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Enterococcus gallinarum

Enterococcus gallinarum is a Gram-positive, facultative anaerobic coccus belonging to the genus Enterococcus within the phylum Bacillota (formerly Firmicutes), previously classified as a group D Streptococcus based on Lancefield grouping and later reclassified through molecular and genetic analyses.^[1] It typically appears as ovoid cells arranged in pairs or short chains, with some strains exhibiting motility due to peritrichous flagella, and is catalase-negative.^[2] This bacterium is ubiquitous in nature, commonly inhabiting the gastrointestinal tracts of humans and animals, as well as environmental reservoirs including soil, plants, water, and various foods such as dairy products and meats.^[3]^[1] As a commensal member of the gut microbiota, E. gallinarum primarily acts as an opportunistic pathogen, causing rare but significant infections, particularly in elderly or immunocompromised patients with underlying conditions such as biliary tract disease or systemic lupus erythematosus (SLE).^[4]^[5] Common clinical manifestations include urinary tract infections, wound infections, and bacteremia, with the latter often polymicrobial and originating from the biliary tract in approximately 77% of cases; overall mortality from E. gallinarum bacteremia remains low at around 13% crude and 1.9% attributable.^[4] It has been implicated in gut translocation contributing to SLE progression and is an emerging concern in nosocomial settings due to its potential for multidrug resistance.^[6] A defining feature of E. gallinarum is its intrinsic low-level resistance to vancomycin, mediated by the vanC gene cluster, which distinguishes it from more virulent species like E. faecalis and E. faecium and complicates treatment in healthcare-associated infections.^[2] Microbiologically, it grows optimally at 35–37°C, tolerates 6.5% sodium chloride, and hydrolyzes esculin in the presence of 40% bile salts, producing black colonies on selective media like bile esculin agar; it also grows on non-selective media such as blood agar (forming small, greyish, non-hemolytic colonies) and MacConkey agar (pink to red colonies).^[3] These traits, combined with its environmental adaptability, underscore its role as a resilient pathobiont in both clinical and ecological contexts.^[7]

Taxonomy and Classification

Etymology and History

The name Enterococcus gallinarum combines the genus Enterococcus, derived from the Greek words enteron (intestine) and kokkos (berry or coccus), referring to its coccal shape and intestinal habitat, with the specific epithet gallinarum, the genitive plural form of the Latin gallina (hen or chicken), alluding to its initial discovery in poultry.^[8]^[7] Enterococcus gallinarum was first isolated in 1978 by Barnes et al. from the intestines of young chicks as part of a study examining the impact of dietary bacitracin on fecal streptococci populations. These isolates were initially grouped among group D streptococci due to their serological reactivity. In 1982, Bridge and Sneath formally described the species as Streptococcus gallinarum sp. nov. based on numerical taxonomic analysis of 136 physiological and biochemical tests, which distinguished it from other streptococcal species through traits such as slow growth on selective media, pink pigmentation on thallous acetate-tetrazolium agar, and a guanine-plus-cytosine content of 37.4 mol%. The species was reclassified as Enterococcus gallinarum comb. nov. in 1984 by Collins et al., who used DNA-DNA hybridization studies to demonstrate its genetic separation from other streptococci (with homology values below 30%) and close relatedness to the enterococcal lineage, including a guanine-plus-cytosine content of 39-40 mol%. This reclassification aligned with the revival of the genus Enterococcus by Schleifer and Kilpper-Bälz, emphasizing its ecological and physiological similarities to Enterococcus faecalis and Enterococcus faecium.^[9] Early characterization also highlighted its intrinsic low-level resistance to vancomycin as a distinguishing feature from susceptible enterococci like E. faecalis.30006-0/fulltext) Prior to formal delineation, isolates were frequently misidentified as E. faecalis owing to comparable Gram-positive coccal morphology, facultative anaerobism, and group D antigen sharing.^[10]

