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Adult Intestinal Botulism: A Rare Presentation in an Immunocompromised Patient With Short Bowel Syndrome

Open AccessPublished:August 03, 2018DOI:https://doi.org/10.1016/j.mayocpiqo.2018.06.005

      Abstract

      The cholinergic heat-labile neurotoxin produced by Clostridium species is primarily responsible for the clinical manifestations of botulism. The classic phenotypic presentation of botulism consists of subacute descending flaccid paralysis with intact sensory function. Traditionally, it is classified into 3 main forms (foodborne, wound-related, and infantile) on the basis of primary site of toxin entry into the human nervous system. Toxemia is the common pathophysiology in all forms of botulism. Adult intestinal toxemia botulism is an extremely rare form of the disease with pathogenesis similar to that of infant-type botulism. Symptomatic adults usually have an anatomic abnormality in the gastrointestinal tract leading to changes in normal gut flora. The current case is an addition to the growing literature on this unusual clinical variant of botulism.

      Abbreviations and Acronyms:

      CDC (Centers for Disease Control and Prevention), HBAT (heptavalent botulinum antitoxin)
      Botulism, a rare infectious clinical entity caused by several Clostridium species, is predominantly manifested as a paralytic neurologic disease in humans.
      • Shapiro R.L.
      • Hatheway C.
      • Swerdlow D.L.
      Botulism in the United States: a clinical and epidemiologic review.
      Because of the dangerous toxins they produce and the potential for mass public involvement, botulism is a nationally notifiable disease.
      • Arnon S.S.
      • Schechter R.
      • Inglesby T.V.
      • et al.
      Botulinum toxin as a biological weapon: medical and public health management.
      Traditionally, botulism has been classified into 3 main forms— infantile, foodborne, and wound-related—based on the primary route of toxin entry to the human body.
      • Brook I.
      Botulism: the challenge of diagnosis and treatment.
      There is also an extremely rare variant called infant-like botulism or adult intestinal toxemia botulism,which mainly affects children older than than 12 months and adults.
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      The clinical presentations are similar in all varieties of botulism. The affected patient presents with descending, symmetric, flaccid paralysis involving the motor and autonomic nervous system. The sensory nervous system is not affected in botulism.
      • Brook I.
      Botulism: the challenge of diagnosis and treatment.
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      We report a case of suspected adult intestinal colonization (intestinal toxemia) botulism and discuss the clinical features to increase awareness among physicians about this rare disease.

      Report of Case

      A 66-year-old woman presented to the emergency department with a 1-day history of worsening low back pain, difficulty raising her arms and walking up stairs, and a “thick tongue” with progressive dysphagia and dysarthria. She also reported a 3-day history of bloating, abdominal pain, and constipation (her daily normal was 2-3 bowel movements per day). She had no fever, vomiting, diarrhea, insect or tick bites, or presence of new skin lesions. She was hemodynamically stable on admission. She was alert and oriented, with normal heart, lung, and abdominal physical examination findings. Her neurologic examination revealed proximal lower and upper extremity motor weakness, normal pupillary size and reaction to light, no ptosis, normal deep tendon reflexes, and normal rectal tone. She was admitted to the medical ward under supervision of the neurology team. The patient's medical history included autoimmune hemolytic anemia, short bowel syndrome following complications of a cholecystectomy leading to ileal resection, lumbago, hypertension, and hypothyroidism. She had been chronically immunosuppressed with oral corticosteroids (10-15 mg/d) for her autoimmune anemia. Her personal and family histories were unremarkable.
      She experienced worsening tachypnea and dysarthria and had bilateral ptosis, lateral gaze palsy with no convergence of the right eye, and sluggish pupillary reaction to light within 12 hours of admission. Physical examination findings were notable for decreased strength in the neck, shoulder, and hip girdle muscles, with normal sensory function. The initial differential diagnosis considered by the neurology team included spinal cord lesions, myasthenia gravis, and atypical variants of Guillain- Barré syndrome. With myasthenia crisis high on the differential list, empiric intravenous immunoglobulins, high-dose corticosteroids, and oral pyridostigmine were initiated.
      On day 2 of hospitalization, worsening respiratory muscle weakness developed, as evidenced by declining negative inspiratory forces and vital capacity. She required tracheal intubation and mechanical ventilatory support for hypercapnic respiratory failure and was transferred to the intensive care unit for further care. Neurologic assessment revealed features of worsening descending symmetrical flaccid paralysis, complete ophthalmoplegia, profound ptosis, dilated pupils, absent gag reflex, dysphagia, dysarthria, inability to lift her head, and an intact sensory nervous system. Botulism was strongly suspected as well as the neurologic conditions that can affect the cranial nerves, brain stem, and spinal cord.
      Electromyography revealed myopathic features without marked effects of repetitive stimulation. Nerve conduction studies showed low-amplitude motor action potentials with normal conduction velocity and normal sensory action potential. Lumbar puncture was not performed. Her C-reactive protein level, white blood cell count, and erythrocyte sedimentation rate were normal, as were thyroid, liver, and renal function and results of a myasthenia serology panel. Magnetic resonance imaging of the brain and spine revealed no abnormalities.
      With strong suspicion for botulism, further therapy with corticosteroids, pyridoxine, and intravenous immunoglobin was discontinued. The Centers for Disease Control and Prevention (CDC) was contacted for guidance and assistance in obtaining botulinum antitoxin therapy. With the help of the CDC team, botulism antitoxin was administered to the patient within 8 hours of diagnostic suspicion on day 2 of her hospital stay. Stool cultures for Clostridium botulinum were not performed; confirmatory toxin testing including serum and stool studies performed at a reference laboratory were reported to be positive for botulinum toxin A. Results of an investigation for exposure to contaminated food conducted by the Florida Department of Health and Epidemiology were negative. Polyethylene glycol solution was administered to facilitate excretion of the toxin and spore-forming bacteria from the intestine. A 2-week regimen of oral metronidazole and intravenous penicillin G was initiated to facilitate the eradication of the C botulinum from the gastrointestinal tract. Surgical tracheostomy was performed for ventilatory support on hospital day 7 because of persistent respiratory failure. The patient had symptomatic improvement as evidenced by improved facial movements, increased ability to nod her head and write letters with her hand, and increased shoulder and hip movements. She was discharged to a rehabilitation facility after 16 days of hospitalization. However, she was readmitted 40 days after her initial admission with paralytic ileus. Although recurrence of botulism ileus was suspected, the patient improved with conservative management and was discharged after 5 days. Unfortunately, she ultimately experienced recurrent deep venous thrombosis, a complication of her prolonged illness, and died in the rehabilitation facility.

