Botulism


Article Author:
Iain Jeffery


Article Editor:
Shahnawaz Karim


Editors In Chief:
Stephen Leslie
Karim Hamawy


Managing Editors:
Avais Raja
Orawan Chaigasame
Carrie Smith
Abdul Waheed
Khalid Alsayouri
Trevor Nezwek
Radia Jamil
Patrick Le
Anoosh Zafar Gondal
Saad Nazir
William Gossman
Hassam Zulfiqar
Steve Bhimji
John Shell
Matthew Varacallo
Heba Mahdy
Ahmad Malik
Sarosh Vaqar
Mark Pellegrini
James Hughes
Beata Beatty
Nazia Sadiq
Hajira Basit
Phillip Hynes
Tehmina Warsi


Updated:
11/14/2018 7:23:52 AM

Introduction

Botulism is a rare but potentially fatal syndrome of diffuse, flaccid paralysis caused by botulinum neurotoxin (BoNT), an exo neurotoxin elaborated by the bacterium Clostridium botulinum. Since its recognition as a foodborne entity in Germany and Belgium in the 1800s, several other etiologies of botulism have been described, including wound botulism, iatrogenic botulism, and inhalational botulism. While administration of polyvalent antitoxin to botulinum neurotoxin mitigates the clinical course of botulism, no true antidote exists, and management continues to rely on weeks of mechanical ventilation and other resource-heavy therapies while the body's neuromuscular signaling mechanisms recover. The most potent poison known to man, botulinum neurotoxin is relatively simple to produce, store, and disperse, and is thus a subject of intense interest for defense organizations around the world.[1] [2]

Etiology

 Botulism is a neuroparalytic syndrome that results from the systemic effects of an exo neurotoxin produced by the gram-positive, rod-shaped, spore-forming, obligate anaerobic bacterium Clostridium botulinum. Other Clostridium species (Clostridium butyricumClostridium baratii) occasionally produce the toxin as well. C. botulinum is a heterogeneous and ubiquitous group of bacteria, usually divided into four groups (groups I, II, III, and IV) based on physiologic characteristics. C. botulinum is easily isolated from soil, marine sediment, seafood, fruits, and vegetables. It forms heat-resistant spores that germinate in anaerobic, substrate-rich conditions to grow into toxin-producing bacilli.[2][3]

Botulinum neurotoxin is considered the deadliest toxin known due to its high potency and lethality, with a lethal dose (LD50 - the amount required to kill 50% of a test sample) of 1 ng to 3 ng (nanograms) of toxin per kilogram (kg) of body mass. The flaccid paralysis of botulism is the result of irreversible inhibition of acetylcholine (ACh) release at the presynaptic nerve terminal of the body's neuromuscular junctions (NMJs). Botulism can be acquired through exposure to the pre-formed toxin via improperly-stored food, iatrogenic injection, or bioterrorism, or it can result from the systemic release of the toxin in vivo, as in the cases of infant and wound botulism.

Epidemiology

Since 1973, the Centers for Disease Control and Prevention (CDC) has maintained the National Botulism Surveillance System to monitor cases of botulism in the United States. In the 5 years from 2011 through 2015, an average of 162 annual cases of botulism was reported. The respective proportions of each botulism type ranged from 71% to 88% for infant botulism, 1% to 20% for foodborne botulism, 5%-10% for wound botulism, and 1% to 4% for botulism of other or unknown origin. With the exception of rare, large outbreaks (i.e., an outbreak of foodborne botulism in Ohio in April 2015 accounted for 27 cases alone), the total number of botulism cases and relative proportions of each subtype have remained relatively stable over the past 10 years. There have been no reported cases of botulism due to bioterrorism in the United States, and only one reported case of iatrogenic botulism, which resulted from the use of an unlicensed, highly concentrated form of BoNT.[4][5]

Mortality from botulism is low. Before the 1950s, mortality rates for foodborne botulism were 60-70%. For the period 1975-2009, overall mortality was 3.0% with 109 botulism-related deaths among 3,618 botulism cases. There were 18 [less than 1%] deaths from 2352 cases of infant botulism, 61 [7.1%] deaths from 854 cases of foodborne botulism, 18 [5.0%] deaths from 359 cases of wound botulism, and 12 [22.6%] deaths from 53 cases of botulism from other or unknown origin.

