# Enterococcus cecorum, un agent pathogène opportuniste des volailles : mieux le connaître pour une meilleure maîtrise en élevage

Rozenn Souillard, Francis Repoila, Jeanne Laurentie, Isabelle Kempf, Pascale Serror

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## To cite this version:

Rozenn Souillard, Francis Repoila, Jeanne Laurentie, Isabelle Kempf, Pascale Serror. Enterococcus cecorum, un agent pathogène opportuniste des volailles: mieux le connaître pour une meilleure maîtrise en élevage. INRAE Productions Animales, 2025, 10.20870/productions-animales.2025.38.1.8283. hal-05186598

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# Enterococcus cecorum, an opportunistic poultry pathogen: deeper understanding for better farm control

INRAE Prod. Anim.,
2025, 38 (1), 8283

Rozenn SOUILLARD<fnref n="1" />, Francis REPOILA<fnref n="2" />, Jeanne LAURENTIE<fnref n="1" />,<fnref n="2" />, Isabelle KEMPF<fnref n="1" />, Pascale SERROR<fnref n="2" />

E-mail: pascale.serror@inrae.fr

■ Enterococcus cecorum has become a major pathogen of poultry worldwide. This bacterium causes locomotor disorders that lead to mortality, increased use of antibiotics and economic losses, particularly in fast-growing broiler farms. This article summarises current epidemiological, zootechnical and basic knowledge with a view to improving disease control and prevention on farms.<fnref n="1" />

## Introduction

Diseases affecting poultry typically have multiple causes, including interactions between environmental conditions, genetics, husbandry practices, and the immune status or susceptibility of the animals. In the last five decades, broiler growth rate has increased fivefold between 29 and 35 days of age (Zuidhof et al., 2014). This rapid increase in body mass exerts mechanical stress on the birds' skeletal systems, facilitating invasion and colonisation of joints by opportunistic bacteria. Such bone infections are most often associated with *Staphylococcus aureus*, *Escherichia coli* or *Enterococcus cecorum* (Wideman, 2016; Wijesurendra et al., 2017). Over the last fifteen years, locomotor pathologies caused by *E. cecorum* have gradually reached a worrying level in broiler farms, affecting both animal health and welfare.

This review attempts to establish a link between current physiological and

molecular knowledge of *E. cecorum* and pathology on farms. It also looks at possible modes of transmission, detection methods and current treatments, as well as preventive zootechnical and biosecurity measures to contain the spread of this bacterium within and between farms. Lastly, it discusses strategies of research and development for controlling this pathogen on farms (Figure 1).

### 1. An opportunistic pathogen in broiler farming

#### 1.1 *E. cecorum*, a commensal bacterial agent of the intestinal tract of poultry

*E. cecorum* was first described in 1983 in Belgium, where it was isolated from the caecal contents of a dead chicken, under the name *Streptococcus cecorum* (Devriese et al., 1983). In 1989, it was

reclassified within the *Enterococcus* genus, which includes more than 75 species of ubiquitous bacteria found in the intestinal microbiota of terrestrial animals, including birds (Parks et al., 2020; Schwartzman et al., 2024).

*E. cecorum* is a Gram-positive cocci-shaped facultative anaerobic and non-spore-forming bacterium (Jung et al., 2018). It is a commensal bacterium in the intestinal microbiota of poultry, particularly chickens (Devriese et al., 1991b). It is also found in the intestinal tract of other animals such as pigs, cattle, horses, ducks and turkeys (Devriese et al., 1991a; Scupham et al., 2008). *E. cecorum* has the ability to form biofilms on inert surfaces (Grund et al., 2022; Laurentie et al., 2023a), and is an opportunistic agent causing locomotor disorders in poultry (Jung et al., 2018).