      Discussion

      The neurotoxin produced by C botulinum, a gram-positive anaerobic spore-forming rod, is responsible for paralytic disease manifestations in humans.
      • Brook I.
      Botulism: the challenge of diagnosis and treatment.
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      Human disease from the toxin produced by Clostridium butyricum and Clostridium baratii has also been reported in case series.
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      • Green J.
      • Spear H.
      • Brinson R.R.
      Human botulism (type F)—a rare type.
      • Gupta A.
      • Sumner C.J.
      • Castor M.
      • Maslanka S.
      • Sobel J.
      Adult botulism type F in the United States, 1981-2002.
      • Harvey S.M.
      • Sturgeon J.
      • Dassey D.E.
      Botulism due to Clostridium baratii type F toxin.
      • Sheppard Y.D.
      • Middleton D.
      • Whitfield Y.
      • et al.
      Intestinal toxemia botulism in 3 adults, Ontario, Canada, 2006-2008.
      According to the CDC's Botulism Surveillance Summary 2016,
      • Centers for Disease Control and Prevention
      National Botulism Surveillance Summary 2016.
      there were 205 confirmed and 10 probable cases of human botulism that year. Distribution of the major types of botulism such as infantile, food, and wound are 73%, 14%, and 12%, respectively. Only 1% of cases were reported to be of other etiology. Among the probable cases, 80% are suspected to be foodborne, and the remaining 20% are attributed to wound botulism.
      • Centers for Disease Control and Prevention
      National Botulism Surveillance Summary 2016.
      Intestinal colonization and growth of C botulinum as a possible mechanism of intoxication was suspected as far back as in 1921, but it was never recognized until 1976 when the pathogenesis of infant botulism was documented.
      • Midura T.F.
      • Arnon S.S.
      Infant botulism: identification of Clostridium botulinum and its toxins in faeces.
      Most cases of infant botulism were confined to children aged less than 12 months. However, since early 1980, there have been sporadic cases of noninfant intestinal colonization, and its consequent clinical manifestations were reported from different continents of the world.
      • Bradley W.G.
      • Shahani B.T.
      • Hyslop Jr., H.Y.
      Case Records of the Massachusetts General Hospital: Case 48-1980—Rapidly progressive neurologic disorder following gastrointestinal symptoms.
      Since the first case description in 1986, a total of 33 cases of intestinal toxemia botulism have been described in the literature. Three species of Clostridium (botulinum, butyricum, and baratii) have been incriminated as the causes of clinical botulism resulting from intestinal toxemia.
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      A detailed summary of published cases is presented in the Table.
      TableSummary of Reported Cases of Intestinal Botulism
      F = female; GI = gastrointestinal tract; IBD = inflammatory bowel disease; M = male; US = United States.
      Reference, yearCountry, year of diagnosis
      Year of diagnosis provided when available.
      Age/sexUnderlying GI pathologyPrior antibiotic useTime to diagnosisOrganism and type of toxin incriminatedAntitoxin therapy receivedOutcome
      Bradley et al,
      • Bradley W.G.
      • Shahani B.T.
      • Hyslop Jr., H.Y.
      Case Records of the Massachusetts General Hospital: Case 48-1980—Rapidly progressive neurologic disorder following gastrointestinal symptoms.
      1980
      US47/MUnknownNoneUnknownClostridium botulinum type BUnknownSurvived
      McCroskey & Hatheway,
      • McCroskey L.M.
      • Hatheway C.L.
      Laboratory findings in four cases of adult botulism suggest colonization of the intestinal tract.
      1988
      US, 198033/FIleojejunal bypassUnknown2 dC botulinum type AUnknownDied
      US, 198870/MUnknownNoneUnknownClostridium baratii type FUnknownSurvived
      Iceland, 198827/MNoneNone25 dC botulinum type BUnknownSurvived
      Green et al,
      • Green J.
      • Spear H.
      • Brinson R.R.
      Human botulism (type F)—a rare type.
      1983
      US, 198154/MNoneNoneUnknownC botulinum type FUnknownSurvived
