Botulism is a rare, life-threatening paralytic illness caused by neurotoxins produced by an anaerobic, gram-positive, spore-forming bacterium, Clostridium botulinum. Unlike Clostridium perfringens, which requires the ingestion of large numbers of viable cells to cause symptoms, the symptoms of botulism are caused by the ingestion of highly toxic, soluble exotoxins produced by C. botulinum while growing in foods.
These rod-shaped bacteria grow best under anaerobic (or, low oxygen), low-salt, and low-acid conditions. Bacterial growth is inhibited by refrigeration below 4° C., heating above 121° C, and high water-activity or acidity. And although the toxin is destroyed by heating to 85° C. for at least five minutes, the spores formed by the bacteria are not inactivated unless the food is heated under high pressure to 121° C. for at least twenty minutes.
The incidence of foodborne botulism is extremely low. Nonetheless, the extreme danger posed by the bacteria has required that “intensive surveillance is maintained for botulism cases in the United States, and every case is treated as a public health emergency.” This danger includes a mortality rate of up to 65% when victims are not treated immediately and properly. Most of the botulism events that are reported annually in the United States are associated with home-canned foods that have not been safely processed. Very occasionally, however, commercially- processed foods are implicated as the source of a botulism events, including sausages, beef stew, canned vegetables, and seafood products.
After their ingestion, botulinum neurotoxins are absorbed primarily in the duodenum and jejunum, and pass into the bloodstream and travel to synapses in the nervous system. There, the neurotoxins cause flaccid paralysis by preventing the release of acetylcholine, a neurotransmitter, at neuromuscular junctions, thereby preventing motor-fiber stimulation. The flaccid paralysis progresses symmetrically downward, usually starting with the eyes and face, and then moving to the throat, chest, and extremities. When the diaphragm and chest muscles become fully involved, respiration is inhibited and, unless the patient is ventilated, death from asphyxia results. Classic symptoms of botulism include nausea, vomiting, fatigue, dizziness, double vision, drooping eyelids, slurred speech, difficulty swallowing, and dryness of skin, mouth, and throat, lack of fever, muscle weakness, and paralysis. Infants with botulism appear lethargic, feed poorly, are constipated, and have a weak cry and poor muscle tone. Throughout all such symptoms, the victims are fully alert and the results of sensory examination are normal.
In foodborne botulism cases, symptoms usually begin anywhere between 12 and 72 hours after the ingestion of toxin-containing food. Longer incubation periods—up to 10 days—are not unknown, however. The duration of the illness is from 1 to 10 (or more) days, depending on host-resistance, the amount of toxin ingested, and other factors. Full recovery often takes from weeks to months. And, as earlier indicated, mortality rate can be from 30% to 65%, with rates generally lower in European countries than in the United States.
Detection and treatment
Although botulism can be diagnosed based on clinical symptoms, its differentiation from other diseases is often difficult—especially in the absence of other known persons affected by the condition. Once suspected, the most direct and effective way to confirm the diagnosis of botulism in the laboratory is testing for the presence of the botulinum toxin in the serum, stool, or gastric secretions of the patient. The food consumed by the patient can also be tested for the presence of toxins. Currently, the most sensitive and widely used method for the detection of the toxins is the mouse neutralization test, which involves injecting serum into mice and looking for signs of botulism. This test typically takes 48 hours, while the direct culturing of specimens takes 5-7 days. Some cases of botulism may go undiagnosed because symptoms are transient or mild, or are misdiagnosed as Guillain-Barre Syndrome.
If diagnosed early, foodborne botulism can be treated with an antitoxin that blocks the action of toxin circulating in the blood. This can prevent patients from worsening, but recovery still takes many weeks. The mainstay of therapy is supportive treatment in intensive care, and mechanical ventilation in case of respiratory failure, which is common.
Long-Term and Permanent Injury
Although a minority of botulism patients eventually recovers their pre-infection health, the majority does not. For those who fully recover, the greatest improvement in muscle strength occurs in the first three months after the acute phase of illness. The outside limit for such improvement appears, however, to be one year. Consequently, physical limitations that still exist beyond the one-year mark are more probably than not permanent. Recovery from acute botulism symptoms may also be followed by persistent psychological dysfunction that may require intervention.