Phylogenetic Position

Enterococcus gallinarum is a Gram-positive bacterium classified within the domain Bacteria, phylum Bacillota, class Bacilli, order Lactobacillales, family Enterococcaceae, and genus Enterococcus. This taxonomic placement reflects its position among lactic acid bacteria adapted to diverse environments, particularly as a commensal in animal gastrointestinal tracts.^[11] Phylogenetically, E. gallinarum belongs to the E. gallinarum-E. casseliflavus group, a clade of closely related enterococcal species distinguished by their motile characteristics and ecological niches. Analysis of 16S rRNA gene sequences reveals that E. gallinarum shares nearly identical sequences with E. casseliflavus and E. flavescens, differing only at a few nucleotide positions (e.g., position 287: cytosine in E. gallinarum versus adenine in the others), resulting in >99% similarity. In contrast, similarity to more distant species like E. faecalis is approximately 97%, and to E. faecium around 98.5%, underscoring its distinct yet related position within the genus.^[12] Evolutionarily, E. gallinarum traces its origins to commensal gut microbiota of early terrestrial animals, emerging approximately 425–500 million years ago during the Paleozoic era amid animal terrestrialization. This adaptation involved speciation driven by host carbohydrate availability and environmental pressures in gastrointestinal ecosystems. Mobile genetic elements, including plasmids and transposons, have significantly influenced its phylogenetic position by facilitating horizontal gene transfer, genome expansion, and acquisition of traits like antibiotic resistance, contributing to the diversification of the enterococcal clade.^[13]

Biological Characteristics

Morphology and Physiology

Enterococcus gallinarum is a Gram-positive coccus with an ovoid shape, typically measuring 0.5 to 1.5 μm in diameter.^[14] Cells are arranged in pairs or short chains and are motile due to peritrichous flagella.^[15]^[2] As a facultative anaerobe, E. gallinarum can grow under both aerobic and anaerobic conditions, with microaerophilic preferences in certain environments.^[16] Optimal growth occurs at temperatures of 35–37°C and pH levels of 6.5–7.5, though it tolerates broader ranges including 10–45°C and pH up to 9.6.^[17]^[15] The species is chemoorganotrophic and homofermentative, fermenting glucose, lactose, and mannitol to produce lactate via the Embden-Meyerhof-Parnas pathway, but fermentation of sorbitol is variable across strains.^[14]^[15] It produces acetoin, yet the Voges-Proskauer test is variable, often negative in many isolates.^[15] Growth characteristics include tolerance to 6.5% NaCl and the ability to hydrolyze esculin in the presence of 40% bile salts.^[2] Colonies on agar are typically small, gray, and non-hemolytic, though pigmented strains may display yellow coloration, a trait shared with related species in the E. casseliflavus group.^[18]^[2]

Genomic Features

The genome of Enterococcus gallinarum consists of a single circular chromosome with a size ranging from approximately 3.3 to 3.7 Mb across sequenced strains, a GC content of about 40%, and an estimated 3,200 to 3,500 protein-coding genes.^[19]^[20] This compact genome structure supports the bacterium's adaptation as a commensal and opportunistic pathogen, with annotation revealing genes involved in core metabolic pathways, stress responses, and environmental sensing typical of enterococci.^[21] A hallmark genetic feature is the intrinsic vanC gene cluster, chromosomally located and comprising five genes: vanC-1, vanXYC, vanT, vanRC, and vanSC. This cluster encodes enzymes that modify peptidoglycan precursors by incorporating D-alanine-D-serine instead of D-alanine-D-alanine, conferring low-level resistance to vancomycin (MIC 4–32 μg/mL) while maintaining susceptibility to teicoplanin.^[22]^[23] Additionally, some strains harbor the esp (enterococcal surface protein) gene, which encodes a surface adhesin that promotes initial attachment and biofilm formation on abiotic surfaces, enhancing persistence in host environments.^[24] E. gallinarum genomes frequently contain mobile genetic elements that facilitate horizontal gene transfer, including plasmids typically 20–50 kb in size that carry additional antimicrobial resistance determinants such as those for aminoglycosides or tetracyclines.^[25] Prophages, such as the temperate phage phiEG37k, integrate into the chromosome and may contribute to genetic diversity through lysogenic conversion, while transposons enable the mobilization of resistance cassettes within and across strains.^[26]^[27] These elements underscore the species' propensity for acquiring adaptive traits via conjugation and transduction in polymicrobial settings.^[28]