#### 1.2. Clinical signs

*E. cecorum* pathologies are primarily observed in chickens, although

<footnote n="1">¹ANSES, Laboratoire de Ploufragan-Plouzané-Niort, 22440, Ploufragan, France</footnote>

<footnote n="2">²Université Paris-Saclay, INRAE, AgroParisTech, Institut Micalis, 78350, Jouy-en-Josas, France</footnote>

<footnote n="1">1 This article was presented at the 15th Journées de la Recherche Avicole et Palmipèdes à Foie gras, 20-21 March 2024 in Tours (Souillard et al., 2024).</footnote>
<figure><img src="image_4.png" /><figcaption>**Figure 1.** Possible routes of contamination by *E. cecorum* and preventive measures.</figcaption></figure>

Routes of contamination and risk factors that may favour the presence of *E. cecorum* in broiler farms (left). Development and research strategies for controlling the pathogen (right). Scanning electron microscopy photo of *E. cecorum*, centre of figure (Photo: © T. Meylheuc and P. Serror, MIMA2-Micalis).

cases have also been reported in other poultry species, such as ducks and turkeys (Dolka *et al.*, 2017; Souillard *et al.*, 2022). The signs of the disease include reduced feed consumption, uneven growth, dehydration and increased mortality ranging from 7 to over 10% (Robbins *et al.*, 2012; Jung & Rautenschlein, 2014). An initial septicaemic phase results in lesions of pericarditis, fibrinous perihepatitis and splenomegaly (Jung & Rautenschlein, 2014). Locomotor disorders and lammess most often appear from three to four weeks of age (Stalker *et al.*, 2010; Jung & Rautenschlein, 2014; Borst *et al.*, 2017). The characteristic clinical sign of locomotor pathology in chickens infected with *E. cecorum* is birds sitting on their hocks (Jung *et al.*, 2018). Typical of enterococcal spondyloarthritis, this sign results from paralysis caused by the development of an inflammatory lesion in the free thoracic vertebra that compresses the spinal cord (Jung & Rautenschlein, 2014). Arthritis, synovitis

and necrosis of the femoral heads have also been observed (Stalker *et al.*, 2010; Borst *et al.*, 2012; Jung & Rautenschlein, 2014). Sepsis and bone lesions result in carcass condemnations at slaughter, with rates reaching up to 9.75%. (Jung & Rautenschlein, 2014). Diseases caused by *E. cecorum* thus result in significant economic losses on farms.

### ■ 1.3 History and epidemiology

*E. cecorum* emerged as a poultry pathogen in the early 2000s. The first cases were reported in Scotland (Wood *et al.*, 2002) and the Netherlands (Devriese *et al.*, 2002), then more widely in other European countries (Makrai *et al.*, 2011; Szeleszczuk *et al.*, 2013; AMCRA, 2021) and North America (Stalker *et al.*, 2010; Borst *et al.*, 2012). In France, there has been a noticeable increase in pathologies associated with *E. cecorum* in poultry over the last 15 years. Data from RNOEA, the French poultry epi-

demiological surveillance network, shows a significant emergence of this bacterium. In 2006, *Enterococcus* represented only 0.4% of all pathogens reported, whereas this proportion had risen to 12.9% by 2020 (Souillard *et al.*, 2022). Most diseases associated with *Enterococcus* were found in broilers. Furthermore, locomotor disorders, which were caused by *E. cecorum*, increased from 6% in 2017 to 14.8% in 2022. Among all transmitted pathogens in broilers reported to the network in 2022 for this production (n = 4 289), *E. cecorum* was second only to *E. coli*, accounting for 16.3% and 63.6%, respectively. This emergence can be explained in part by increased vigilance on the part of veterinarians in the field and improvements in laboratory diagnostic methods since the 2010s (Dolka *et al.*, 2017; Karunarathna *et al.*, 2017; Suyemoto *et al.*, 2017; Tessin *et al.*, 2024). However, *E. cecorum* pathology is now a major disease in broiler production worldwide.
## ■ 1.4. Pathogenesis

