gull (L. argentatus) in Arcata, and the other five E. coli isolates did not conform to known serotypes. The remaining two isolates with the EAE gene were recovered from a glaucous-winged gull (L. glaucescens) and a Western gull from Lynwood.

Antibiotic resistance was confirmed in 13 of 19 selected bacterial isolates (Table 3). All isolates with resistance to the tested antibiotics had resistance to multiple antibiotics (range, 3–8 antibiotics). There was no resistance to the 16 antibiotics in five of six isolates of E. coli, including the isolate typed as O57, and the Salmonella Newport isolate. Resistance to ampicillin was most prevalent (53%), followed by resistance to ceftiofur (37%), cephalothin (32%), and augmentin (26%) (Table 3). Sample sizes were too small to compare resistance between bird species or rehabilitation centers.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

The frequency of Salmonella spp. isolation in this study (1.1%; Table 2) was lower than that observed among seabirds elsewhere (Butterfield et al., 1983). In other studies birds were sampled at or near sites with greater potential for bacterial contamination, such as sewage outfalls or landfills (Kapperud and Rosef, 1983), or sampling was limited to gulls, which have been long implicated as carriers of Salmonella (Fenlon, 1983). The ready availability of human waste disposal sites fosters transmission of enteric bacteria to gulls (Fricker, 1984).

Salmonella Newport was previously reported in a gull (Larus sp.) (Fenlon, 1983), a common loon (Gavia immer) (White and Forrester, 1979), and in California sea lions (Zalophus californianus) (Smith et al., 2002). It is commonly isolated from human sewage and environmental samples (Fenlon, 1983) and is the third most common Salmonella spp. serotype isolated from humans in the United States (Zansky et al., 2002). During the period extending from 1997 to 2001, the number of confirmed human infections of Salmonella serotype Newport reported to the Centers for Disease Control and Prevention increased from 5% to 10% of all Salmonella spp. infections (Zansky et al., 2002).

Escherichia fergusonii and K. pneumoniae occurred significantly more often in common murres (Alcidae) than in gulls (Laridae) (Table 2). Common murres are colonial birds and, in rehabilitation centers, are caged with other common murres to decrease their stress level while in captivity (Stoskopf and Kennedy-Stoskopf, 1986). Based on the high prevalence of E. fergusonii and K. pneumoniae we observed in murres, we question if the practice of caging them together may facilitate an increased transmission of these potential pathogens.

Although most common murres samples were collected at one center (Cordelia) and most gull samples were collected from another center (Lynwood), there were no significant differences in species richness of bacteria isolated between the centers. There were differences in how rapidly the samples were shipped after collection. More gull samples were evaluated from Cultureswabs 48 hr after the sample was taken (67% of gull samples; 24% of murre samples). Many microorganisms readily maintain viability in Cultureswabs from 24 hr to 48 hr, but viability decreased after 48 hr (Smith and Jackson, 2001). In this study, recovery of Proteus spp. was significantly greater from samples inoculated more than 48 hr after sampling, which may indicate bacterial overgrowth in these samples and may explain the higher prevalence found in gulls compared to common murres (Table 2).

Of the six E. coli that carried the EAE gene, one was identified as a type O57, a strain found in swine (Fratamico et al., 2004). The remaining five could not be typed, possibly because the serotypes used for comparisons were primarily from humans and other mammals, and avian E. coli strains generally do not readily conform to types recognized in mammals (Gerlach, 1986). Of these five, three also carried the alpha intimin genes, indicating potential pathogenicity. The presence of both EAE and alpha intimin places them in a class of E. coli strains known as enteropathogenic E. coli (EPEC), which is linked to human illness (Nataro and Kaper, 1998). In addition to the normal fecal-oral route of transmission, EPEC also may be transmitted by dust particles (Nataro and Kaper, 1998).

