Botulism is a toxic disorder resulting from ingestion of the exotoxin produced by botulinum neurotoxin–producing Clostridia. It affects a wide variety of birds and mammals and has a worldwide distribution. Initial clinical signs include leg weakness and paresis that develops into a flaccid paralysis progressing from the legs to the nictitating membranes. Diagnosis is based on clinical signs and identification of botulinum toxin in serum or digestive contents or on identification of the toxin-producing clostridia.
Botulism is an intoxication that results from ingestion of preformed botulinum neurotoxins (BoNTs). The disease occurs worldwide and has been identified in at least 264 species of birds representing 39 families. Mammalian species affected by the toxin include humans, mink, ferrets, cattle, swine, dogs, horses, laboratory rodents, and various zoo animals.
Intoxications are sporadic in poultry, but an increased number of cases associated with free-range systems and decreased antimicrobial use has been recently observed (1, 2). Massive mortality events can occur in waterfowl.
Ruminants fed poultry manure contaminated with C botulinum spores have developed botulism.
Etiology of Botulism in Poultry
Clostridium botulinum is a gram-positive, spore-forming, rod-shaped anaerobic bacterium.
Nine types of BoNTs are produced by the proteolytic C botulinum group I strains (toxin types A and B and their variants and type F); the nonproteolytic C botulinum group II (types B, E, F) and group III (types C, D, and their mosaic variants C/D and D/C); and the proteolytic C argentinense group IV (type G). All strains can produce neurotoxins that cause flaccid paralysis.
Botulinum toxins are the most potent naturally occurring protein toxins known: an estimated 30–100 ng is sufficient to cause botulism in humans.
Botulinum toxins are neurotoxins with an affinity for motor neurons. After absorption, the toxin binds irreversibly to the presynaptic membrane of cholinergic nerve terminals. It enters the cell and blocks release of acetylcholine across the neuromuscular junctions, resulting in flaccid paralysis. Death results from cardiac and respiratory failure.
Toxin types A, B, E, and F botulinum neurotoxin–producing clostridia are associated with human food-poisoning disease while toxin types C and D BoNT-producing C botulinum are linked with avian and nonhuman mammalian botulism. Outbreaks in poultry and waterfowl are caused by the mosaic C/D, mosaic D/C, D, and C toxins and, infrequently, type E toxins.
C botulinum and other BoNT-producing clostridia strains are saprophytic bacteria, inhabiting soils and freshwater wetland (lake, marsh) sediments as well as decaying organic matter. Botulinum neurotoxin–producing clostridia are commonly found in the intestine of wild birds, but presence in the intestine of healthy poultry is variable.
Spore germination and bacterial growth with toxin production require an anaerobic environment that must also provide the necessary substrates as well as a temperature of 25°C or higher. This might explain why most outbreaks of botulism in waterfowl occur during the summer and fall.
Epizootiology of Botulism in Poultry
Certain invertebrates, such as insect larvae, can store various botulinum neurotoxins and are considered mechanical vectors. Rodents and birds can also harbor BoNT-producing clostridia strains in their intestines and, depending on their susceptibility, may or may not develop the disease.
Decomposition of contaminated invertebrates, dead rodents, or birds will provide the necessary environment for the bacteria to grow, produce BoNTs, and contaminate other BoNT-sensitive hosts.
During an outbreak, the main spreading factor is the carcass-maggot cycle. When an animal dies, spore germination and bacterial growth with toxin production will occur in that animal. Invertebrates, mostly maggots from necrophilous flies, will consume the BoNT and then be ingested by other birds, perpetuating the cycle of poisoning, death, carcass decay, and toxin production.
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Botulism may also result from direct ingestion of decaying organic matter that contains toxin. Contaminated feed, litter, boots, and equipment have also been reported as possible sources for introducing BoNT-producing clostridia into a poultry farm.
Environmental factors that contribute to the occurrence of outbreaks in wild birds, particularly waterfowl, include low and fluctuating water levels, the presence of vertebrate carcasses and rotting vegetation, and high ambient temperatures. The decomposition of the rotting fish, birds, and other carcasses produces an environment suitable for toxin production.
Outbreaks in commercial poultry are rare and generally tend to recur on the same farm, often affecting the same houses or pens. It is believed that moving poultry production indoors has decreased the risk of avian botulism. An increased incidence of cases in poultry is associated with free-range systems and decreased antimicrobial use (1, 2).
Clinical Findings of Botulism in Poultry
The time between consuming the BoNT and the appearance of the first clinical sign of botulism is determined by the amount of BoNT absorbed. Incubation periods in poultry range from 2 hours to ~2 weeks.
Clinical signs in poultry and wild birds are similar. Leg weakness and paresis that progress to flaccid paralysis of the legs, wings, neck, and nictitating membranes are characteristic clinical signs.
Limberneck, a common name for botulism in birds, comes from the neck paralysis typically observed in affected birds. Clinical signs in broiler chickens may also include ruffled or quivering feathers, feathers that are easily pulled out, and labored breathing.
Severely affected birds are in ventral recumbency on the floor with their eyes partially or completely closed and neck outstretched (see botulism photograph). They are unable to lift or hold their neck up and cannot raise their eyelids because of the flaccid paralysis that develops. Affected birds may have their legs extended behind them, because they are unable to pull them into a normal sitting position.