According to a recently published study that tracked the long-term outcomes of 217 cases of botulism, a large majority of patients reported “significant health, functional, and psychosocial limitations that are likely the consequences of the illness.” These limitations included: fatigue, weakness, dizziness, dry mouth, and difficulty lifting things. The victims also reported difficulty breathing caused by moderate exertions, such as walking or lifting heavy items. They were also more likely to have limitations in vigorous activities, like running or playing sports, climbing up three flights of stairs, or carrying groceries. Summarizing its finding, the study concluded that:
Even several years after acute illness, patients who had botulism were more likely than control subjects to experience fatigue, generalized weakness, dizziness, dry mouth, difficulty lifting things, and difficulty breathing caused by moderate exertion. In addition, patients reported worse overall psycho-social status than did control subjects, with patients being significantly less likely to report feeling happy, calm and peaceful, or full of pep.
There is, as a result, no question that the damaging effects of botulism are life-long.
Some background information on canning
The canning process dates back to the late 18th century in France when the Emperor Napoleon Bonaparte, concerned about keeping his armies fed, offered a cash prize to whoever could develop a reliable method of food preservation. Nicholas Appert conceived the idea of preserving food in bottles, like wine. After fifteen years of experimentation, he realized if food is sufficiently heated and sealed in an airtight container, it would not spoil. More than fifty years later, Louis Pasteur provided the explanation for effectiveness of canning when he was able to demonstrate that the growth of microorganisms is the cause of food spoilage.
An Englishman, Peter Durand, took the idea one step further and replaced the breakable glass bottles with cylindrical tinplate canisters (later shortened to “cans”). Durand did not can foods himself, but sold his patent to two other Englishmen, Bryan Donkin and John Hall, who set up a commercial canning factory. By 1813, Donkin and Hall were busily producing their first canned goods for the British army, thus continuing the connection of canning to the military.
The basic principles of canning have not changed dramatically since Nicholas Appert and Peter Durand developed the process. Heat sufficient to destroy microorganisms is applied to foods packed into sealed, or “airtight” containers. The canned foods are then heated under steam pressure at temperatures of 240-250°F (116-121°C). The amount of time needed for processing is different for each food, depending on the food’s acidity, density and ability to transfer heat.
Processing conditions are chosen and designed to be the minimum needed to ensure that the foods are made “commercially sterile,” while still retaining the greatest flavor and nutrition. The U.S. Food and Drug Administration must first approve all canning-processes. Once the cans are sealed and heat processed, the resulting canned food must maintain its high eating quality for more than two years and be safe to eat as long as the can is not damaged in any way. Historically, commercially canned food has a near-perfect track record, having caused only four outbreaks in over forty years. The last outbreak occurred in 1974 and involving beef stew.
Botulism Associated with Commercial Carrot Juice—Georgia and Florida, September 2006
On September 8, 2006, the Georgia Division of Public Health (GDPH) and CDC were notified of three suspected cases of foodborne botulism in Washington County, Georgia. On September 25, the Florida Department of Health and CDC were notified of an additional suspected case in Tampa, Florida. This report describes the joint effort.
On September 8, the three patients from Washington County, Georgia, went to a local hospital with cranial nerve palsies and progressive descending flaccid paralysis resulting in respiratory failure; the patients had shared meals on September 7. On the evening of September 8, physicians suspected foodborne botulism, notified the state health department, and collected clinical specimens for testing at CDC. On the same evening, CDC provided clinical consultation and dispatched botulinum antitoxin, which was administered to each of the patients the following morning. After receiving antitoxin, the patients had no progression of neurologic symptoms, but they remain hospitalized and on ventilators.