Pathophysiology

Botulinum neurotoxin is a 150kDa protein that comprises a 100kDa heavy chain and 50kDa light chain linked by a single disulfide bridge. There are eight distinct serotypes of BoNT, A (BoNT/A) through H (BoNT/H), based on recognition by polyclonal serum. Toxin subtypes A, B, E, and rarely F, G, and H cause human disease. The vast majority of cases reported in the US are caused by BoNT/A and BoNT/B. While most strains of C. botulinum produce only one toxin serotype, dual toxin-producing strains have been identified. Toxin type A is the most potent, followed by BoNT/B.

The mode of entry of the toxin into the bloodstream depends on the type of exposure. In infant botulism, the lack of a robust immune system allows the proliferation of toxin-elaborating C. botulinum colonies in the digestive tract or bronchioles following ingestion or inhalation of spores. Once released, BoNT migrates via transcytosis across the mucosal barrier (either intestinal or pulmonary epithelium) into the circulation. The ingestion of preformed toxin in improperly stored food results in food-borne botulism, which is then absorbed in the intestinal tract similarly to infant botulism. Wound botulism is the result of C. botulinum spore germination in devitalized tissue, most commonly as a result of subcutaneous injection of spore-contaminated illicit drugs, with the release of BoNT into the local circulation.

Once in the bloodstream, BoNT travels to and binds presynaptic nerve terminals of the voluntary motor and autonomic NMJs. The heavy chain moiety of the toxin promotes endocytosis, after which the light chain is cleaved and released into the cytosol. The light chain targets and cleaves serotype-specific targets of the SNARE (SNAP-25, VAMP, or syntaxin) polypeptide complex, proteins required for fusion of ACh-containing vesicles with the presynaptic membrane. Fusion allows exocytosis of ACh into the NMJ and depolarization of the postsynaptic membrane. By cleaving these fusion complexes, BoNT blocks presynaptic ACh release and inhibits muscle contraction, causing a flaccid paralysis. Despite serotype-specific differences in target sites, all BoNT serotypes share the downstream syndrome of flaccid paralysis secondary to failure of ACh release at the NMJ.

Toxicokinetics

After exposure to BoNT, the time to symptom onset depends upon the dose of the toxin and the relevant kinetics of absorption. For food-borne botulism, symptoms typically appear within 12 to 72 hours of ingesting contaminated food, although onset times from as little as 2 hours to as long as 8 days have been recorded. For infectious (i.e., wound and infant) botulism, the onset depends on spore exposure time, time to germination, and how quickly the resulting colonies elaborate sufficient BoNT to cause symptoms, which varies widely with bacterial species, toxin serotype, and the patient’s age and immunological status.

Following symptom onset, the duration of symptoms is a function of toxin dose, toxin elimination, and regeneration of cleaved polypeptide components of the SNARE complex. The LD50 of BoNT is 1 ng/kg to 3ng/kg of body mass. Smaller doses affect fewer SNARE components and are cleared more quickly than larger doses. The elimination half-life (t1/2) of each toxin serotype is not known, however, a murine model of BoNT/A administered parenterally demonstrated a serum t1/2 of approximately 230 minutes.

Elimination of BoNT from the blood is enhanced by administration of serotype-specific neutralizing antibody (antitoxin), which limits the total number of SNARE complexes affected by the toxin. Once bound by antitoxin, BoNT is sequestered in the liver and spleen. Time to antitoxin administration significantly affects the clinical course. In one study of infant botulism, untreated infants had a significantly longer duration of mechanical ventilation (2.4 weeks versus 0.7 weeks), hospital admission (5.7 weeks versus 2.6 weeks), and tube feeding (10 weeks versus. 3.6 weeks) compared to treated infants. Similarly, earlier antitoxin administration (less than 12 hours) has been shown to reduce intensive care unit length of stay in both foodborne and wound botulism.

Regeneration of SNARE polypeptides is required for resumption of normal ACh release and muscle function and is related in part to the specific polypeptide targets of BoNT serotypes. A recent study comparing the activity of BoNT/A to BoNT/B revealed significantly longer time to the regeneration of the BoNT/A target protein SNAP-25. Case reports of infant botulism by different Clostridium species that elaborate the BoNT/E and BoNT/F serotypes describe much faster onset and resolution of symptoms compared to cases caused by the typical BoNT/A, which further supports the importance of SNARE component regeneration for the duration of the syndrome.