Courtesy of Dr. H. John Barnes.
Weakness is the earliest clinical sign in waterfowl. Birds are initially reluctant to fly when approached and have weak wingbeats and difficulty taking flight. As the disease progresses, they lose their ability to fly and develop stumbling gaits and eventually paralysis. Birds in water can drown, because they cannot keep their heads up.
Lesions
BoNTs do not cause lesions in affected birds, but maggots or other invertebrates may be found in the crop. Carcasses are usually in good condition and do not show evidence of a chronic or debilitating disease.
Diagnosis of Botulism in Poultry
Detection of toxin
Identification of toxin-producing clostridia
Preliminary diagnosis of botulism is based on the presence of evocative but not specific clinical signs and the absence of gross or microscopic lesions.
Strategies to confirm botulism include detection of BoNT from serum or digestive contents of sick birds, detection of the BoNT-producing clostridia in samples, or detection of BoNTs or BoNT-producing clostridia in feed or in the close environment of the sick birds.
A bioassay test in mice (mouse-lethality assay) is still considered the gold standard for detecting BoNTs, but because of ethical issues and the diagnosis delay caused by this test, alternative methods such as ELISA and mass spectrometry are often preferred. BoNT-producing clostridia can also be detected with PCR assays, but these do not detect biologically active BoNTs.
BoNTs are heat labile and can be destroyed at 80°C for ≥ 10 minutes, and sera must therefore be refrigerated or frozen as soon as possible after collection and shipped with ice packs to the testing laboratory.
Leg weakness or paralysis may be the only clinical sign in mild intoxications, which must be differentiated from the following:
Marek's disease, especially the acute transient paralysis form
enterococcal spondylitis and osteomyelitis
drug and chemical toxicosis (especially ionophore toxicity)
appendicular skeletal problems
In waterfowl, botulism must be differentiated from chemical toxicosis, especially lead poisoning, and acute, virulent infectious diseases (fowl cholera, duck viral enteritis, highly pathogenic avian influenza, etc).
Control and Prevention of Botulism in Poultry
Disposal of dead birds
Cleaning and disinfection
Biosecurity measures
Birds with botulism may recover without treatment or with supportive care, depending on their susceptibility and BoNT dose.
Beta-lactam antimicrobials have been used successfully in poultry during outbreaks. Antimicrobial use should be judicious and may be most helpful when there is a toxicoinfectious component (eg, botulism associated with C botulinum growth in the intestine).
Botulism antitoxins matching the toxin type can neutralize circulating botulinum toxins in birds. Multivalent antitoxins are available in some countries. Antitoxin treatment may be cost-prohibitive or of limited availability.
Prompt collection and rapid disposal of dead birds is critical to limiting the outbreak and breaking the carcass-maggot cycle. The following measures to mitigate losses might also be used:
physically separating clinically affected from clinically normal birds
replacing the litter
controlling fly and rodent infestation
implementing biosecurity measures to limit spread to other facilities
Cleaning and disinfecting with products effective against spore-forming bacteria should be performed after an outbreak to avoid recurrence.
In waterfowl outbreaks, wild birds should be dispersed from affected areas and water levels stabilized. Elimination of large, shallow areas may prevent conditions favorable for decay of vegetation and die-off of invertebrates, but again, rapid and proper disposal of dead carcasses is the most effective method.
Immunization with a toxoid vaccine is not cost-effective in commercial birds, but it has successfully been used in broilers, pheasants, and ducks housed on farms with recurring cases of botulism.
Zoonotic Risk of Botulism in Poultry
The zoonotic potential of type C botulism is minimal. Botulism in humans is caused by toxin types A, B, E, and F, and is mostly foodborne in origin. Rare cases of human botulism have been identified or suspected to be linked to toxinotypes C, D, C/D, and D/C. However, botulism caused by type C toxin has been confirmed in several nonhuman primates.
The CDC lists botulinum toxin as a category A agent due to the potential for use in bioterrorism or agroterrorism.
Key Points
Botulism is caused by ingestion of preformed botulinum neurotoxins (BoNTs). The disease is manifested clinically by progressive neurological clinical signs from the legs to the nictitating membranes, culminating in flaccid paralysis and cardiac and respiratory failure.
Outbreaks occur in waterfowl and poultry.
Diagnosis is based on clinical signs, epidemiological circumstances, and detection of BoNT in the serum or digestive contents of affected birds or by detection of the BoNT-producing clostridia in samples.
References
Woudstra C, Le Maréchal C, Souillard R, et al. New insights into the genetic diversity of Clostridium botulinum group III through extensive genome exploration. Front Microbiol. 2016;19(7):757. doi:10.3389/fmicb.2016.00757
Bano L. Bacterial diseases in a post-antibiotic era. Presented at: XXIInd World Veterinary Poultry Association Congress; September 26, 2023; Verona, Italy.
For More Information
Meurens F, Carlin F, Federighi M, et al. Clostridium botulinum type C, D, C/D, and D/C: an update. Front Microbiol. 2023;13:1099184. doi:10.3389/fmicb.2022.1099184
AAAP guidelines for judicious therapeutic use of antimicrobials in poultry.