On September 9, the Washington County Health Department, Richmond County Health Department, and GDPH launched an investigation. The three patients had consumed several food items during their two meals together on September 7, including juice from a single 1-liter bottle of Bolthouse Farms carrot juice. The bottle had a “best if used by” date of September 18, 2006. Clinical specimens and leftover food and juice were collected and sent to CDC for testing. On September 13, botulinum toxin type A was identified in the serum and stool of all three patients. On September 15, leftover carrot juice recovered from the home of one of the patients also tested positive for botulinum toxin type A.
During September 8-15, FDA, the Georgia Department of Agriculture, the Georgia Hospital Association, and public health officials in all 50 states were notified of the outbreak and the implicated product as information became available. After these notifications, no additional cases of botulism in Georgia were reported to the state and local health departments or to CDC. During this time, FDA launched an investigation of the Bolthouse Farms, Inc., manufacturing plant in Bakersfield, California. FDA and CDC tested other bottles of the implicated brand of carrot juice, including bottles from different lots, and all were negative for botulinum toxin. Because botulinum toxin was found only in the bottle of carrot juice consumed by the three patients, a lapse in refrigeration of the carrot-juice bottle during transport or storage was suspected, which would have allowed for growth of Clostridium botulinum and subsequent production of botulinum toxin. Based on the CDC test results, on September 17, FDA issued a consumer advisory on the importance of keeping carrot juice refrigerated. However, information obtained from patient interviews regarding storage and transport of the carrot juice did not confirm mishandling by the patients.
On September 25, officials at the Florida Department of Health, the Hillsborough County Health Department, and CDC were notified that a patient had been hospitalized in Tampa, Florida, on September 16, with respiratory failure and descending paralysis. On September 28, botulinum toxin type A was identified in the patient’s serum. Circulating toxin persisted more than 10 days after illness onset in this completely paralyzed patient, indicating ingestion of a massive toxin dose. Accordingly, the patient was treated with antitoxin, which prevents binding of circulating botulinum toxin to nerve endings. The patient remains hospitalized, paralyzed, and on a ventilator. The Hillsborough County Health Department collected an open, 450-milliliter bottle of Bolthouse Farms carrot juice, which had been found by a family member in the hotel room where the patient had been staying during the month before being hospitalized. The hotel room had no refrigerator. The bottle, which had a “best if used by” date of September 19, 2006, had a different lot number than the bottle associated with the Georgia cases. On September 29, botulinum toxin was identified in carrot juice from the bottle found in the patient’s hotel room; the toxin was subsequently identified as botulinum toxin type A. The Hillsborough County Health Department and CDC notified FDA, public health officials in all 50 states, and infection-control practitioners in Hillsborough County about the botulism case and implicated product.
The carrot juice consumed by these four patients was manufactured by Bolthouse Farms, Inc., and distributed in all 50 states, Mexico, Canada, and Hong Kong with the labels “Bolthouse Farms 100% Carrot Juice,” “Earthbound Farm Organic Carrot Juice,” and “President’s Choice Organics 100% Pure Carrot Juice.” Investigations of these cases by state and local health departments and investigations of the manufacturer by FDA are ongoing. On September 29, GDPH and the Georgia Department of Agriculture recommended that Georgia residents not purchase or consume Bolthouse Farms carrot juice. The same day, the FDA warned consumers not to drink Bolthouse Farms carrot juice with “best if used by” dates of November 11, 2006 or earlier (i.e., all bottles produced before the date the warning was issued), and Bolthouse Farms issued a voluntary recall of these products.
The 2007 Castleberry Botulism Outbreak
On July 7, 2007, the Centers for Disease Control and Prevention (“CDC”) learned that two siblings in Texas were critically ill with botulism and that their illnesses were likely acquired by eating contaminated food. The two children were admitted to pediatric intensive care, and there required mechanical ventilation. The CDC released doses of botulinum antitoxin, which was administered to the children the next morning.
Four days later on July 11, public health officials in Indiana reported to the CDC that a married couple in Indiana were suspected of having foodborne botulism. Serum samples were collected from each of them on July 10 and then sent to the Botulism Reference Laboratory at the CDC. On July 16, one day after the lab received the serum samples, botulinum toxin type A was detected by mouse bioassay in the man’s serum sample. Botulinum toxin was also detected by mouse bioassay in serum submitted by the wife, but the sample volume was insufficient to determine the toxin type. Investigations conducted by state and local health departments in both Texas and Indiana revealed that all four patients had eaten types of Castleberry’s hot dog chili before symptom onset.
