Identification of human enteric pathogens in gull feces at Southwestern Lake Michigan bathing beaches

Kinzelman, Julie; McLellan, Sandra L.; Amick, Ashley AmickA.; Preedit, Justine; Scopel, Caitlin O.; Olapade, Ola OlapadeO.; Gradus, Steve GradusS.; Singh, Ajmer; Sedmak, Gerald SedmakG.

doi:10.1139/w08-096

Cited by 57 publications

(50 citation statements)

References 59 publications

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“…represent a smaller fraction of the population, at ϳ10% (43). Gull feces can also contain some human pathogens, such as Campylobacter and Salmonella (46). Compared to human sewage, the presence of gull fecal pollution poses a comparatively lessened risk of illness, yet can lead to an excessive number of beach closings (10).…”

Section: Discussionmentioning

confidence: 99%

Distribution and Differential Survival of Traditional and Alternative Indicators of Fecal Pollution at Freshwater Beaches

Cloutier

McLellan

2017

Appl Environ Microbiol

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Alternative indicators have been developed that can be used to identify host sources of fecal pollution, yet little is known about how their distribution and fate compare to traditional indicators. Escherichia coli and enterococci were widely distributed at the six beaches studied and were detected in almost 95% of water samples (n ϭ 422) and 100% of sand samples (n ϭ 400). Berm sand contained the largest amount of E. coli (P Ͻ 0.01), whereas levels of enterococci were highest in the backshore (P Ͻ 0.01). E. coli and enterococci were the lowest in water, using a weight-to-volume comparison. The gull-associated Catellicoccus marimammalium (Gull2) marker was found in over 80% of water samples, regardless of E. coli levels, and in 25% of sand samples. Human-associated Bacteroides (HB) and Lachnospiraceae (Lachno2) were detected in only 2.4% of water samples collected under baseflow and post-rain conditions but produced a robust signal after a combined sewage overflow, despite low E. coli concentrations. Burdens of E. coli and enterococci in water and sand were disproportionately high in relation to alternative indicators when comparing environmental samples to source material. In microcosm studies, Gull2, HB, and Lachno2 quantitative PCR (qPCR) signals were reduced twice as quickly as those from E. coli and enterococci and approximately 20% faster than signals from culturable E. coli. High concentrations of alternative indicators in source material illustrated their high sensitivity for the identification of fecal sources; however, differential survival and the potential for long-term persistence of traditional fecal indicators complicate the use of alternative indicator data to account for the levels of E. coli and enterococci in environmental samples. IMPORTANCE E. coli and enterococci are general indicators of fecal pollution and may persist in beach sand, making their use problematic for many applications. This study demonstrates that gull fecal pollution is widespread at Great Lakes beaches, whereas human and ruminant contamination is evident only after major rain events. An exploration of sand as a reservoir for indicators found that E. coli was ubiquitous, while gull host markers were detected in only 25% of samples. In situ sand beach microcosms provided decay rate constants for E. coli and enterococci relative to alternative indicators, which establish comparative benchmarks that would be helpful to distinguish recent from past pollution. Overall, alternative indicators are useful for identifying sources and assessing potentially high health risk contamination events; however, beach managers should be cautious in attempting to directly link their detection to the levels of E. coli or enterococci.KEYWORDS beaches, water quality, human-associated indicators, gull-associated indicators, qPCR F ecal contamination of recreational waters can be a serious threat to public health. Due to the vast diversity of fecal-borne human pathogens, the USEPA has recommended the use of fecal indicator bacteria (FIB),...

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Section: Discussionmentioning

confidence: 99%

Distribution and Differential Survival of Traditional and Alternative Indicators of Fecal Pollution at Freshwater Beaches

Cloutier

McLellan

2017

Appl Environ Microbiol

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“…In particular, human pathogens, such as Campylobacter, Salmonella, and Listeria, have been isolated from ringbilled gull (Laurus delawarensis) fecal material (16,27). Further, high levels of fecal indicator organisms deposited locally (e.g., where water quality samples are collected) by gulls may mask contamination from more serious regional sources, such as sewage overflows released into estuaries and rivers (24).…”

Section: Discussionmentioning

confidence: 99%

“…Other studies have shown that gull feces contain a large and variable population containing both E. coli and enterococci (10 5 to 10 9 CFU g Ϫ1 and 10 4 to 10 8 CFU g Ϫ1 , respectively) and could contribute these indicator organisms to beach water in the Great Lakes (11). Gull feces also have been shown to contain a variety of fecal bacteria pathogenic to humans, such as Salmonella, Campylobacter, Aeromonas, and Yersinia (16,20,21,27). Certain Bacteroides and Prevotella spp.…”

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confidence: 99%

Bacteroidales Diversity in Ring-Billed Gulls ( Laurus delawarensis ) Residing at Lake Michigan Beaches