Clinical strains of *E. cecorum* appear to be adapted to colonise the gut from the first days of life, whereas commensal isolates do not appear to colonise the gut at a detectable level until the third week of life (Devriese *et al.*, 1991b; Borst *et al.*, 2017) (Figure 2). Indeed, Borst *et al.* (2017) showed that in farms with clinical episodes of *E. cecorum*, the bacterium was detected in the intestinal contents as early as the first week of life in 60% of animals. Conversely, *E. cecorum* was only detectable from the third week of life in 30% of animals in farms without an infectious episode (Borst *et al.*, 2017). According to the current model, the bacterium enters the bloodstream after colonising the intestine and crossing the intestinal mucosa, which explains why it is detected in organs such as the heart, liver and spleen during the early phase of infection (Figure 3). During this septic phase, *E. cecorum* is thought to spread to skeletal sites, including the thoracic vertebrae, femoral heads and joints, causing inflammation that leads to lameness and paralysis (Borst *et al.*, 2017). The resistance of clinical isolates of *E. cecorum* to high concentrations of lysozyme could give them an ecological advantage in the early colonisation of chicks (Manders *et al.*, 2024).

## ■ 1.5. Virulence or opportunism

Several molecular epidemiology studies have used pulsed-field electrophoresis (PFGE) to profile commensal and clinical isolates. Results from the USA, Canada, Belgium, the Netherlands, Germany and Poland have shown that commensal isolates are more diverse than clinical isolates, suggesting the evolution of specific clones with higher pathogenic potential (Kense & Landman, 2011; Boerlin et al, 2012; Borst et al., 2012; Robbins et al., 2012; Huang et al., 2023). Genomic analysis of approximately one hundred avian clinical isolates collected in France between 2007 and 2017 confirmed the clonal nature of avian clinical isolates, which are part of a phylogenetic clade found in the United States and Europe (Laurentie et al., 2023a). More recently, a phylogenetic study of about thirty

<figure><img src="image_5.png" /><figcaption>**Figure 2.** Temporal association between the presence of *E. cecorum* and clinical signs.</figcaption></figure>

*E. cecorum* colonises the intestine of healthy chickens at a detectable level from the third week. In clinically-affected flocks, *E. cecorum* is detected as early as the first week in the intestines of chicks.

<figure><img src="image_6.png" /><figcaption>**Figure 3.** Model of *E. cecorum* infection in chicks.</figcaption></figure>

Early colonisation of the intestine by *E. cecorum* (during the first week) allows the bacteria to cross the intestinal mucosa and spread throughout the body. *E. cecorum* then reaches the organs (liver, heart, kidney) and bone sites that cause the inflammatory lesions responsible for lameness and paralysis.

clinical strains from American farms, isolated from septicaemic animals during the first three weeks of life, seems to raise doubts concerning the clonal nature of the clinical isolates responsible for lameness by revealing a septicaemia-associated clone (Rhoads *et al.*, 2024). Mutations identified in seven

genes conserved across all strains appear to reflect host adaptation. At present, we cannot rule out the emergence of a new clone responsible for septicaemia. It would be interesting to assess the infectious potential of these strains and determine their ability to induce lameness.
Despite these advances, distinguishing between clinical and commensal strains remains a challenge. The identification of genes preferentially found in clinical isolates could help to distinguish them from non-clinical isolates (Borst et al., 2015; Huang et al., 2023; Laurentie et al., 2023a). For example, the capsule protects bacteria from phagocytosis and the prevalence of certain capsule genes in clinical isolates suggests a role in virulence (Huang et al., 2023; Laurentie et al., 2023a). Other genes more frequently found in the genomes of clinical isolates may contribute to virulence by encoding functions that are likely to provide alternative metabolic capacities for survival and reproduction within the host (Borst et al., 2015; Laurentie et al., 2023a; Rhoads et al., 2024). Currently, there is no infection model to distinguish clinical from non-clinical isolates or to study the impact of specific genes on virulence. The lethality test on embryonated chicken eggs has shown significant variations in mortality and lesions between isolates, but its relevance and reliability need to be consolidated due to disparities between studies (Borst et al., 2014; Ekesi et al., 2021; Dolka et al., 2022; Huang et al., 2023; Laurentie et al., 2023a). Oral inoculation in two-week-old birds was found to be more effective than intravenous inoculation or air sacs in reproducing spinal lesions, as evidenced by macroscopic and microscopic examination for spinal lesions (Martin et al., 2011). The team of A. Jung's team in Germany described an oral infection model in day-old chicks that was as close as possible to field conditions. Although this model reproduced the septic phase and late clinical signs in up to 20% of infected birds, only one of the two clinical isolates tested proved virulent (Schreier et al., 2021). Recently, an *in ovo* infection model at 18 days of embryonic development detected the bacterium in the femoral head and free thoracic vertebra in over 60% of birds (Arango et al., 2023). However, as the presence of *E. cecorum* was not tested in the intestinal microbiota, it is not possible to determine whether the bone infection resulted from the initial infection or from early intestinal