Texas investigators found an unopened can of Castleberry’s Austex Hot dog Chili Sauce Original date stamped with a manufacture date and time of May 7 at 9:41 p.m. at the children’s home and tested it for botulism. The Texas Department of Health Services laboratory tested an aliquot from this can using an enzyme-linked immunosorbent assay (ELISA) for botulinum toxin and did not detect the toxin.
The Indiana couple had an unlabeled, sealed plastic bag of leftover chili mixture in their refrigerator that local health officials collected and sent to the CDC for C. botulinum toxin testing. On July 16 the CDC detected botulinum toxin type A by mouse bioassay in the chili mixture. Empty, well-rinsed cans of Castleberry’s Hot Dog Chili Sauce Original and chili made by another company were found in the couple’s recycling bin. CDC re-rinsed the two cans and tested the rinse water for botulinum toxin by mouse bioassay; both were negative. The label on the can of Castleberry’s Hot Dog Chili Sauce Original indicated a production-date of May 8, and a time of 2:23 AM—less than five hours after the production-time indicated on the can collected from the Texas home.
On July 17, CDC staff provided information regarding the production-dates and times to the FDA. The evidence strongly suggested that brands of Castleberry’s hot dog chili sauce were the common source of the four ill persons with botulism. On July 18, FDA issued a consumer advisory. On that same day, after being informed about the outbreak, and findings from the FDA investigation of the canning facility, Castleberry’s Food Company issued a voluntary recall that included a limited number of production dates of Castleberry’s Hot Dog Chili Sauce Original, Castleberry’s Austex Hot Dog Chili Sauce Original, and Kroger Hot Dog Chili Sauce. The recall was expanded on July 21 to include all production dates for 91 types of canned chili sauce, chili, other meat products, chicken products, and dog food that were manufactured in the same set of cookers, or “retorts” as the hot dog chili sauce at the Castleberry’s facility in Augusta, Georgia.
By August 24, eight cases of botulism had been reported to the CDC. In addition to the Indiana couple, the mother of the children in Texas had developed symptoms of botulism, which brought the total number of Castleberry-associated cases in Texas to three. There was also three unrelated residents of Ohio who had developed botulism consuming Castleberry’s hot dog chili sauce in the week before symptom onsets. Botulinum toxin was identified in leftover chili sauce collected from the refrigerator belonging to one of the Ohio cases.
The Castleberry’s manufacturing facility in Georgia produces products regulated both by the FDA and USDA-FSIS. Initial reports of illnesses were linked to meatless hot dog chili sauce and thus, fell under the jurisdiction of the FDA. The agency’s Atlanta District Office took the lead in the investigation of facilities.
The inspection started on the evening of July 17. FDA investigators requested company maintenance records, which were not immediately available because they were stored on a laptop of a vacationing employee. Finally, three days later, under threat of severe penalty, the company produced some of the requested records. Included in records provided to federal investigators was a 42-page report written by a consultant hired by Castleberry’s to investigate swollen cans of stew, chili, and hash produced in April and May 2007. The consultant had attributed spoilage to post-process handling operations in one of the plant’s cooking equipment. Reports by two other company-hired consultants would also implicate post processing as the reason for swollen cans. Unfortunately, Castleberry’s had not investigated the issues further.
On July 18 and 19, a team of federal investigators were sent to the firm’s warehouse. Samples of Castleberry’s Austex and Castleberry’s brand Hot Dog Chili Sauce with the “best by May 7, 2009” and “best by May 8, 2009” lot codes were collected and sent to FDA laboratories for testing. FDA testing of sample 428113, consisting of 17 swollen cans, found C. Botulinum toxin in 16 of the cans. This sample included the same time-stamp and lot code from the May 8, 2007 production as the can found in the Indiana home. FDA testing of sample 420352, consisting of six swollen cans, found C. Botulinum in four cans. FDA sample 420353 included one swollen can, and its contents tested positive for C. Botulinum toxin.
