Carbapenemase in poultry: blaNDM-5 found in a broiler farm
Carbapenemase in poultry production systems has now been documented in the United Arab Emirates for the first time. Screening 77 cecal samples from broiler farmhouses and slaughterhouses found three confirmed producers. One of them was a Klebsiella pneumoniae ST11 strain carrying blaNDM-5, a gene whose mobile backbone matches a human clinical isolate from India at more than 98 percent nucleotide identity.
Why carbapenemase in poultry matters for One Health
Carbapenems are the antibiotics clinicians reach for when everything else has failed. Carbapenem-resistant Enterobacterales sit on the World Health Organization critical-priority list, because they spread quickly and leave few treatment options behind.
For years these organisms were treated as a hospital problem. That framing has been eroding across antimicrobial resistance surveillance. Carbapenemase genes including blaNDM, blaVIM and blaOXA-48-like have been turning up in food-producing animals and in agricultural environments. When a resistance determinant crosses from a clinical setting into a broiler house, the question stops being whether it can happen and becomes how widely it already has.
Data from poultry production in the Gulf region were essentially absent before this survey. Carbapenemase in poultry is not a European or Asian story alone. This study went looking for it in a national industry with two large commercial producers, and found it.
How the survey was designed
| Design element | Specification |
|---|---|
| Sampling period | June 2023 to April 2024, an eleven-month campaign |
| Setting | Broiler farmhouses and slaughterhouses in the United Arab Emirates |
| Sample set | 77 poultry-associated samples: 59 cecal droppings plus 18 cecal content specimens |
| Farm distribution | 18 poultry houses across 6 farms at the first company, 9 poultry houses across 3 farms at the second |
| Screening | MacConkey agar supplemented with meropenem |
| Confirmation | Modified carbapenem inactivation method using a 10 microgram meropenem disk |
| Susceptibility testing | Kirby-Bauer disk diffusion with CLSI breakpoints and Escherichia coli ATCC 25922 quality control, following M100-S30 |
| Sequencing | Illumina NovaSeq, paired-end 150 bp reads |
| Typing | Multilocus sequence typing and capsular polysaccharide locus typing |
| Comparative analysis | 538 K. pneumoniae ST11 genomes carrying blaNDM-5 plus 42 Metapseudomonas otitidis genomes |
| Phylogenetic method | Core genome single nucleotide polymorphisms, recombination removed, maximum-likelihood trees |
The selective step is what makes the design work. Growing on meropenem-supplemented MacConkey agar concentrates the organisms that can survive a carbapenem. The modified carbapenem inactivation method then separates true enzyme producers from the imposters. Reduced carbapenem susceptibility can also come from porin loss or efflux pump overexpression, and neither of those is a carbapenemase. The method used here suspends a loopful of overnight culture in broth, incubates it with a meropenem disk for four hours, then transfers the disk onto a lawn of a standard E. coli indicator strain. If a carbapenemase is present, the disk is inactivated and the inhibition zone collapses.
What the screening found: 3 of 77 samples
Three isolates, 3.9 percent of the 77 samples screened, were confirmed as carbapenemase producers. All three came from a single cecal dropping sampled directly inside a farmhouse. That is a striking concentration for a survey of this size.
Two of the three, 268MR1 and 377MR1, met the criteria for multidrug resistance, meaning resistance to at least three antimicrobial classes. One was a Klebsiella pneumoniae and two were Metapseudomonas otitidis.
| Isolate | Species | Sequence type and capsule | Carbapenemase gene | Other beta-lactamases | Plasmid replicons detected |
|---|---|---|---|---|---|
| 377MR1 | Klebsiella pneumoniae | ST11, KL105 | blaNDM-5 | blaSHV-182, blaTEM-1B, blaOXA-1 | IncFIB(K), IncFII(K), IncR, Col(MG828) |
| 201MP1 | Metapseudomonas otitidis | Not reported | blaPOM-1 | blaLCR-1 | None detected |
| 268MR1 | Metapseudomonas otitidis | Not reported | blaPOM-1 | blaLCR-1 | None detected |
All three isolates were resistant to meropenem and imipenem. All three were also resistant to ampicillin, amoxicillin-clavulanic acid, cefoperazone, ceftriaxone, cefoxitin, ciprofloxacin and nalidixic acid. Only 377MR1 also carried resistance to tetracycline, gentamicin and amikacin. Only 268MR1 of the two otitidis isolates was additionally resistant to chloramphenicol.
The Klebsiella pneumoniae isolate and blaNDM-5
Isolate 377MR1 is the one that carries public health weight. blaNDM-5 is an acquired metallo-beta-lactamase, and acquiring it is a different event from being born with it. Its presence explains the meropenem and imipenem resistance directly.