Species we isolated that are known or suspected human pathogens include K. pneumoniae (Ko et al., 2002), Ps. aeruginosa (Hsueh et al., 2002), Aeromonas spp. (Altwegg and Geiss, 1989), E. fergusonii (Funke et al., 1993), Enterobacter spp. (Sanders and Sanders, 1997), A. baumanii (Bergogne-Bérézin and Towner, 1996), Proteus spp., Providencia spp., and Morganella morganii (O’Hara et al., 2000). Several of these, including Ps. aeruginosa, often are associated with nosocomial infections (Hsueh et al., 2002).

Ten of 16 antibiotics tested had at least one bacterial isolate with resistance to it (Table 3). Antibiotic resistance in bacteria has been found in other studies at rehabilitation centers (Smith et al., 2002; Ziegerer et al., 2002) as well as in studies of free-ranging birds (White and Forrester, 1979; Nascimento et al., 2003). Resistance to ampicillin (53%), a commonly used antibiotic, is consistent with results obtained from research conducted at other sites (Nascimento et al., 2003). Pseudomonas aeruginosa, K. pneumoniae, Acinetobacter spp., and E. coli have evolved in recent years into important nosocomial pathogens because of their multi-drug resistance (Jones, 2001). Among the isolates tested, Ps. aeruginosa was resistant to the most antibiotics.

Humans and seabirds come into close contact in wildlife rehabilitation centers. The transfer of zoonotic bacterial pathogens from bird to human, human to bird, and bird to bird represents risks for human and seabird health that can largely be prevented. Considering that many enteric bacteria are spread primarily via the fecal-oral route (Flammer, 1999), the transfer of enteric bacteria can effectively be reduced with proper hygiene, husbandry, and disinfection. The efficacy of simple measures, such as hand washing, is well documented (Pittet et al., 2000). Surfaces such as countertops and doorknobs, as well as objects used in patient care, such as blankets and sponges, are easily overlooked in cleaning and may harbor bacteria and should be disinfected regularly. In addition, housing birds individually may help to avoid transfer of novel pathogens to susceptible birds.

The pathogenicity of many of these bacteria to seabirds is poorly understood (Gerlach, 1986), although morbidity and mortality have been observed (Hall et al., 1977; Brand et al., 1988). Because an animal’s susceptibility to bacteria may be influenced by a number of factors, including the physiologic and psychological stresses involved in rehabilitation (Thornton et al., 1998), measures to minimize stress during the rehabilitation process should also be emphasized.

This study focused on captive birds in rehabilitation centers and on their caregivers, not on free-ranging seabirds. However, reducing transmission of pathogenic bacteria among seabirds in rehabilitation centers would reduce the potential risk to free-ranging seabirds whenever rehabilitated birds are released back into wild populations.

	ACKNOWLEDGMENTS

 
This project was supported by the California Department of Fish and Game’s Oil Spill Response Trust Fund through the Oiled Wildlife Care Network at the Wildlife Health Center, School of Veterinary Medicine, University of California, Davis, California. R. Golightly provided invaluable insight and guidance on the design of and logistics involved with the project, as well as feedback on previous drafts of the manuscript. This project would not have been possible without the help of the many rehabilitation-center staff and volunteers, particularly J. Huckabee, M. Ziccardi, S. Newman, C. Doucette, M. Bellizzi, J. Hobba, and J. Magis. Technical support was provided by J. Sajecki and K. Rogers, as well as the staff of Humboldt State University’s stockrooms: M. Cole, C. Hansen, R. Thompson, M. Early, A. Baker, and T. Jones. Statistical support was graciously provided by B. Bigg. S. Jang of the University of California at Davis generously provided advice on microbiologic matters and enabled serotyping of Salmonella spp. isolates. We thank C. DebRoy of Pennsylvania State University for the testing of, and many consultations on, our isolates of Escherichia coli.

	FOOTNOTES

 
² Current address: ABR, Inc., PO Box 249, Forest Grove, Oregon 97116, USA

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
ALTWEGG, M., AND H. K. GEISS. 1989. Aeromonas as a human pathogen. Critical Reviews in Microbiology 16: 253–286.[Medline]

ANONYMOUS. 1992. 20E Analytical profile index: Enterobacteriaceae and other Gram-negative bacteria. 10th Edition. BioMérieux Vitek, Hazelwood, Missouri, 327 pp.