colonisation. Distinguishing between commensal and clinical isolates of *E. cecorum* remains challenging due to the lack of reliable molecular or phenotypic tools.

## ■ 1.6. Antibiotic resistance

Several North American and European studies show a high prevalence of tetracycline resistance (>70%) in clinical and non-clinical isolates of *E. cecorum*, while macrolide resistance (erythromycin, spiramycin and tylosin) is more common in clinical isolates (Jung et al., 2018; Laurentie et al., 2023b). Conversely, lincomycin resistance is more prevalent in isolates of non-clinical origin, which have more extensive antibiotic resistance profiles than clinical isolates (Boerlin et al., 2012; Borst et al., 2012; Jackson et al., 2015; Laurentie et al., 2023b). In France, 43.3% of isolates appear to be resistant to more than three classes of antibiotics, compared to 1.4% of isolates sensitive to the twenty or so molecules tested (Laurentie et al., 2023b). Nevertheless, the majority of isolates of clinical origin remain sensitive to the antimicrobials authorised for use in poultry. Similarly, it is reassuring to note that resistance to antimicrobials of critical importance in human medicine such as vancomycin, gentamicin, tigecycline, linezolid and daptomycin is not widespread in *E. cecorum* (Laurentie et al., 2023b) (Figure 4). These trends are validated by the distribution of resistance genes in genomes (Sharma et al., 2020; Laurentie et al., 2023b; Huang et al., 2024). Tetracycline resistance genes (*tet*(M) and *tet*(L)), macrolide resistance genes (*erm*(B)) and, to a lesser extent, bacitracin resistance genes (*bcr* operon) are the most common. Chromosomal mutations in the *gyr*A and *parC* genes explain more than 65% of quinolone resistance (Laurentie et al., 2023b) and a *pbp2* gene could contribute to ampicillin resistance (Huang et al., 2024). While no plasmids have been described in *E. cecorum*, the most common resistance genes are carried by complex genetic elements that have all the characteristics of mobile elements.

## ■ 1.7 Predisposing factors in animals

Animal sensitivity can influence the development of locomotor pathologies caused by *E. cecorum*. Increased body weight in poultry can lead to mechanical stresses on the locomotor system, leading to bone lesions with colonisation by various opportunistic bacteria (Wideman, 2016). Abnormal development of the locomotor system, such as early osteochondrosis lesions, could also predispose poultry to *E. cecorum* infections (Borst et al., 2017). However, no comparative studies on predisposition to infection as a function of lineage growth rate have been published thus far. A reduction in animal immunity or concomitant infections could also play a role in the development of the disease. The hypothesis of an alteration in the intestinal barrier favouring translocation of the bacteria has been raised in relation to intercurrent infections (*E. coli* or *Eimeria* parasites) or changes in the microbiota (Borst et al., 2017). However, co-infection of *E. cecorum* with a mixture of three *Eimeria* spp. species, including *Eimeria tenella*, has recently been associated with a decrease in the incidence of *E. cecorum* bacteraemia and the severity of spondyloarthritis (Borst et al., 2019). This result could be explained by a change in the intestinal microbiota, especially as a strain of *E. tenella* has been shown to contribute to the diversification of the caecal microbiota and the strengthening of the intestinal mucosa (Zhou et al., 2020). Heat stress, which causes changes in the composition of the intestinal microbiota, could also alter the integrity of the intestinal mucosa and promote *E. cecorum* translocation (Schreier et al., 2022b). While none of these factors is sufficient to trigger infection by *E. cecorum*, their combination could contribute to additive risk.