The strain did not stop there. It carried three further beta-lactamase genes in blaSHV-182, blaTEM-1B and blaOXA-1. Its resistome spanned most of the antibiotic classes a poultry veterinarian could reach for: aminoglycoside-modifying enzymes aac(6′)-Ib10, aph(3′)-Ia, rmtB and aadA2, quinolone resistance determinants qnrB1, oqxA and oqxB, the macrolide resistance gene mph(A), fosfomycin resistance in fosA6, phenicol resistance in catB3, sulfonamide resistance in sul1, tetracycline resistance in tet(A), and trimethoprim resistance in dfrA12 and dfrA14.
Four plasmid replicons were detected: IncFIB(K), IncFII(K), IncR and Col(MG828). That matters, because plasmids are the vehicles that move resistance genes between bacteria. A chromosomal resistance gene stays with its host lineage. A plasmid-borne gene can travel.
Virulence genes were present in the same strain too, including a complete yersiniabactin siderophore cluster of ybtS, ybtX, ybtQ, ybtP, ybtA, irp2, irp1, ybtU, ybtT, ybtE and fyuA, the enterobactin system genes fepC, entB and entA, the outer membrane protein ompA, and a full set of E. coli common pilus adhesin genes. Multidrug resistance and a virulence arsenal in one poultry-associated isolate is the combination that turns a surveillance finding into a concern.
The two Metapseudomonas otitidis isolates and blaPOM-1
The second species tells a different story, and the difference matters for how the risk is read.
Both otitidis isolates carried blaPOM-1, which is intrinsic to the species rather than acquired. An organism that is naturally resistant to carbapenems was never susceptible to them in the first place, so its detection is less alarming than the detection of an acquired gene in a pathogen. Neither isolate carried a plasmid replicon, which supports the conclusion that their resistance determinants sit on the chromosome rather than on a movable element.
That does not make them harmless. Both carried blaLCR-1 alongside qnrVC1, sul1, aadA10 and tmexD4. Both carry a type VI secretion system from the HSI-I cluster, a pyoverdine siderophore system, and a full flagellar motility system. Toxin injection systems and iron-scavenging machinery support environmental persistence and competition against other bacteria.
Where the blaNDM-5 cassette came from
The most consequential finding is architectural. In isolate 377MR1, blaNDM-5 sits inside a gene cassette arranged as IS30, blaNDM-5, bleMBL, PRAI and DsbD, flanked upstream by an IS6 element and downstream by an IS91-like transposase.
Every element of that structure is a mobility signal. Insertion sequences and transposases are the machinery that lifts a resistance gene out of one genome and drops it into another. Alignment against a human ST11 isolate recovered in India in 2019 showed near-complete synteny and more than 98 percent nucleotide identity across the shared region.
Identical architecture, not similar architecture. That finding does not prove the poultry isolate came from a patient, or that a patient got it from poultry. What it does show is that both strains carry the same mobile genetic backbone, the kind of structure that makes a gene internationally portable. The two otitidis isolates show the opposite pattern: their chromosomal blaPOM-1 regions are almost entirely conserved and highly syntenic with each other, consistent with vertical inheritance rather than recent horizontal transfer.
What the global phylogeny shows
Placing the poultry isolate against 538 publicly available K. pneumoniae ST11 genomes carrying blaNDM-5 puts it inside a well-supported clade of globally distributed carbapenem-resistant strains. The geographic split is lopsided.
| Region | blaNDM-5 positive ST11 isolates | Share of the 538 genomes |
|---|---|---|
| Asia | 316 | 58.7 percent |
| Europe | 162 | 30.1 percent |
| China, a subset of the Asian total | 271 | 50.4 percent |
South America, North America, Africa and Oceania contributed the remainder, which the study reports only as smaller contributions. Capsular typing across the same population found substantial diversity, with KL24, KL64, KL47, KL15 and KL105 all present. KL105 is one of the dominant capsular types among blaNDM-5-positive ST11 isolates, and isolate 377MR1 belongs to it. The coexistence of multiple capsule types inside one sequence type points to frequent capsular switching, which helps a lineage evade immunity and adapt to new environments.
The 44-genome analysis of M. otitidis placed the two poultry isolates in a tight lineage alongside a human isolate from the United States recovered in 2016. That is a sub-lineage distributed across two continents and two host types.
The counter-intuitive findings
Three results deserve more attention than the headline prevalence figure.
The first is that the resistance signal was concentrated in one sample. Three confirmed producers out of 77 samples would normally suggest scattered contamination. Three from a single cecal dropping sampled inside one farmhouse suggests something else: a focal population rather than a diffuse background. With this sample size the study cannot tell which explanation is right, and that uncertainty is itself the finding worth carrying forward.