History and Physical

Botulism classically begins with cranial nerve palsies (“bulbar symptoms”) that progress to the symmetrical descending weakness of the trunk, extremities, and smooth muscle, with eventual flaccid paralysis. Patients usually have no sensory deficits except for blurred vision, although paresthesias are occasionally seen. Typical early symptoms include diplopia (visual disturbances), dysphagia (difficulty swallowing), dysphonia (voice change), and dysarthria (slurred speech), reflecting the high susceptibility of cranial nerve efferent presynaptic terminals to the activity of BoNT. Involvement of the diaphragm precipitates respiratory failure, often requiring intubation and mechanical ventilation. Palsies of autonomic smooth muscle cause constipation and urinary retention. Food-borne botulism will often present with a prodrome of abdominal pain, nausea, and vomiting beginning 12 to 72 hours after ingestion of the preformed toxin.

The presentation and severity of infant botulism are variable, due to different inoculum sizes, host susceptibilities, and time to presentation. Early symptoms frequently involve constipation, weakness, feeding difficulties, weak cry, and drooling. A ‘floppy baby’ exhibiting global hypotonia implies the need for immediate intubation and mechanical ventilation.

Wound botulism should be suspected in patients who present with bulbar symptoms and cellulitis secondary to subcutaneous administration of illicit drugs. The incubation time for wound botulism is 5 to 15 days from the time of spore introduction. Wound botulism is the only variant presenting with fever and signs of infection.

Evaluation

Many presentations of botulism are subtle and easily missed. Because therapy should be administered as early as possible, and laboratory confirmation of botulism takes several days, treatment will often proceed based on clinical suspicion alone. A careful history and physical exam are therefore essential. Electrophysiologic studies (electromyogram/EMG) can support a presumptive diagnosis based on history and physical while laboratory results are pending.[6]

Laboratory confirmation of botulism can be obtained with serum and stool assays for BoNT, stool microscopy for spores, stool cultures, and wound cultures in the case of wound botulism. Laboratory testing to detect BoNT has traditionally relied on the mouse lethality assay, wherein a live mouse is injected with a sample of stool or serum from a subject and observed for signs of botulism and death. Attempts at developing immunologic assays for BoNT detection (ELISA, electrochemiluminescence) suffer from low-quality antibodies and confounding by factors in complex matrices like stool and serum, with consequently low sensitivity. Endopeptidase assays have demonstrated high sensitivity and specificity and are still currently in development.

Treatment / Management

Treatment of botulism consists of antitoxin administration, hospital admission, close monitoring, respiratory support as required, and debridement plus antibiotics in the case of wound botulism. Any patient with a clinical presentation concerning for botulism should be hospitalized immediately for close observation. Antitoxin therapy available to healthcare providers currently exists in two forms: heptavalent equine serum antitoxin, indicated for patients older than 1 year, and human-derived immunoglobulin, indicated for infants under the age of 1. Heptavalent equine serum antitoxin contains antibodies to BoNT/A-BoNT/G and is available through State Health Departments and the CDC.[7][8]

When botulism is suspected, the clinician should seek immediate assistance from their regional Poison Control Center, State's Health Department, or the CDC Director’s Emergency Operations Center. If suspicion is high and symptoms are progressing, immediate antitoxin acquisition and administration is indicated. The dose for adults is one vial. The dose for infants, children, and adolescents should be established in conjunction with Poison Control.

Close monitoring should include frequent clinical evaluation of ventilation, perfusion, and upper airway integrity, continuous pulse oximetry, spirometry, and arterial blood gas measurement. Intubation should be considered for patients with upper airway compromise or vital capacity less than 30% of predicted.

For wound botulism, debridement and antibiotic therapy are indicated following antitoxin administration. Appropriate regimens include three million units of Penicillin G intravenously (IV) every 4 hours, or metronidazole 500 mg every 8 hours for penicillin-allergic patients. Aminoglycosides are relatively contraindicated as they have been shown to potentiate neuromuscular blockade caused by botulism. Antibiotics should not be used in infant botulism because of possible BoNT release following cell lysis. Additional therapies include total parenteral nutrition in cases of severe ileus and whole bowel irrigation in cases of foodborne botulism without severe ileus.