AUCOIN, D. 2000. Target: The antimicrobial reference guide to effective treatment. 2nd Edition. North American Compendium, Inc., Port Huron, Michigan, 158 pp.

BANGERT, R. L., A. C. S. WARD, E. H. STAUBER, B. R. CHO, AND P. R. WIDDERS. 1988. A survey of the aerobic bacteria in the feces of captive raptors. Avian Diseases 32: 53–62.[Medline]

BERGOGNE-BEREZIN, E., AND K. J. TOWNER. 1996. Acinetobacter spp. as nosocomial pathogens: Microbiological, clinical, and epidemiological features. Clinical Microbiology Reviews 9: 148–165.[Medline]

BLANCO, M., J. E. BLANCO, J. BLANCO, M. P. ALONSO, C. BALSALOBRE, M. MOURINO, C. MADRID, AND A. JUAREZ. 1996. Polymerase chain reaction for detection of Escherichia coli strains producing cytotoxic necrotizing factor type 1 and type 2 (CNF-1 and CNF-2). Journal of Microbiological Methods 26: 95–101.

BRAND, C. J., R. M. WINDINGSTAD, L. M. SIEGFRIED, R. M. DUNCAN, AND R. M. COOK. 1988. Avian morbidity and mortality from botulism, aspergillosis, and salmonellosis at Jamaica Bay Wildlife Refuge, New York, USA. Colonial Waterbirds 11: 284–292.

BRITTINGHAM, M. C., S. A. TEMPLE, AND R. M. DUNCAN. 1988. A survey of the prevalence of selected bacteria in wild birds. Journal of Wildlife Diseases 24: 299–307.[Abstract]

BUTTERFIELD, J., J. C. COULSON, S. V. KEARSEY, P. MONAGHAN, J. H. MCCOY, AND G. E. SPAIN. 1983. The herring gull Larus argentatus as a carrier of Salmonella. Journal of Hygiene (London) 91: 429–436.

DEBACKER, V., L. HOLSBEEK, G. TAPIA, S. GOBERT, C. R. JOIRIS, T. JAUNIAUX, F. COIGNOUL, AND J. M. BOUQUEGNEAU. 1997. Ecotoxicological and pathological studies of common guillemots Uria aalge beached on the Belgian coast during six successive wintering periods (1989–90 to 1994–95). Diseases of Aquatic Organisms 29: 159–168.

EDWARDS, P. R., AND W. EWING. 1986. Salmonella. In Identification of Enterobacteriaceae. 4th Edition, P. R. Edwards and W. Ewing (eds.). Elsevier Press, New York, New York, pp. 181–340.

FENLON, D. R. 1983. A comparison of Salmonella serotypes found in the faeces of gulls feeding at a sewage works with serotypes present in the sewage. Journal of Hygiene, Cambridge 91: 47–52.

FLAMMER, K. 1999. Zoonoses acquired from birds. In Zoo & wild animal medicine: Current therapy. 4th Edition, M. E. Fowler (ed.). W. B. Saunders Co., Philadelphia, Pennsylvania, pp. 151–156.

FRATAMICO, P. M., L. K. BAGI, E. J. BUSH, AND B. T. SOLOW. 2004. Prevalence and characterization of Shiga toxin–producing Escherichia coli in swine feces recovered in the National Animal Health Monitoring System’s Swine 2000 study. Applied and Environmental Microbiology 70: 7173–7178.[Abstract/Free Full Text]

FRICKER, C. R. 1984. A note on Salmonella excretion in the black headed gull (Larus ribibundus) feeding at sewage treatment works. Journal of Applied Bacteriology 56: 499–502.[Medline]

FUNKE, G., A. HANY, AND M. ALTWEGG. 1993. Isolation of Escherichia fergusonii from four different sites in a patient with pancreatic carcinoma and cholangiosepsis. Journal of Clinical Microbiology 31: 2201–2203.[Abstract/Free Full Text]

GANNON, V. P. J., M. RASHED, R. K. KING, AND E. J. G. THOMAS. 1993. Detection and characterization of the EAE gene of Shiga-like toxin producing Escherichia coli using polymerase chain reaction. Journal of Clinical Microbiology 31: 1268–1274.[Abstract/Free Full Text]

GERLACH, H. 1986. Bacterial diseases. In Clinical avian medicine and surgery, G. J. Harrison and L. R. Harrison (eds.). W. B. Saunders Co., Philadelphia, Pennsylvania, pp. 434–453.