The second is that the two species pose very different risks, and the raw count hides it. Two of the three isolates carry an intrinsic, chromosomally encoded carbapenemase. Detecting those is not evidence of a resistance gene spreading. The acquired blaNDM-5 in the Klebsiella isolate is the finding with clinical weight, and it is one isolate rather than three.
The third is the direction of the genomic evidence. The poultry isolate does not sit on a distant branch of the tree, newly diverged and locally contained. It sits inside the dominant global clade, with a cassette matching a clinical isolate from another continent. A surveillance framing that treats farm findings as separate from hospital findings is not supported by this tree.
What this means for poultry producers and buyers
Read the numbers before the alarm. A 3.9 percent isolation rate from 77 samples, taken from two companies in one country, is an early warning signal rather than a prevalence estimate. The study says so itself. The right response is neither dismissal nor panic, but a change in what gets tested and why.
The practical implication is about surveillance design. Meropenem-supplemented MacConkey agar followed by mCIM confirmation is the workflow that generated this result, and it is reproducible in a routine laboratory. A producer or buyer who runs only general hygiene indicators will never see this class of organism, because carbapenem-resistant bacteria are not outcompeting anything in a plate count.
The second implication is about the sample itself. All three isolates came from cecal material collected inside a farmhouse, not from carcass swabs at the abattoir. Gut content screening reaches the reservoir directly. Post-harvest sampling catches what survives processing, which is a different and later question.
Practical recommendations
- Screen gut content, not only carcass surfaces, if the goal is to detect carbapenemase in poultry. All three isolates here came from cecal material.
- Confirm phenotype before drawing conclusions. Reduced carbapenem susceptibility also arises from porin loss and efflux, neither of which is a carbapenemase.
- Sequence every confirmed producer. The risk difference between an acquired blaNDM-5 and an intrinsic blaPOM-1 is the difference between a one-isolate signal and a species property.
- Track plasmid replicons alongside the resistance gene. A chromosomal gene stays in its lineage; IncFIB(K), IncFII(K), IncR and Col(MG828) do not.
- Include capsular typing in genomic surveillance. KL105 recurs across distinct carbapenemases and works as an epidemiological marker.
- Sample more than one cecal dropping per house. Three positives in one sample could be a focal population or coincidence, and this dataset cannot separate them.
- Treat worker, animal and environmental sampling as separate streams. Without them, cross-host transmission cannot be inferred in either direction.
- Report genomic links to clinical isolates without overclaiming direction. Shared architecture is evidence of mobility, not proof of transmission.
Limitations
The study is explicit about its own boundaries. The sample size was small and the number of carbapenemase-producing isolates was low, which reflects the exploratory design and precludes any robust estimate of prevalence across the national poultry industry. Sampling was restricted to broiler farms belonging to two commercial companies, so the findings do not generalize to poultry production across the country.
Contamination control is the second gap. Standard aseptic procedures were followed throughout, but formal controls such as field blanks and sequencing audits were not systematically included, so low-level contamination cannot be completely ruled out. On the phenotypic side, the modified carbapenem inactivation method ran without certified carbapenemase-positive and carbapenemase-negative reference strains as external quality controls. Susceptibility testing used Escherichia coli ATCC 25922 as the only quality control organism, without the additional strains recommended for non-fermenting Gram-negative bacteria.
Whole genome sequencing used short reads, which limits complete resolution of plasmids and complex resistance regions. That constraint prevents a definitive determination of the genetic location and mobility of some resistance determinants. Long-read sequencing, S1-PFGE and conjugation assays would settle what this dataset can only suggest.
The final limitation is the one that bounds every One Health claim here. Farm workers, poultry and environmental reservoirs were not sampled concurrently. The comparative genomics show close evolutionary relatedness between the poultry isolates and previously reported human clinical strains, and relatedness is all they show. Direct cross-host transmission, transmission pathways and plasmid dissemination cannot be inferred from this design, and the authors frame the work as an early warning signal rather than a prevalence estimate.
Bottom line
Carbapenemase in poultry is now documented in the United Arab Emirates. Three of 77 cecal samples from broiler farmhouses and slaughterhouses yielded confirmed carbapenemase producers, all from one farmhouse sample. Two were Metapseudomonas otitidis carrying the intrinsic blaPOM-1, which is largely a species property. The consequential finding is a single Klebsiella pneumoniae ST11 KL105 isolate carrying blaNDM-5 on a cassette whose architecture matches a human clinical isolate from India at more than 98 percent nucleotide identity, with four plasmid replicons and a broad resistome in the same strain. The sample is too small for a prevalence figure. It is large enough to change what a poultry surveillance program should be looking for.