Ecology and Habitat

Natural Distribution

Enterococcus gallinarum is commonly isolated from various environmental sources, including soil, water, and plant material. It has been recovered from both tropical and temperate soils, as well as surface waters and sewage-polluted seawater and freshwater systems. The bacterium is associated with plants such as forage crops, buds, blossoms, and grasses, and it has been detected in sewage and animal feces beyond poultry sources. These environmental niches highlight its adaptability to diverse non-host settings, often linked to fecal contamination.^[7] In animal reservoirs, E. gallinarum is prevalent in the intestines of avian species, particularly poultry like chickens and turkeys, where it was first isolated in 1978 from the intestine of a young chick.^[29] It is also detected at lower rates in pigs, cattle, and wild birds such as gulls and buzzards, as well as occasionally in pets like dogs and cats. These reservoirs contribute to its dissemination through agricultural and natural ecosystems.^[7] The bacterium exhibits a ubiquitous global distribution, with higher isolation rates in temperate regions and agricultural areas due to livestock exposure and environmental contamination. It has been reported across Europe (e.g., Portugal, Spain, Italy), Asia (e.g., China, Japan), South America (e.g., Brazil), North Africa (e.g., Tunisia), and other regions, reflecting its widespread presence in farming and natural habitats.^[7]

Host Interactions

Enterococcus gallinarum primarily serves as a commensal bacterium in the gastrointestinal tracts of birds and humans, where it contributes to the normal microbial flora without typically causing harm. In avian hosts, particularly poultry such as chickens and pigeons, it constitutes a notable portion of the intestinal enterococci, with isolation rates reaching up to 9% in healthy reared birds and detection in approximately 32% of fecal samples from various bird species.^[30]^[7] In humans, it is a transient member of the gut microbiota, representing a small proportion of the fecal enterococcal population and exhibiting low carriage rates (e.g., 0.6–9%) in healthy adults, often persisting at low densities of 10⁴–10⁶ bacteria per gram of intestinal content.^[31]^[32] Colonization by E. gallinarum relies on robust mechanisms that enable survival and adherence within the host intestine. It demonstrates high tolerance to intestinal stresses, including low pH levels down to 4.0 and bile salt concentrations up to 0.3-0.5%, allowing it to withstand the acidic stomach and bile-rich small intestine during transit and establishment.^[33]^[2] These adaptations underscore its role as an opportunist that thrives in the dynamic gut ecosystem alongside other microbiota. The zoonotic potential of E. gallinarum highlights its transmission from avian reservoirs to humans, primarily through contaminated poultry products or environmental exposure in agricultural settings. Studies have identified the bacterium in chicken meat and farm environments, with higher carriage rates observed among poultry farm workers compared to the general population, suggesting occupational exposure as a key vector for cross-species transfer.^[34]^[35] This transmission pathway positions poultry as a significant reservoir, potentially disseminating antimicrobial-resistant strains to human hosts via food chains or direct contact.^[36]