## 2. Which transmission route(s)?

### ■ 2.1. Vertical transmission

How poultry are contaminated and how *E. cecorum* is introduced into farms is still poorly understood. The
<figure><img src="image_7.png" /><figcaption>**Figure 4.** Distribution of antibiotic resistance in *E. cecorum* strains.</figcaption></figure>

Out of 208 strains of *E. cecorum*, 43.3% are resistant to more than three classes of antibiotics and a large majority are resistant to tetracyclines (>90%) and macrolides (>60%) (according to Laurentie *et al.*, 2023b).

possibility of vertical transmission has been studied, with inconclusive results. Indeed, genomic and metabolic patterns of *E. cecorum* from breeding birds and the clinical isolates from their offspring have not shown any correlation and the bacterium has not been found in the hatchery environment (Kense & Landman, 2011; Robbins *et al.*, 2012). Furthermore, experimental infection of breeder

chickens failed to detect the presence of the bacterium in eggs (Thofner & Christensen, 2016). Although vertical transmission of *Enterococcus* species has been demonstrated, this does not seem to involve *E. cecorum* (Shterzer *et al.*, 2023). Current research is limited, and further investigation is required to explore the possibility of vertical transmission of the bacterium in broiler farms.

## 2.2. Horizontal transmission

Horizontal transmission can result from direct contact between animals or indirectly, via contaminated equipment. Birds excrete *E. cecorum* in their droppings, and can thus become infected via the faecal-oral route (Borst *et al.*, 2017). In addition, the bacterium could be transmitted by inhalation of
contaminated dust from farm houses (Jung & Rautenschlein, 2014). The frequency of recurrences on farms, as reported in Belgium (Herdt et al., 2008) and France (Potier et al, 2024) suggests that there may be biological reservoirs such as darkling beetles, rodents, etc., or environmental reservoirs in areas of persistence difficult to clean and disinfect, such as feeding lines, ventilation and heating systems, as well as drinking pipettes, feeders and cracks in the floor (Luyckx et al., 2015; Tessin et al., 2024). A recent study shows a higher prevalence in summer (Dunnam et al., 2023). The bacterium survives on different substrates (litter, dust, plastic) at different temperatures and humidity levels, particularly on litter at 15°C and 32% humidity (Grund et al., 2021). In this study, the two clinical strains showed prolonged survival compared with the commensal strain. Although *E. cecorum* has not been isolated from the environment of farms affected by the bacterium (Robbins et al., 2012; Grund et al., 2022), the presence of DNA from the 16S gene of *E. cecorum* was detected in the drinking systems (Grund et al., 2022) and also after cleaning in the air admission circuit and the anteroom (Tessin et al., 2024). Further research is therefore needed to provide a better understanding of the *E. cecorum* contamination routes and of persistence areas on the farms.

# 3. Diagnosis and treatment

## ■ 3.1. Diagnosis of the disease

Lameness, with potential paralysis characterised by a "sitting on the hocks" position, increased mortality and arthritic lesions, necrosis of the femoral heads or spondyloarthritis are clinical signs suggestive of *E. cecorum* infection. Other bacterial agents, such as *E. coli*, can also cause these clinical signs and lesions in poultry. Bacteriological analysis is therefore necessary to confirm the diagnosis of *E. cecorum* infection. Isolation of *E. cecorum* from lesions is classically performed in the presence of CO₂ (5%) on a blood agar medium to which colistin and nalidixic acid may be added to inhibit the growth of

Gram-negative bacteria. Identification is currently carried out using MALDI-TOF (matrix-assisted laser desorption-ionisation time-of-flight) mass spectrometry, which is easier and more reliable than PCR identification (Karunarathna et al., 2017). This development has certainly contributed to the increase in the identification of *Enterococcus* and *E. cecorum* species in avian pathology since 2006 (Souillard et al., 2022).