FAQ
What is carbapenemase in poultry?
A carbapenemase is an enzyme that destroys carbapenem antibiotics, the last-line drugs used when other options fail. In poultry the term covers bacteria recovered from farm or slaughterhouse samples that produce such an enzyme. This survey found three confirmed producers among 77 cecal samples, including a Klebsiella pneumoniae strain carrying the acquired gene blaNDM-5.
How common is carbapenem resistance in poultry farms?
This survey cannot answer that. Three confirmed producers out of 77 samples is a 3.9 percent isolation rate in one country, from two commercial companies and their associated farms. The authors describe the work as an exploratory early warning signal rather than a prevalence estimate, and state directly that the sample size precludes a robust industry-wide figure.
Which bacteria carried the carbapenemase genes in this study?
Two species. One isolate was Klebsiella pneumoniae ST11 KL105 carrying blaNDM-5, which is an acquired metallo-beta-lactamase. The other two were Metapseudomonas otitidis carrying blaPOM-1, which is intrinsic to the species. Only the Klebsiella isolate carried an acquired carbapenemase gene, and only it carried plasmid replicons.
What is blaNDM-5 and why does it matter?
blaNDM-5 is an acquired gene encoding a class B metallo-beta-lactamase, which destroys carbapenems and explains meropenem and imipenem resistance directly. It matters because the gene sits on a mobile cassette. In this study its genetic environment matched a human ST11 isolate from India at over 98 percent nucleotide identity, showing a shared mobile backbone.
How was carbapenemase production confirmed?
Samples grew on MacConkey agar supplemented with meropenem. Confirmed producers were identified with the modified carbapenem inactivation method: a loopful of overnight culture was suspended in broth, incubated with a 10 microgram meropenem disk for four hours, then the disk was placed on a lawn of Escherichia coli ATCC 25922. A collapsed inhibition zone indicates an active carbapenemase.
Where did the blaNDM-5 gene in the poultry isolate come from?
The study cannot say, and it does not claim to. What it shows is that the gene cassette in the poultry isolate, IS30, blaNDM-5, bleMBL, PRAI and DsbD flanked by an IS6 element and an IS91-like transposase, is nearly identical to one from a human ST11 isolate recovered in India in 2019. Shared architecture indicates mobility, not transmission direction.
Is carbapenemase in poultry a risk to people?
Direct transmission was not demonstrated. Farm workers, poultry and environmental reservoirs were not sampled at the same time, so the study cannot infer transmission pathways. What it does establish is close evolutionary relatedness between a poultry-associated isolate and previously reported human clinical strains, plus a plasmid-borne acquired carbapenemase gene in a multidrug-resistant, virulent Klebsiella strain.
Why does the Klebsiella isolate matter more than the other two?
Because the resistance is acquired rather than innate. Metapseudomonas otitidis carries blaPOM-1 as an intrinsic chromosomal gene, so it was never susceptible to carbapenems and its detection is largely a species property. The Klebsiella isolate acquired blaNDM-5, carries four plasmid replicons including IncFIB(K) and IncFII(K), and also carries a complete yersiniabactin siderophore cluster.
How were the samples collected and screened?
Seventy-seven poultry-associated samples were collected over eleven months from broiler farmhouses and slaughterhouses, comprising 59 cecal droppings and 18 cecal content specimens. The samples came from 18 poultry houses across six farms at one company and nine poultry houses across three farms at another. All three confirmed isolates came from a cecal dropping taken inside a farmhouse.
What should poultry producers do about carbapenem resistance?
Screen gut content as well as carcass surfaces, confirm phenotype before drawing conclusions, and sequence every confirmed producer. The distinction that matters most operationally is between an acquired gene such as blaNDM-5 and an intrinsic one such as blaPOM-1, because only the first signals a resistance determinant that can move between bacteria and between hosts.
What did the study not prove?
It did not prove transmission. There was no concurrent sampling of workers, birds and environment, so cross-host transfer and plasmid dissemination cannot be inferred. It also did not establish prevalence, because the sample was small and limited to two companies. No formal contamination controls such as field blanks were included, so low-level contamination cannot be entirely excluded.
Can carbapenem-resistant bacteria spread through the food chain?
This study does not demonstrate that, and it is careful not to claim it. All three isolates came from cecal material inside a farmhouse rather than from retail product, so the food chain link was not tested. What the genomic evidence does show is a mobile genetic backbone shared with a clinical isolate from another continent, which is a reason for surveillance rather than a measured exposure pathway.