Pathogenicity and Clinical Significance

Associated Infections

Enterococcus gallinarum primarily causes nosocomial infections, with bacteremia being the most common clinical manifestation.^[4] It is one of the more common species among non-E. faecalis and non-E. faecium enterococci causing bloodstream infections.^[37] Other associated infections include rare cases of endocarditis, typically affecting native heart valves in elderly patients, intra-abdominal infections often originating from biliary sources, wound infections in surgical settings, and meningitis reported primarily in immunocompromised individuals or following neurosurgical procedures.^[38]^[4]^[39] Epidemiologically, non-E. faecalis/non-E. faecium VRE species, including E. gallinarum, represent 1-2% of all vancomycin-resistant enterococcal (VRE) bloodstream infections, with higher incidence observed in hospitalized patients undergoing abdominal surgery or those with indwelling medical devices.^[37] Risk factors include prolonged hospitalization, prior broad-spectrum antibiotic exposure, immunosuppression (such as in transplant recipients or those with malignancies), advanced age over 65 years, and gastrointestinal conditions facilitating translocation from the gut microbiota.^[2]^[40] Outbreaks have been linked to contaminated medical equipment in healthcare facilities, underscoring its opportunistic role in institutional settings.^[41] In specific cases, E. gallinarum bacteremia often presents polymicrobially, with biliary tract involvement in up to 77% of episodes, and is associated with post-surgical complications.^[4] Motile enterococci like E. gallinarum account for less than 5% of enterococcal bacteremia, and endocarditis cases due to E. gallinarum are exceedingly rare, typically occurring without evident predisposing cardiac abnormalities.^[38] Meningitis is documented in isolated case reports, predominantly in patients with cerebrospinal fluid shunts or recent craniotomies.^[39] Mortality rates for E. gallinarum bacteremia are around 10-13% crude.^[37]^[4]

Virulence Mechanisms

Enterococcus gallinarum employs several virulence mechanisms that facilitate its transition from a commensal gut bacterium to an opportunistic pathogen. Biofilm formation occurs on indwelling medical devices such as catheters, allowing persistence in hostile environments and resistance to antimicrobials and host immunity, though specific mediators like esp and ebp are better characterized in other enterococci.^[42] In addition to biofilm production, E. gallinarum may produce extracellular enzymes that aid in tissue invasion and damage. Gelatinase, a metalloprotease, degrades host extracellular matrix components like collagen and gelatin, facilitating bacterial spread into deeper tissues. Serine protease contributes to proteolysis of host proteins, enhancing invasiveness. Some strains exhibit cytolytic activity, lysing host cells including erythrocytes and leukocytes, promoting tissue destruction and nutrient release.^[43]^[43]^[44] Host evasion is further supported by intrinsic low-level resistance to vancomycin conferred by the chromosomal vanC gene cluster, which modifies peptidoglycan precursors to reduce antibiotic binding. Quorum sensing systems contribute to the coordination of virulence factors in response to population density. Polysaccharide structures on the cell surface inhibit phagocytosis by host immune cells, such as macrophages. Adhesion to endothelial cells, mediated by surface proteins, promotes endovascular colonization and is implicated in conditions like endocarditis.^[22]^[45]^[2]

Diagnosis and Management

Identification Methods

Enterococcus gallinarum is isolated from clinical or research samples using selective culture media that exploit its ability to tolerate bile and hydrolyze esculin. On bile esculin azide agar, the organism grows as small, black colonies within 24-48 hours at 37°C, resulting from the precipitation of esculetin with ferric ions following esculin hydrolysis. This medium effectively selects for enterococci while inhibiting many other gram-positive bacteria.^[46] Phenotypic characteristics aid initial differentiation during culture. E. gallinarum strains are typically motile, observable via motility medium or hanging drop preparations, and produce no or minimal yellow pigment on agar plates, unlike the pigmented E. casseliflavus. Growth occurs under aerobic or anaerobic conditions, in 6.5% NaCl, and at temperatures from 10°C to 45°C, confirming its enterococcal affiliation.^[15]^[4] Biochemical testing refines identification through carbohydrate fermentation and enzymatic profiles. A key diagnostic feature is positive fermentation of L-arabinose, producing acid without gas. Additionally, E. gallinarum acidifies methyl-α-D-glucopyranoside, a test that distinguishes it from E. faecium, which is negative. Hippurate hydrolysis is typically negative, further differentiating it from species like E. faecalis. These tests, often performed using commercial systems like API 20 Strep, achieve reliable species-level identification when combined in a stepwise key.^[15]^[47]^[15] Molecular methods provide definitive confirmation, particularly for vancomycin-resistant isolates. Polymerase chain reaction (PCR) targeting the chromosomally located vanC-1 gene, intrinsic to E. gallinarum, amplifies a specific 796-bp product using primers such as VanC-1F (CGGAGCCGAGATGTGGTTTT) and VanC-1R (GGGTCACCTCGTCGTAGAAT), enabling differentiation from other enterococci like those harboring vanC-2. Multiplex PCR assays can simultaneously detect multiple vancomycin resistance genes for broader screening.^[48]^[48]^[49] Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) offers rapid, accurate species-level identification directly from colonies or blood cultures, with success rates exceeding 90% for enterococci when using updated databases. It outperforms traditional biochemical panels in speed and discriminatory power, identifying E. gallinarum based on unique protein spectral profiles.^[50] For challenging cases, such as non-motile variants, 16S rRNA gene sequencing remains the gold standard, providing over 99% sequence identity to reference E. gallinarum strains and resolving ambiguities in phenotypic methods. This approach has confirmed species identity in atypical isolates previously misidentified by biochemical tests.^[12]