      Gupta et al,
      • Gupta A.
      • Sumner C.J.
      • Castor M.
      • Maslanka S.
      • Sobel J.
      Adult botulism type F in the United States, 1981-2002.
      2005
      US, 198623/MUnknownUnknownUnknowntype FYesSurvived
      US, 199255/MNoneNone1 dC baratii type FYesSurvived
      US, 199359/FNoneNoneUnknownC baratii type FYesSurvived
      US, 199561/MNoneNone<1 dClostridium butyricum type EYesSurvived
      US, 199554/FNoneYes<1 dC baratii type FYesSurvived
      US, 199733/MNoneYes<1 dC baratii type FYesSurvived
      US, 200065/FEsophageal dilationNo2 dC baratii type FYesSurvived
      US, 200076/FDiverticulitisNo1 dtype FYesSurvived
      US, 200145/FGastric staplingYes<7 dtype FYesRecovery
      US, 200252/FColonoscopyYes<7 dC baratii type FYesRecovery
      Chia et al,
      • Chia J.K.
      • Clark J.B.
      • Ryan C.A.
      • Pollack M.
      Botulism in an adult associated with food-borne intestinal infection with Clostridium botulinum.
      1986
      US37/FAntrectomy, vagotomy, and Billroth type INoneUnknownC botulinum type AYesDied
      Freedman et al,
      • Freedman M.
      • Armstrong R.M.
      • Killian J.M.
      • Boland D.
      Botulism in a patient with jejunoileal bypass.
      1986
      US45/FIntestinal obstruction and resectionUnknown5 dC botulinum type BNoSurvived
      McCroskey et al,
      • McCroskey L.M.
      • Hatheway C.L.
      • Woodruff B.A.
      • Greenberg J.A.
      • Jurgenson P.
      Type F botulism due to neurotoxigenic Clostridium baratii from an unknown source in an adult.
      1991
      US, 198754/MTruncal vagotomy and pyloroplastyNone2 dC baratii type FYesSurvived
      Shen et al,
      • Shen W.P.
      • Felsing N.
      • Lang D.
      • Goodman G.
      • Cairo M.S.
      Development of infant botulism in a 3-year-old female with neuroblastoma following autologous bone marrow transplantation: potential use of human botulism immune globulin.
      1994
      US3/FNoneYesUnknownC botulinum type AYesDied
      Fenicia et al,
      • Fenicia L.
      • Franciosa G.
      • Pourshaban M.
      • Aureli P.
      Intestinal toxemia botulism in two young people, caused by Clostridium butyricum type E.
      1999
      Italy, 19949/MMeckel diverticulumYes5 dC butyricum type ENoSurvived
      Italy, 199519/FMeckel diverticulumYes2 dC butyricum type EYesSurvived
      Italy, 199756/MNone, but heart surgery and antibiotic use 1 mo beforeYes30 dC botulinum type AUnknownSurvived
      Griffin et al,
      • Griffin P.M.
      • Hatheway C.L.
      • Rosenbaum R.B.
      • Sokolow R.
      Endogenous antibody production to botulinum toxin in an adult with intestinal colonization botulism and underlying Crohn's disease.
      1997
      US67/MIBD + colonic resectionUnknown3 dC botulinum type AYesSurvived
      Arnon,
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      1995
      US48/FColostomy for bowel cancerUnknownUnknownC botulinum type BUnknownUnknown
      US51/FIleojejunal bypassYesUnknownC botulinum type BUnknownUnknown
      Harvey et al,
      • Harvey S.M.
      • Sturgeon J.
      • Dassey D.E.
      Botulism due to Clostridium baratii type F toxin.
      2002
      US, 200143/FNoneYes<7 dC barati type FYesSurvived
      Kobayashi et al,
      • Kobayashi H.
      • Fujisawa K.
      • Saito Y.
      • et al.
      A botulism case of a 12-year-old girl caused by intestinal colonization of Clostridium botulinum type Ab.
      2003
      Japan12/FNoneNo5 dC botulinum type AYesSurvived
      Sheppard et al,
      • Sheppard Y.D.
      • Middleton D.
      • Whitfield Y.
      • et al.
      Intestinal toxemia botulism in 3 adults, Ontario, Canada, 2006-2008.
      2012
      Canada45/MUnknownNo6 dC botulinum type BYesRecovery
      Canada50/FIBD, bowel surgeryNo3 dC botulinum type AYesRecovery
      Canada63/FIBD, bowel surgeryNo1 dC botulinum type AYesRecovery
      Hannett et al,
      • Hannett G.E.
      • Schaffzin J.K.
      • Davis S.W.
      • et al.
      Two cases of adult botulism caused by botulinum neurotoxin-producing Clostridium baratii.
      2014
      US79/MEndoscopy 3 d priorNo3 dC baratii type FYesDied
      US68/FNoneYes3 dC baratii type FYesRecovery
      Schaack et al,
      • Schaack L.