Complications

  • Nosocomial infections
  • UTI
  • Thrombophlebitis
  • Deep vein thrombosis
  • Pressure sores
  • Contractures
  • Failure to thrive

Pearls and Other Issues

 

Vaccines

An investigational pentavalent botulinum toxoid is available for persons at elevated risk for BoNT exposure, such as laboratory workers and military personnel. No FDA-approved vaccine exists for the general public. The pentavalent toxoid is not being considered for public use due to cost, the number of required vaccinations, and the recent decline in immunogenicity.

Security

Botulinum neurotoxin has been considered for use as a weapon of mass destruction by terrorist organizations and nations for over 60 years, and several examples of the militarized development of BoNT exist. The Aum Shinrikyo cult in Japan attempted to disperse BoNT at United States bases in Japan in the 1990s. Operation Desert Storm revealed several thousand liters of concentrated BoNT in Iraq, half of which had been loaded onto military weapons systems. Models of terrorist attacks employing BoNT release into consumer goods have indicated several deficiencies in the country’s capacity to thwart such an attack. Due to its potency, its lethality, and the facility with which it can be isolated, acquired, stored, and disseminated, BoNT continues to be an area of intense interest for national security organizations around the world.

Enhancing Healthcare Team Outcomes

An evidence-based approach to botulism

Botulism is a serious neurological disorder that can be life-threatening. Because of the systemic effects, the disorder is best managed by a multidisciplinary team that consists of a neurologist, infectious disease expert, intensivist, pulmonologist, pharmacist and ICU nurses.

Unlike the past, the mortality from botulism has significantly declined in the last 3 decades. today, the risk of death for an infant is less than 1%. However, the recovery is often prolonged and may take months or even years to fully become functional. For those who suffer from hypoxia, some type of neurological deficit will be present for life.[9][10][11]

Prevention

The most important concern for prevention of botulism is proper food handling technique. In particular, appropriate processing of home-canned and home-preserved food, including minimum temperature, pressure, and cooking times per manufacturer’s recommendations, kills Clostridium spores and effectively prevents toxin exposure. Boiling home-canned food for 10 minutes will inactivate preformed toxin and kill bacteria, but will not destroy spores. Infant botulism is best prevented by avoiding honey for infants less than 12 months of age. 


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Botulism - Questions

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What agent can inhibit acetylcholine release at the presynaptic terminal?



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Which of the following prevents the release of acetylcholine by preventing fusion of vesicles to the membrane?



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Which of the following prevents the release of acetylcholine from the nerve endings?



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Which of the following statements about acetylcholine is false?



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Following the ingestion of improperly canned tomatoes, a 17-year-old female patient contracts botulism. What is the treatment of choice?



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What neurotransmitter does Clostridium botulinum affect?



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A 17-year-old male patient with a history of intravenous drug use complains of a few days history of pain to his left arm, double vision, fever, and difficulty swallowing. He is awake, alert, and oriented to person, place and time, and denies any headache or neck stiffness. Exam shows a blood pressure of 110/81 mmHg, temperature of 99.3 F, heart rate of 110 beats/min, and respiratory rate of 18. Kernig and Brudzinski testing are within normal limits. A large erythematous, warm, and indurated rash on the left arm is noted with several track marks and pustular lesions. Cranial nerves II through XII are grossly intact, and the bladder is distended. Which of the following is the next best step?



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A patient is seen in the emergency room with a 2-day history of low-grade fever, general malaise, and neurological findings. Botulism is suspected. What finding should prompt consideration of another disease entity?



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A patient initially notices double vision after eating supper. Shortly thereafter, she starts to experience weakness in arms and legs, difficulty with swallowing, extreme trouble focusing her vision, and some minor breathing difficulties. 911 is called and she is brought to the ER. The doctor notices bilateral drooping of the eyelids and dilated fixed pupils. Her respiratory status has become more fragile. What is the likely diagnosis?



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What is a common cause of botulism in the United States?



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Which of the following drugs can block release of acetylcholine from its vesicles?



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A 48-year-old female presents with the complaint of lower extremity weakness, slurred speech, and blurred vision. Also, she reports the acute onset of abdominal pain, nausea, and vomiting 18 hours prior. On exam, she is awake, alert, and oriented to person, place, and time, shows dilated pupils, paraparesis, areflexia, and bilateral external ophthalmoplegia. The sensory exam is normal. Electromyography and nerve conduction velocity studies show short duration and small amplitude of recruited motor unit action potentials after voluntary contraction and lower extremity decreased compound muscle action potentials. Repetitive nerve stimulation reveals insignificant incremental response at 50 Hz stimulation and decremental response at 3 Hz stimulation. What is the most probable diagnosis?