Federal investigators conducted extensive tests on Castleberry equipment. The findings are presented in an FDA report issued on August 10, 2007, Attachment No. 1, FDA Inspectional Observations dated 08/10/2007, (Summary pages only). Noted observations include:
The system, equipment, and procedures used for thermal processing of foods in hermetically sealed containers were not operated and administered in a manner that ensures commercial sterility is achieved.
Each retort did not have an accurate temperature records device.
Failure to supply a suitable water valve used for water cooling to prevent leakage of water into the retort during processing.
The condensate bleeder was not checked with sufficient frequency to ensure removal of condensate or equipped with an automatic alarm system for the continuous monitoring of condensate bleeder functioning.
Required information was not entered on designated forms at the time the observation was made by the retort or processing system operator or designated person.
Failure to maintain fixtures in repair sufficient to prevent food from becoming adulterated.
Failure to properly adjust the temperature-recording device. The temperature recorded on the temperature-recording device chart was higher than the mercury-in-glass thermometer during processing.
The report ultimately placed blame on Castleberry management saying there was no commitment from employees in making the products and there was not adequate management oversight. As one Castleberry employee noted: “Two years ago the [implicated retorts] were maintained very well, but they are maintained poorly now.” The FDA plainly agreed, citing Castleberry’s for the “failure to maintain fixtures in repair sufficient to prevent food from becoming adulterated.”
Castleberry made substantial fixes at its plant and then reopened in the fall of 2007. The company re-branded its line to American Originals, and redesigned product labels. But in March, 2008, the plant was forced to close again after a February 27 joint-inspection by the FDA and USDA revealed deviations in some equipment operations on the processing line. The line was not related to deficiencies noted in the summer of 2007 but because under-processing caused the botulism outbreak, the plant’s operating permit was suspended.
The 2014 Villa Romano Green Farms Botulism Outbreak
In late May 2014 John Napierski, purchased seven jars of VR Greens Farms (VRGF) Basil Pine Nut Pesto at a Farm Stand operated at the Bella Collina Towne and Golf Club in San Clemente, California. While on a road trip east, Mr. Napierski gave two jars to friends in Denver, Colorado. He then continued his trip to Ohio and gave two jars to his daughter, Kathryn (“Katy”), who was a nursing student working and attending college in Cincinnati. Katy and her friend, Arielle Allen, used a portion of one jar of pesto as an ingredient in a chicken pasta dish they cooked at home and shared on July 13. On July 15 Katy complained of a sore throat and difficulty swallowing. Arielle started to have similar symptoms on July 17. Over the next ten days both women continued to experience neurological symptoms. Both women had multiple medical encounters before botulism was suspected as the cause of their symptoms. Katy was admitted to Bethesda North Hospital on July 17 and transferred to the University of Cincinnati Medical Center on July 18. Arielle was admitted to the University of Cincinnati Medical Center on July 27 due to worsening bulbar and facial weakness. Arielle’s admission to the hospital prompted the attending neurologist to note her friendship with Katy and similarity in symptoms between the two women. He diagnosed both Katy and Arielle as having suspected botulism and notified public health authorities. Botulism antitoxin was obtained from the Centers for Disease Control and Prevention (CDC) and administered to Arielle on the evening of July 28. Serum and stool collected from Arielle and Katy did not test positive for C. botulinum. The toxin, however, was found in pesto sauce leftover from the chicken pasta meal.
Investigators at the City of Cincinnati Health Department and the Ohio Department of Health quickly determined that Katy and Arielle had shared a meal of pasta with chicken and jarred pesto sauce. During a visit to Arielle’s apartment, investigators found leftover chicken pasta with pesto in the apartment refrigerator. This was collected for laboratory testing for the presence of Clostridium botulinum toxin as was an unopened jar of pesto that Katy had. On July 29 Ohio investigators notified the CDC, the Food and Drug Administration (FDA), and the California Department of Public Health (CDPH) Food and Drug Branch (FDB) that two Ohio residents had botulism and that the suspected source was VRGF Basil Pine Nut Pesto. CDPH FDB contacted Dominic Romano, owner of VRGF, and informed him of the illnesses.