Treatment Strategies and Resistance

Enterococcus gallinarum exhibits intrinsic low-level resistance to vancomycin, primarily mediated by the chromosomal vanC gene cluster, which results in minimum inhibitory concentrations (MICs) typically ranging from 4 to 16 μg/mL for vancomycin and lower levels for teicoplanin.^[51]^[52] This resistance is constitutive and distinguishes E. gallinarum from high-level vancomycin-resistant enterococci (VRE) mediated by acquired vanA or vanB genes. Despite this, the species generally remains susceptible to ampicillin, with MICs often below 4 μg/mL, as well as to linezolid and daptomycin, which maintain reliable activity against most isolates.^[53]^[37] Treatment of E. gallinarum infections prioritizes beta-lactam antibiotics, such as ampicillin or penicillin, as first-line agents for susceptible strains due to their favorable pharmacodynamics and low toxicity profile.^[53] In severe cases like endocarditis, combination therapy with ampicillin and gentamicin is recommended to achieve bactericidal synergy, as demonstrated by in vitro studies showing enhanced killing against E. gallinarum.^[54] For vancomycin-nonsusceptible isolates or when beta-lactams are contraindicated, linezolid or daptomycin serve as effective alternatives, with clinical outcomes improved in bloodstream infections treated with these agents.^[37] Removal of infected foreign devices, such as central lines or prosthetic materials, is essential to eradicate persistent sources of infection and prevent relapse.^[55] While E. gallinarum rarely acquires high-level glycopeptide resistance through vanA or vanB gene clusters, isolated reports document such events, particularly in hospital settings, leading to multidrug-resistant phenotypes.^[56]^[57] These acquisitions underscore the need for vigilant monitoring of E. gallinarum in intensive care units (ICUs), where surveillance for VRE and infection control measures can mitigate dissemination.^[58]

Recent Research Developments

Autoimmunity Links

Recent research has identified Enterococcus gallinarum as a translocating gut pathobiont capable of escaping the intestinal barrier and contributing to autoimmune responses, particularly in systemic lupus erythematosus (SLE) models.^[59] In a 2025 study using lupus-prone murine gnotobiotic models, E. gallinarum was observed to migrate from the gut to extraintestinal sites including the liver and spleen, where it elicited systemic immune dysregulation.^[59] This translocation was associated with the induction of interferon-γ–producing T helper 17 (TH17) cells and IgG3 anti-RNA autoantibodies, mirroring key features of SLE pathology in both murine models and human patients.^[59] The underlying mechanisms involve E. gallinarum's molecular components activating innate immune pathways. Specifically, bacterial RNA from E. gallinarum stimulates Toll-like receptor 8 (TLR8) on monocytes, driving TH17 cell differentiation and promoting the production of anti-RNA autoantibodies.^[59] This activation fosters a pro-inflammatory environment that exacerbates systemic inflammation, including renal autoimmune damage, akin to SLE manifestations.^[59] Unlike typical commensal behavior in healthy hosts, this pathobiont's translocation in genetically susceptible individuals amplifies autoreactive responses, highlighting its role in immune dysregulation rather than direct infection.^[59] These findings carry significant implications for autoimmune disease management. Elevated IgG3 antibodies against E. gallinarum RNA have been detected in SLE patients and correlate with disease activity, positioning them as potential biomarkers for monitoring flares.^[59] Furthermore, targeted antibiotic treatment to suppress E. gallinarum colonization reduced autoantibody levels, TH17 responses, and clinical symptoms in lupus-prone mouse models, as shown in a 2018 study, suggesting a therapeutic avenue through microbiota modulation.^[60]