## ■ 3.2. Treatment

Antibiotic susceptibility tests for *E. cecorum* are performed according to *E. faecalis* or *E. faecium* standards (Borst et al., 2012; Jackson et al., 2015; Dolka et al., 2016). Epidemiological cut-offs (ECOFFs) have been provisionally established for about twenty antibiotics in *E. cecorum* (Laurentie et al., 2023b). These require independent validation by other laboratories on a larger collection of strains before they can be adjusted and approved by the European Committee for Antimicrobial Susceptibility Testing (EUCAST). A better assessment of the antibiotic resistance of strains should help to improve the effectiveness of treatments and thus better control the use of antibiotics in livestock farming.

Currently, if an *E. cecorum* infection is diagnosed, early antibiotic treatment must be implemented rapidly to limit the spread of infection within a poultry flock. Treatment is ineffective on birds already exhibiting lesions and paralysis. If the choice of antibiotic is based on the results of the antibiogram, penicillin derivatives, in particular amoxicillin, are commonly used (Devriese et al., 2002; Herdt et al., 2008; Jung et al., 2018), sometimes requiring repeated treatments within a flock. However, due to the frequent recurrence of the disease on certain farms and its severity, antibiotic treatment during the first week of life has been suggested to control the disease, using amoxicillin and/or tylosin (Herdt et al., 2008) or lincospectin (Schreier et al., 2022a). In accordance with Regulation (EU) no 2019/6, which regulates the use of antibiotics in animals to reduce antibiotic resistance, the use of antimicrobial

medicinal products in a poultry flock for prophylactic purposes must remain exceptional "when the risk of infection or infectious disease is very high and the consequences are likely to be serious" (Article 107 of Regulation (EU) no 2019/6). It is essential to control the circumstances under which *E. cecorum* infections occur, in order to implement preventive measures based on farm management and sanitary measures.

# 4. Possible measures to implement on poultry farms to prevent the spread of infection

## ■ 4.1. Farm management to limit risk

Various zootechnical measures have been proposed to limit the risk of *E. cecorum* pathologies (Figure 1). Among these, adjusting lighting programmes to slow animal growth during the first few weeks of life could limit the impact of the disease (Jung et al., 2018). Insufficient darkness in buildings has been identified as a risk practice. Less than six hours of light cut-off at ten days of age would constitute an aggravating practice (Remiot et al., 2019). In addition, increasing skeletal strength and limiting mechanical stress on the musculoskeletal system could help reduce the risk of bone lesions and *E. cecorum* infections. Optimising early rearing conditions with good litter quality, sufficient air ventilation and temperature control could also limit the risk of disease (Remiot et al., 2019; Schreier et al., 2022b). Disease prevention also involves preventing digestive disorders and intercurrent infections that could promote infection, such as coccidiosis (Borst et al., 2017) or immunosuppressive diseases such as Gumboro disease (Sary et al., 2018). Finally, the frequency of recurrences suggests that *E. cecorum* persists in the environment, including farm buildings, even though the presence of viable bacteria has not been demonstrated due to the lack of a selective culture medium (Tessin et al., 2024). The presence of *E. cecorum* in watering systems is still a matter of debate (Grund et al., 2022; Tessin et al., 2024). It has also been shown that inadequate cleaning
and disinfection could be a risk factor (Remiot *et al.*, 2019) and that *E. cecorum* DNA could be detected after the cleaning/disinfection of houses, in the anteroom, pipes and air circuits (Tessin *et al.*, 2024). The potential environmental persistence of *E. cecorum*, evidenced by detection even after cleaning and disinfection, underscores the need to reinforce biosecurity (compliance with the anteroom and protocols for changing clothes and washing hands, disinfection of equipment) and hygiene practices (disinfection of houses and water pipes) to better prevent the disease.

An alternative way of preventing the proliferation of undesirable bacteria on farms is to use mixtures of bacteria to form a protective biofilm on buildings before chick arrival (Guéneau *et al.*, 2022a) (Figure 5). The application of a mixture of *Bacillus* spp. and *Pediococcus* spp. strains could limit the development of enterobacteria and enterococci (Guéneau *et al.*, 2022b). This measure could contribute to better environmental hygiene management for birds. The rotation of disinfection agents (bacteria) and bacterial biofilms between two flocks should reduce the risk of emergence of resistant strains.