On July 30 California investigators conducted a site visit at the VRGF Farm Stand. A variety of canned products were produced seasonally and sold at the farm location. Most of the products sold at the farm stand were produced at unregistered/unpermitted locations. Mr. Romano was advised that he must immediately cease the unlicensed manufacturing and sale of low-acid canned and acidified foods. A Notice of Violations was issued to Mr. Romano for lack of license/registration. The firm initiated a voluntary recall of all suspect low-acid canned and acidified foods. The California Department of Public Health issued an alert on July 30 advising consumers to not eat VR Green Farms jarred products because of improper production making them susceptible to contamination with Clostridium botulinum.
California investigators learned that in April or May the pesto had been made by Rose Schwinn dba Rose’s Artesian Creations. Ms. Schwinn was a family friend of Dominic Romano. According to Mr. Romano only 10-12 jars were produced and were intended to be a test product. This was later found to be inaccurate. On July 31 CDPH FDB investigator, Melissa DeHart, contacted Ms. Schwinn to discuss manufacturing processes. Ms. Schwinn reported that she manufactured the product in her home kitchen and that she had made small batches products sold at the Farm Stand “on and off for a few years.” She did not maintain a Processed Food Registration or a Cannery License with CDPH as required to manufacture these types of foods for retail sales.
Rose Schwinn described the process used to make the pesto sauce. Raw garlic cloves and salt were ground in the food processor. Fresh basil leaves and olive oil were added and then mixed with pine nuts and parmesan cheese. The ingredients were processed in small batches and added to one large pot due to limited size of the food processor. The product could sit for up to one hour at room temperature before it was filled into the jars.
New jars were cleaned by placing them in her household dishwasher on the hot cycle with dish detergent and bleach. The jars were then filled with water and place in the microwave until boiling. The lids were maintained in hot water until use. The ingredients were mixed together without a heat step to form a sauce and then filled into hot mason jars. Lids were applied and the jars were placed into a stove top water bath canning unit. The water in the canning unit was brought to a boil and the product was heated. A thermometer was not used. The jars were allowed to cool, the seal around the lid checked, and the product was labeled for distribution. The label did not include a complete ingredient statement, lot code, best by date, or a “Perishable Keep Refrigerated” statement. CDPH FDB described the manufacturing process to be conducted under “insanitary conditions at a home residence.”
The CDPH Food and Drug Laboratory Branch (FDLB) collected an unopened jar of VRGF Basil Pine Nut Pesto from Rose Schwinn. The sample was tested for pH, water activity, and Elisa screening for C. botulinum. Test results showed for sample #062080514, the pH was 5.3 and water activity was 0.965. Non-refrigerated foods that are packed in hermetically sealed jars with a pH above 4.6 and water activity above 0.85 are at risk for supporting C. botulinum toxin formation and must be manufactured in accordance with an approved scheduled process, controls and in California pursuant to a Cannery License. Clearly, VRGF Basil Pine Nut Pesto did not meet the minimum requirements for food safety. Investigators determined that VRGF Basil Pine Nut Pesto placed “consumers of the product at risk for C. botulinum toxin illness.”
State public health laboratories in Ohio and California tested several samples of the pesto. The Ohio Department of Health Bureau of Public Health Laboratories tested an unopened jar collected from Katy as well as leftover chicken pasta with pesto found in Arielle’s apartment. The left over pasta meal was positive for Clostridium botulinum toxin type B. The unopened jar of pesto sauce tested negative for Clostridium botulinum toxins. Of the two jars that had been dropped off in Colorado, one jar had been consumed with no ill effects. The second jar had a swollen lid and was shipped to Ohio for C. botulinum testing. This jar also tested negative for C. botulinum toxins. CDPH FDLB also tested an unopened jar of pesto collected from John Napierski. This jar showed low levels of C. botulinum toxin B by Luminex system testing and “borderline” testing results by Elisa but definitive testing by the mouse bioassay was negative.