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Which of the following is the most likely mechanism of action for migraine prevention with botulinum toxin?



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What is the mechanism of action of botulinum toxin?



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All of the following statements about Clostridium botulinum are true except:



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Which of the following Clostridium botulinum toxins is the most common cause of foodborne outbreaks?



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Which of the following statements about Clostridium botulinum toxin is true?



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How are the clinical pictures of foodborne and of wound botulism different?



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Which of the following statements is not true of wound botulism?



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Which of the following statements about mortality from Clostridium botulism is false?



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Which of the following neurological derangements is not seen in botulism?



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Which of the following tests is helpful in the diagnosis of botulism?



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Which of the following may be helpful in the diagnosis of botulism?



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The treatment of botulism requires rigorous, supportive care with which of the following being the most critical?



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The medical management of foodborne botulism may include all of the following except:



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Which is not part of the treatment of wound botulism?



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Which of the following is the antibiotic of choice for wound botulism?



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Which is not accomplished by boiling food for ten minutes?



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A patient develops abdominal pain, nausea, vomiting, and diarrhea 12 hours after eating some peaches that were home canned by her grandmother. What is the most likely etiological agent?



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Select the incorrect pairing of bacterial toxin and its action.



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Botulinum toxin, in very small doses, is a popular treatment for facial wrinkles. Historically, this toxin has been associated with paralysis and death. Which of the following best describes its mechanism of action?



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What is the pathophysiology of botulism toxin?



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Which of the following medications can exacerbate botulism?



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A patient presents with a case of botulism from eating contaminated canned soup. What is the primary treatment for this infection?



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How does botulinum toxin reducing sweating?



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A patient with no significant past medical history is brought to the emergency department with flaccid paralysis, ptosis, and diplopia. He reports eating canned food the day before the presentation. The release of which of the following neurotransmitters is inhibited by the bacterial toxin most likely responsible for the patient's condition?



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Botulism - References

References

Dong M,Masuyer G,Stenmark P, Botulinum and Tetanus Neurotoxins. Annual review of biochemistry. 2018 Nov 2     [PubMed]
Silva ROS,Martins RA,Assis RA,Oliveira Junior CA,Lobato FCF, Type C botulism in domestic chickens, dogs and black-pencilled marmoset (Callithrix penicillata) in Minas Gerais, Brazil. Anaerobe. 2018 Jun     [PubMed]
Hellmich D,Wartenberg KE,Zierz S,Mueller TJ, Foodborne botulism due to ingestion of home-canned green beans: two case reports. Journal of medical case reports. 2018 Jan 4     [PubMed]
Czerwiński M,Czarkowski MP,Kondej B, Foodborne botulism in Poland in 2016 Przeglad epidemiologiczny. 2018     [PubMed]
Rao AK,Lin NH,Jackson KA,Mody RK,Griffin PM, Clinical Characteristics and Ancillary Test Results Among Patients With Botulism-United States, 2002-2015. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2017 Dec 27     [PubMed]
Zariquiey-Esteva G,Galeote-Cózar D,Santa-Candela P,Castanera-Duro A, Botulism in the ICU: Nursing care plan. Enfermeria intensiva. 2018 Apr - Jun     [PubMed]
Long SS, BabyBIG has BIG advantages for treatment of infant botulism. The Journal of pediatrics. 2018 Feb     [PubMed]
Sobel J,Rao AK, Making the Best of the Evidence: Toward National Clinical Guidelines for Botulism. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2017 Dec 27     [PubMed]
Griese SE,Kisselburgh HM,Bartenfeld MT,Thomas E,Rao AK,Sobel J,Dziuban EJ, Pediatric Botulism and Use of Equine Botulinum Antitoxin in Children: A Systematic Review. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 2017 Dec 27     [PubMed]
Martin SJ,Penrice G,Amar C,Grant K,Gorrie GH, Wound botulism, its neurological manifestations, treatment and outcomes: A case series from the Glasgow outbreak, 2015. Scottish medical journal. 2017 Nov     [PubMed]
Opila T,George A,El-Ghanem M,Souayah N, Trends in Outcomes and Hospitalization Charges of Infant Botulism in the United States: A Comparative Analysis Between Kids' Inpatient Database and National Inpatient Sample. Pediatric neurology. 2017 Feb     [PubMed]

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