## ■ 4.2. Strategies for prevention

Vaccination of poultry could be a valuable tool for controlling *E. cecorum* diseases on farms (Figure 1). However, there is currently no commercial vaccine available, although research is ongoing. In particular, it has been shown that vaccination of breeding hens with a polyvalent inactivated vaccine against *E. cecorum* did not prevent the disease in chicks (Borst *et al.*, 2019). Serological ELISA methods have yet to be developed to assess serological responses to *E. cecorum* infection and vaccination in breeding hens and chicks (Jung & Rautenschlein, 2020; Silberborth *et al.*, 2024).

Modern poultry farming practices disrupt the natural vertical transmission of chicken microbiota by preventing contact between hens and chicks. As a result, the animals acquire a poorly diverse and ill-defined microbiota from

<figure><img src="image_8.png" /><figcaption>**Figure 5.** Research strategies to prevent the proliferation of *E. cecorum* in the poultry houses and the chick environment.</figcaption></figure>

In addition to vaccinating breeding flocks against *E. cecorum*, two biological control methods need to be developed: bacterial consortia and the use of bacteriophage cocktails. These two methods are not mutually exclusive. They can be used to treat the chick's environment, eggs and poultry houses. They can also be used to protect chicks from intestinal colonisation by the pathogen via a "barrier effect" of the bacterial consortia and/or the elimination of virulent bacteriophages.

their environment. This early disruption of colonisation can lead to an imbalance in the microbiota, or dysbiosis, and/or a lack of maturation of the intestinal mucosa and immune system, which can affect production performance and resistance to pathogens (Rubio, 2019; Rychlik, 2020). The colonisation of the initial microbiota is essential for inducing a good immune response (Rodrigues *et al.*, 2021). While the role of the intestinal microbiota in the infectious potential of *E. cecorum* has not been established, the intestinal detection of clinical isolates in the first two weeks and the efficacy of early treatment with lincospectin in preventing infection suggest a window of opportunity for intervention to promote the ecological barrier of the microbiota and the mucosal barrier (Hankel *et al.*, 2021; Schreier *et al.*, 2022a) (Figure 5). Among the various strategies considered in livestock farming to stimulate the ecological barrier of the intestinal microbiota, the use of probiotic strains such as *Bacillus* for their antagonistic activity is one of the oldest (Cutting, 2011). Various *Bacillus* strains have been isolated for their inhibitory activity against *E. cecorum* (Medina Fernández *et al.*, 2019; Penaloza-Vazquez *et al.*, 2019; Sandvang *et al.*, 2024). Their efficacy depends on the probiotic strains and the *E. cecorum* isolate targeted. Further work is needed to study their

efficacy in vivo and characterise the inhibiting molecules. Understanding the role of the microbiota in the pathogenesis of *E. cecorum* is a prerequisite for developing new preventive strategies that could be based on the transfer of healthy microbiota or the implantation of consortia of avian probiotic or commensal bacteria.

Cocktails of bacteriophages are also available in some European countries and North America as food supplements or probiotics (Bacteriophage. news., n.d.; Gigante & Atterbury, 2019; Abd-El Wahab *et al.*, 2023). Phages lyse bacteria with the advantage of having a limited host spectrum, reducing collateral effects in the targeted microbiota. Their use in cocktails also reduces the risk of resistant strains emerging. To date, virulent phage specific to *E. cecorum* have not been described, but this approach is worth considering because of the genetic similarity of clinical strains. Administration of these phages during the first two weeks of rearing could help prevent or delay early colonisation of infectious isolates. However, whatever alternative methods are considered, it is essential to assess their environmental consequences on human and animal health, environmental microbial ecology and the risk of emergence of resistant strains.
## Conclusion

Like many opportunistic pathogens, the virulence of *E. cecorum* is multifactorial. Its relatively recent emergence suggests a direct correlation with changes in rearing practices, which may have led to the selection of a clone capable of infecting fast-growing broilers chickens. It is essential to improve our zootechnical, epidemiological and fundamental knowledge of the physiology and pathogenesis of *E. cecorum* in order to implement effective measures for the prevention and control of the disease. To effectively manage this pathogen, it is essential to develop rapid diagnostic methods capable of distinguishing clinical from non-clinical strains, thus clarifying routes of transmission and farm contamination.