      • Weiland J.
      • Steck A.
      Intestinal botulism: the lurking threat of bariatric surgery.
      2017
      US33/FGastric bypassUnknown10 dC botulinum type FYesSurvived
      Freund et al,
      • Freund B.
      • Hayes L.
      • Rivera-Lara L.
      • et al.
      Adult intestinal colonization botulism mimicking brain death.
      2017
      US43/FNoneNo21 dC botulinum type AYesSurvived
      Parameswaran et al,
      • Parameswaran L.
      • Rao A.
      • Chastain K.
      • et al.
      A case of adult intestinal toxemia botulism during prolonged hospitalization in an allogeneic hematopoietic cell transplant recipient.
      2017
      US27/FGraft-vs-host diseaseYes59 dC botulinum type AYesDied
      a F = female; GI = gastrointestinal tract; IBD = inflammatory bowel disease; M = male; US = United States.
      b Year of diagnosis provided when available.
      The 7 antigenic variants of botulinum neurotoxin, designated by the letters A through G, are some of the most lethal toxins known to mankind. Human botulism is predominantly caused by toxin types A, B, and E.
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      Type A is the major toxin incriminated in 56% of reported cases, followed by toxin type B and type E in 41% and 3% of cases, respectively, in the latest CDC report.
      • Centers for Disease Control and Prevention
      National Botulism Surveillance Summary 2016.
      Neurotoxin produced by C butyricum and C baratii are referred to as “botulinum-like” and can be neutralized by either botulinum type E or type F antitoxin.
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      Toxin specificity to motor neuronal synapses and inhibition of acetylcholine release leading to blockage of synaptic transmission are responsible for the lethality of the toxin.
      • Brook I.
      Botulism: the challenge of diagnosis and treatment.
      Spores from C botulinum are ubiquitous in our environment and can be isolated from soil, dust, food, and water sources. Biodiversity of the normal adult intestinal gut milieu normally does not allow germination, vegetation, and toxin production of the ingested C botulinum spores. Infants are susceptible to C botulinum colonization because of an immature gut mucosal barrier and a weak local immune response. All patients with adult intestinal toxemia have an underlying structural abnormality, an alteration of normal intestinal flora, or both. Structural abnormalities include either an anatomic defect or altered anatomy of the gastrointestinal tract by surgery or inflammatory bowel disease. The alterations of intestinal microflora are related to the prevalence of broad-spectrum antibiotic usage. The development of adult intestinal botulism is believed to be caused by ingestion and germination of spores resulting in intestinal colonization of bacteria, in situ production of the botulism neurotoxins within the gastrointestinal tract, and subsequent systemic absorption.
      • Moberg L.J.
      • Sugiyama H.
      The rat as an animal model for infant botulism.
      This process differs from classic foodborne botulism in that the causative toxin is acquired from intra-intestinal production rather than from food contaminated with preformed toxin.
      • Moberg L.J.
      • Sugiyama H.
      The rat as an animal model for infant botulism.
      We believe that short bowel syndrome related to her prior surgical complication and immunosuppression due to long-term corticosteroid use are the 2 predisposing factors for presumptive C botulinum intestinal colonization (intestinal toxemia) in our patient.
      The classic triad of botulism consists of the acute or subacute presentation of a symmetric, descending flaccid paralysis involving the bulbar muscles, a clear sensorium, and the absence of fever.
      • Arnon S.S.
      Botulism as an intestinal toxemia.