Jeter

McDermott

Bower

et al. 2009

Appl Environ Microbiol

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This study investigated the occurrence and diversity of Bacteroidales fecal bacteria in gulls residing in the Great Lakes region. Members of this bacterial order have been widely employed as human and bovine host-specific markers of fecal pollution; however, few studies have focused on gulls, which can be a major source of fecal indicator bacteria and pathogens at beaches. We found a low but consistent occurrence of Bacteroidales in gulls at five beaches in three different counties spanning the Wisconsin shoreline of Lake Michigan. The percentages of gulls positive for Bacteroidales were 4 to 8% at beaches in the southern part of the state and 8 to 50% at beaches in the north. Sequencing of 931 clones from seven gull Bacteroidales 16S rRNA gene libraries revealed a large amount of diversity in both individual and pooled gull fecal samples. Two libraries constructed from pooled gull fecal samples (n ‫؍‬ 5 and n ‫؍‬ 6) did not have a greater richness of sequences than individual samples, suggesting that even within a single gull diversity is high and an extensive sequencing effort is needed to characterize the populations. Estimates of the numbers of operational taxonomic units (OTUs) for the libraries obtained using different similarity levels revealed a large amount of microdiveristy with a limited number of OTUs at the 95% similarity level. Gull sequences were clustered by the beach from which they were collected, suggesting that there were geographic effects on the distribution of Bacteriodales. More than 53% of the 16S rRNA gene sequences from gulls at the southern beaches were associated with the family Porphyromonadaceae, primarily the genus Parabacteroides, whereas sequences from gulls at the northern beaches were comprised of Bacteroidaceae and Prevotellaceae sequences. Comparison of gull sequences with sequences from goose, canine, raccoon, and sewage sources revealed distinct clusters of closely related gull sequences; however, these sequences were widely dispersed across a dendrogram that included all other sources, including previously characterized gull Bacteroidales from other studies, suggesting that geographic influence or simply sample representation plays a greater role in the observed population structure than strictly the host gut environment.

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“…Studies of the pharynx, cloaca, or feces of great or black cormorants have found positivity rates ranging from 47.8% to 74.4% for these birds (69,70). Plesiomonas has also been recovered from 3.9% to 7.4% of ring-billed and herring gull feces on bathing beaches located on southwestern Lake Michigan (71). Other avian species reported to yield P. shigelloides include whooper swan, black stork, goldeneyes, herons, and penguins (72,73,74).…”

Section: Invertebrate and Vertebrate Hostsmentioning

confidence: 99%

Plesiomonas shigelloides Revisited

Janda¹,

2016

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SUMMARYAfter many years in the familyVibrionaceae, the genusPlesiomonas, represented by a single species,P. shigelloides, currently resides in the familyEnterobacteriaceae, although its most appropriate phylogenetic position may yet to be determined. Common environmental reservoirs for plesiomonads include freshwater ecosystems and estuaries and inhabitants of these aquatic environs. Long suspected as being an etiologic agent of bacterial gastroenteritis, convincing evidence supporting this conclusion has accumulated over the past 2 decades in the form of a series of foodborne outbreaks solely or partially attributable toP. shigelloides. The prevalence ofP. shigelloidesenteritis varies considerably, with higher rates reported from Southeast Asia and Africa and lower numbers from North America and Europe. Reasons for these differences may include hygiene conditions, dietary habits, regional occupations, or other unknown factors. Other human illnesses caused byP. shigelloidesinclude septicemia and central nervous system disease, eye infections, and a variety of miscellaneous ailments. For years, recognizable virulence factors potentially associated withP. shigelloidespathogenicity were lacking; however, several good candidates now have been reported, including a cytotoxic hemolysin, iron acquisition systems, and lipopolysaccharide. WhileP. shigelloidesis easy to identify biochemically, it is often overlooked in stool samples due to its smaller colony size or relatively low prevalence in gastrointestinal samples. However, one FDA-approved PCR-based culture-independent diagnostic test system to detect multiple enteropathogens (FilmArray) includesP. shigelloideson its panel. Plesiomonads produce β-lactamases but are typically susceptible to many first-line antimicrobial agents, including quinolones and carbapenems.

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Identification of human enteric pathogens in gull feces at Southwestern Lake Michigan bathing beaches

Cited by 57 publications

References 59 publications

Distribution and Differential Survival of Traditional and Alternative Indicators of Fecal Pollution at Freshwater Beaches

Distribution and Differential Survival of Traditional and Alternative Indicators of Fecal Pollution at Freshwater Beaches

Bacteroidales Diversity in Ring-Billed Gulls ( Laurus delawarensis ) Residing at Lake Michigan Beaches

Plesiomonas shigelloides Revisited

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