The development of a robust animal model reproducing at least the early phase of infection is necessary to understand the interaction of *E. cecorum* with the microbiota and its host, using global approaches (metagenomics, metabolomics and proteomics). This knowledge should enable preventive strategies to be defined to limit the use of antibiotics and the associated selection pressure, as well as reducing the clinical impact, animal suffering and economic losses on farms.

## Authors' contributions

All the authors took part in writing the article, coordinated and supervised by Pascale Serror.

## Acknowledgements

J. Laurentie received a grant from ANSES and INRAE. The work behind this synthesis was supported by INRAE's GISA metaprogramme (CecoType project), the French Ministry of Agriculture (DGAL) through the Ecoantibio2 programme number 2018-180 and INRAE's Microbiology and Food Chain Department (Mica).

This article was first translated with [www.DeepL.com/Translator](http://www.DeepL.com/Translator). The authors are grateful to Sean P. Kennedy for English language editing.

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## Abstract

In less than 20 years, *Enterococcus cecorum* has become one of the major pathogens in broiler farms, distributed worldwide. This opportunistic bacterium is a commensal of the poultry gut, responsible for locomotor disorders that can lead to flock mortality. *E. cecorum* is a cause of poor animal welfare, increased use of antibiotics and economic losses. This review aims to establish a link between *E. cecorum* infections and the current physiological and molecular knowledge of the bacterium. Genomic analyses indicate that clinical isolates of *E. cecorum* are adapted to intestinal colonisation of chicks from the very first days of life. Conversely, commensal strains colonise the intestine later, at the earliest during the third week of life. The contamination routes of farms and the factors that could favour *E. cecorum* infection are most likely multiple: vertical and horizontal transmissions, zootechnical parameters, biosecurity practices and animal susceptibility. This review also presents a number of ideas under development to improve the control of *E. cecorum* on farms and prevent infections.
# Résumé

## Enterococcus cecorum, un agent pathogène opportuniste des volailles : mieux le connaître pour une meilleure maîtrise en élevage

En moins de 20 ans, Enterococcus cecorum est devenu l'un des agents pathogènes majeurs dans les élevages de poulets de chair et de répartition mondiale. Cette bactérie opportuniste, commensale de l'intestin des volailles, est responsable de pathologies locomotrices pouvant entraîner de la mortalité dans les élevages. Elle est à l'origine d'une dégradation du bien-être animal, d'une utilisation accrue d'antibiotiques et de pertes écolonomiques. Cette revue tente d'établir un lien entre les pathologies à E. cecorum et les connaissances actuelles physiologiques et moléculaires de la bactérie. Les analyses génomiques indiquent notamment que les isolats cliniques de E. cecorum seraient adaptés à la colonisation intestinale du poussin dès les premiers jours de vie. À l'inverse, les souches commensales coloniseraient l'intestin plus tardivement, au plus tôt durant la troisième semaine de vie. Les voies de contamination des élevages et les facteurs de risque qui pourraient favoriser l'infection à E. cecorum sont probablement multiples : transmission verticale et horizontale, paramètres zootechniques, pratiques de biosécurité et sensibilité des animaux. Cette revue présente également quelques pistes en cours de développement pour mieux maîtriser E. cecorum au sein des élevages et prévenir les infections.

SOUILLARD, R., REPOILA, F., LAURENTIE, J., KEMPF, I., & SERROR. P. (2025). *Enterococcus cecorum*, an opportunistic poultry pathogen: deeper understanding for better farm control. *INRAE Productions Animales*, 38(1), 8283.

https://doi.org/10.20870/productions-animales.2025.38.1.8283

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