GLUNDER, G. 1981. Occurrence of Enterobacteriaceae in feces of granivorous passeriform birds. Avian Diseases 25: 195–198.[Medline]

HALL, R. F., D. G. WALDHALM, W. A. MEINERSHAGEN, AND D. A. DUBOSE. 1977. Isolation of Salmonella spp. from dead gulls (Larus californicus and Larus delawarensis) from an Idaho irrigation reservoir. Avian Diseases 21: 452–454.[Medline]

HINTZE, J. 2001. NCSS and PASS. Number Cruncher Statistical Systems software. Kaysville, Utah.

HSUEH, P., M. CHEN, C. SUN, W. CHEN, H. PAN, L. YANG, S. CHANG, S. HO, C. LEE, W. HSIEH, AND K. LUH. 2002. Antimicrobial drug resistance in pathogens causing nosocomial infections at a University Hospital in Taiwan, 1981–1999. Emerging Infectious Diseases 8: 63–68.[Medline]

JESSUP, D. A., AND F. A. LEIGHTON. 1996. Oil pollution and petroleum toxicity to wildlife. In Non-infectious diseases in wildlife, G. Hoff, A. Fair-brother, and L. Locke (eds.). Iowa State University Press, Ames, Iowa, pp. 141–156.

JONES, R. N. 2001. Resistance patterns among nosocomial pathogens. Chest 119: 397S–404S.[Medline]

KAPPERUD, G., AND O. ROSEF. 1983. Avian wildlife reservoir of Campylobacter fetus subsp. jejuni, Yersinia spp., and Salmonella spp. in Norway. Applied and Environmental Microbiology 45: 375–380.[Abstract/Free Full Text]

KO, W., D. L. PATTERSON, A. J. SAGNIMENI, D. S. HANSEN, A. VON GOTTBERG, S. MOHAPATRA, J. M. CASELLAS, H. GOOSSENS, L. MULAZIMOGLU, G. TRENHOLME, K. P. KLUGMAN, J. G. MCCORMACK, AND V. L. YU. 2002. Community-acquired Klebsiella pneumoniae bacteremia: Global differences in clinical patterns. Emerging Infectious Diseases 8: 160–166.[Medline]

NASCIMENTO, A. M. A., L. CURSINO, H. GONCALVES-DORNELAS, A. REIS, E. CHARTONE-SOUZA, AND M. Â. MARINI. 2003. Antibiotic-resistant Gram-negative bacteria in birds from the Brazilian Atlantic forest. Condor 105: 358–361.

NATARO, J. P., AND J. B. KAPER. 1998. Diarrheagenic Escherichia coli. Clinical Microbiological Review 11: 142–201.

O’HARA, C. M., F. W. BREENER, AND J. M. MILLER. 2000. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clinical Microbiology Reviews 13: 534–546.[Abstract/Free Full Text]

OJENIYI, B., P. AHRENS, AND A. MEYLING. 1994. Detection of fimbrial and toxin genes in Escherichia coli and their prevalence in piglets with diarrhea. The application of colony hybridization assay, polymerase chain reaction and phenotypic assays. Journal of Veterinary Medicine B 41: 49–59.[Medline]

ORSKOV, I., F. ORSKOV, B. JANN, AND K. JANN. 1977. Serology, chemistry and genetics of O and K antigens of Escherichia coli. Bacteriological Reviews 41: 667–710.[Free Full Text]

PITTET, D., S. HUGONNET, S. HARBARTH, P. MOUROUGA, V. SAUVAN, S. TOUVENEAU, AND T. V. PERNEGER. 2000. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 356: 1307–1312.[Medline]

REID, S. D., D. J. BETTING, AND T. S. WHITTAM. 1999. Molecular detection and identification of intimin alleles in pathogenic E. coli by multiplex PCR. Journal of Clinical Microbiology 37: 2719–2722.[Abstract/Free Full Text]

SANDERS, W., JR., AND C. C. SANDERS. 1997. Enterobacter spp.: Pathogens poised to flourish at the turn of the century. Clinical Microbiology Reviews 10: 220–241.[Abstract]

SIBLEY, D. A. 2000. The Sibley guide to birds. Alfred A. Knopf, New York, New York, 544 pp.