      Clinical presentation without cranial nerve involvement is extremely rare. Similar to infantile botulism, the adult intestinal variety can present with constipation, lethargy, and poor feeding. Our patient had all of these features before hospital admission. Although not performed in most clinical microbiology laboratories, definitive diagnosis of intestinal toxemia botulism is performed by demonstration of neurotoxigenic species, with or without concomitant presence of toxin, in the stool of the patient with clinical features compatible with botulism. Detection of botulinum toxin in the serum of an adult patient is also diagnostic. Electromyography, cerebrospinal fluid and serum toxin assays, and imaging are helpful to exclude other etiologies in the differential diagnosis such as Guillain-Barré syndrome, myasthenia gravis, organophosphate poisoning, tick bite, and other metabolic abnormalities.
      • Brook I.
      Botulism: the challenge of diagnosis and treatment.
      However, in a patient with a classic history and characteristic physical findings, prompt testing for botulinum toxin should be arranged through the CDC or the state health department laboratory. In our case, testing for C botulinum or botulinum toxin in stool was not performed on samples collected on admission. Because of the hazardous nature of botulinum toxin, and in accordance with regulatory guidance from the U. S. Centers for Medicare and Medicaid Services, clinical microbiology laboratories are specifically instructed to not perform culture isolation, identification studies, or toxin analysis for C botulinum. Routine stool culture for specific detection of C botulinum is also not recommended because of biosafety considerations.
      Improved critical care practice has resulted in reduction in case fatality rates, even though the number of botulism outbreaks has remained steady over the years. Supportive care is the mainstay of therapy in suspected or confirmed botulism cases. Neutralization of the antitoxin and eradication of the Clostridium species are also advised. The CDC guidelines advocate administration of botulism antitoxin for adult patients as soon as a clinical diagnosis is made, without waiting for laboratory confirmation. Heptavalent botulinum antitoxin (HBAT), containing antitoxin against the neurotoxin subtypes A through G, is available through the CDC. Antibiotic therapy in botulism remains controversial. Treatment with penicillin and metronidazole are recommended in wound-related botulism cases. Because of concern about disease aggravation by bacteriolysis and release of toxin, antibiotics are not recommended in infantile botulism. However, the adult intestinal toxemia variant is characterized by its protracted course and also risk of relapse even after treatment with antitoxin because of the ongoing intraluminal production of toxin. Restoration of the normal gut microbial flora by elimination of the toxin-producing bacteria is necessary for disease control. In the absence of guidelines for any additional treatment such as antibiotics in cases of intestinal colonization, we decided to use metronidazole and penicillin G to eradicate the bacteria colonizing the intestinal tract. Recurrence of botulism was reported 10 days after administration of botulism antitoxin in a patient with intestinal colonization.
      • Fagan R.P.
      • Neil K.P.
      • Sasich R.
      • et al.
      Initial recovery and rebound of type F intestinal colonization botulism after administration of investigational heptavalent botulinum antitoxin.
      The authors proposed that once HBAT cleared (the half-life of HBAT is 12-24 hours) from the patient's system, the continued absorption of toxin from the colonized intestines was possibly responsible for the recurrence. In our case, the patient returned to the hospital with constipation, which could be explained by the recurrence of botulism. Retrospectively, we believe that our patient had rebound botulism neurotoxicity and could have benefited from an additional dose of antitoxin. Guidance in the literature is scarce regarding when to proceed with a second antitoxin dose.

      Conclusion

      Adult intestinal toxemia botulism is rare and underrecognized. Astute clinical acumen and prompt antitoxin therapy may be lifesaving in this rare disease.

      Acknowledgments

      We thank the microbiology laboratory at Mayo Clinic in Florida and the CDC botulism detection section for their assistance.
      Drs Guru and Becker contributed equally to the submitted manuscript.

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