Emerging Resistance Patterns

Recent reports indicate an uptick in high-level vancomycin resistance among Enterococcus gallinarum isolates, primarily driven by the acquisition of the vanA gene cluster on mobile genetic elements such as plasmids. A notable example is a 2013 clinical isolate from Canada, reported in 2015, which exhibited a minimum inhibitory concentration (MIC) of ≥256 μg/mL for vancomycin and 48 μg/mL for teicoplanin, alongside both vanA and vanB operons in addition to the intrinsic vanC.^[61] This acquired resistance contrasts with the species' typical low-level intrinsic resistance mediated by vanC, highlighting the potential for horizontal gene transfer to exacerbate clinical challenges.^[32] Co-resistance to aminoglycosides, particularly high-level gentamicin resistance, has been observed in approximately 10-15% of E. gallinarum isolates, often linked to enzymes like AAC(6')-Ie-APH(2'')-Ia that disrupt synergistic bactericidal effects with cell wall agents.^[62] Global surveillance data reveal a rise in such multidrug-resistant strains post-2010, with notable increases in Asia, including high vanA prevalence in China, Japan, and Korea due to nosocomial transmission in hospitals.^[63] This trend is partly attributed to antibiotic overuse in poultry farming, where E. gallinarum colonization rates in broiler flocks exceed 15%, facilitating zoonotic spillover through contaminated meat.^[64] European data on vancomycin resistance primarily reflect trends in other enterococci species like E. faecium, with limited species-specific surveillance for high-level resistance in E. gallinarum as of 2022.^[65] Looking ahead, the emergence of E. gallinarum strains with combined vanA and aminoglycoside resistance raises concerns for pan-resistant variants that could undermine standard therapies like ampicillin or linezolid.^[63] Enhanced antimicrobial stewardship programs, including targeted surveillance in high-risk settings like intensive care units and poultry operations, are essential to curb dissemination and preserve treatment options.^[66]

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PCR products were detected in 63 of the 100 clinical isolates. The restriction fragment length patterns were consistent with vanA for 10 strains, vanB for 30 ...
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As Enterococcus gallinarum was isolated from 2 blood cultures, gentamicin was switched to ampicillin. Surgery was not considered because of the patient's ...
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In this study, we describe a clinical isolate of Enterococcus gallinarum exhibiting high-level resistance to vancomycin and teicoplanin.Missing: characteristics | Show results with:characteristics
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Acquired vanA- and vanB-mediated glycopeptide resistance has been well described in Enterococcus faecalis and Enterococcus faecium, and high-level ...
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Feb 5, 2025 · Enterococcus gallinarum is a translocating gut microbe that can escape the intestine and stimulate systemic autoimmune responses in mice.
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Characterization of an Enterococcus gallinarum Isolate Carrying a ...
Jun 18, 2015 · In this study, we characterized a clinical isolate of E. gallinarum containing both vanA and vanB operons conferring vancomycin resistance.Missing: etymology | Show results with:etymology
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Enterococcus gallinarum and Enterococcus casseliflavus/flavescens are enterococci intrinsically resistant to vancomycin belonging to the E. gallinarum group ...
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### Summary of Enterococcus gallinarum Resistance Data (2021)
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