SMITH, E. G., AND T. L. JACKSON. 2001. Comparison of a new liquid Stuart aerobic swab transport system with two currently available systems. In Abstracts of the 101st Annual Meeting of the American Society for Microbiology. Orlando, Florida, Abstract C-53.

SMITH, W. A., J. A. MAZET, AND D. C. HIRSH. 2002. Salmonella in California wildlife species: Prevalence in rehabilitation centers and characterization of isolates. Journal of Zoo and Wildlife Medicine 33: 228–235.[Medline]

STEELE, C. M. 2003. Prevalences of zoonotic disease agents among seabirds in rehabilitation centers along the Pacific coast. Master’s Thesis, Humboldt State University, Arcata, California, 37 pp.

STOSKOPF, M. K., AND S. KENNEDY-STOSKOPF. 1986. Aquatic birds. In Zoo and wild animal medicine, M. E. Fowler (ed.). W. B. Saunders Company, Philadelphia, Pennsylvania, pp. 293–313.

THORNTON, S. M., S. NOLAN, AND F. M. D. GULLAND. 1998. 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. Journal of Zoo and Wildlife Medicine 29: 171–176.[Medline]

TOMASZ, A. 1994. Multiple-antibiotic-resistant pathogenic bacteria. New England Journal of Medicine 330: 1247–1251.[Free Full Text]

VELGE, P., A. CLOECKAERT, AND P. BARROW. 2005. Emergence of Salmonella epidemics: The problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes. Veterinary Research 36: 267–288.[Medline]

WHITE, F. H., AND D. J. FORRESTER. 1979. Antimicrobial resistant Salmonella spp. isolated from double-crested cormorants (Phalacrocorax auritus) and common loons (Gavia immer) in Florida. Journal of Wildlife Diseases 15: 235–237.[Abstract]

WILLIAMS, R. J., AND D. L. HEYMANN. 1998. Containment of antibiotic resistance. Science 279: 1153–1154.[Free Full Text]

WITHAM, P. K., C. T. YAMASHIRO, K. J. LIVAK, AND C. A. BATT. 1996. A PCR-based assay for the detection of Escherichia coli Shiga-like toxin gene in ground beef. Applied Environmental Microbiology 62: 1347–1353.[Abstract]

ZANSKY, S., B. WALLACE, D. SCHOONMAKER-BOPP, P. SMITH, F. RAMSEY, J. PAINTER, A. GUPTA, P. KALLURI, AND S. NOVIELLO. 2002. Outbreak of multi-drug resistant Salmonella Newport—United States, January–April 2002. Morbidity and Mortality Weekly Report 51: 545–548.

ZIEGERER, K., F. S. TSENG, AND M. A. POKRAS. 2002. Impact of antibiotic use in a wildlife rehabilitation clinic. Wildlife Rehabilitation 20: 69–83.

Received for publication 7 October 2004.

This article has been cited by other articles:

				A. Castinel, P. J. Duignan, W. E. Pomroy, N. Lopez-Villalobos, N. J. Gibbs, B. L. Chilvers, and I. S. Wilkinson NEONATAL MORTALITY IN NEW ZEALAND SEA LIONS (PHOCARCTOS HOOKERI) AT SANDY BAY, ENDERBY ISLAND, AUCKLAND ISLANDS FROM 1998 TO 2005 J. Wildl. Dis., July 1, 2007; 43(3): 461 - 474. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Steele, C. M. Articles by Botzler, R. G. Search for Related Content PubMed PubMed Citation Articles by Steele, C. M. Articles by Botzler, R. G.