In March 2017, the Centers for Disease Control and Prevention (CDC) and several state health departments attributed a multi-state outbreak of Shiga toxin-producing Escherichia coli O157:H7 to I.M. Healthy brand SoyNut Butter manufactured by Dixie Dew, sold through the World Finer and KeHe distribution network and sold at retail at Target and other retailers.
Outbreak investigators collected open containers of SoyNut Butter from the homes of sick people, and unopened containers from retail locations. Containers of SoyNut Butter from lots #243162 and 244161 tested positive for E. coli. Whole genome sequencing revealed that the same strain of E. coli was found in clinical isolates from sick people and containers of I.M. Healthy SoyNut Butter. Epidemiologic investigation determined that 32 people ill with this strain of E. coli had been infected by eating or attending a facility that served I.M. Healthy SoyNut Butter. This included residents of Arizona (4), California (5), Florida (2), Illinois (1), Massachusetts (1), Maryland (1), Missouri (1), New Jersey (1), Oregon (11), Virginia (2), Washington (2), and Wisconsin (1).
During the outbreak, investigators identified 2 ill people who either developed HUS or had a culture independent diagnostic test (CIDT) showing infection with STEC bacteria. In interviews, both patients reported eating I.M Healthy SoyNut Butter in the week before the illness. However, the CDC did not include these people as case patients because no bacterial isolates were available for molecular subtyping, so there were unable to confirm if they were infected with one of the outbreak strains.
On March 7, 2017, The SoyNut Butter Company recalled all varieties of I.M. Healthy SoyNut Butters and all varieties of I.M. Healthy Granola products. On March 10, 2017, The SoyNut Butter Company expanded its recall to include Dixie Diner’s Club brand Carb Not Beanit Butter. On March 24, 2017, Pro Sports Club recalled 20/20 Lifestyle Yogurt Peanut Crunch Bars because they contain a recalled ingredient. However, I.M. Healthy SoyNut Butter continued to be sold at least through early September 2017.
An outbreak strain of STEC O157 was isolated from 11 I.M Healthy SoyNut Butter samples. Multiple STEC isolates were identified from some samples. Nine samples were from opened, leftover products from case patient homes in California, Oregon, and Washington, and 2 samples were from unopened containers from retail stores in California; all had best-by dates of August 30, 2018 (10 products) or August 31, 2018 (1 product).
On March 3, 2017, the FDA issued a warning about the presence of E. coli O157:H7 in I.M. Healthy Creamy SoyNut Butter with a Best Buy Date of 08/30/2018. Outbreak investigators identified Lot No. 243162 as one of the lots that was contaminated with E. coli O157:H7.
What the FDA found
The FDA inspected the facility between March 3 and 15, 2017. On March 3, 2017, Dixie Dew refused to allow FDA investigators access to the facility’s environmental sampling and production records; the FDA subsequently issued a Demand for Records under section 414 of the Federal Food, Drug, and Cosmetic Act. After receiving the Demand for Records, Dixie Dew provided FDA investigators with the necessary records. At the close of the inspection, the FDA provided Dixie Dew with a list of the investigators’ inspectional observations (Form FDA 483), noting objectionable conditions seen during the inspection. Dixie Dew responded to the report in writing with a list of actions it had taken to correct the conditions; however, FDA found the corrective actions were not adequate to fully address the risks that were identified and issued the Suspension Order to prevent further illnesses from occurring.
The FDA announced on March 28, 2017, the FDA used authorities granted under the 2011 FDA Food Safety Modernization Act to suspend the food facility registration of Dixie Dew Products, Inc. (Dixie Dew) of Erlanger, Kentucky, because products manufactured in this facility may be contaminated. The FDA’s decision to suspend the registration of Dixie Dew Products was prompted by the E. coli O157:H7 outbreak and the findings of FDA’s March 2017 inspection of Dixie Dew, which identified insanitary conditions that could lead to contamination with E. coli O157:H7 in finished products. The FDA determined that no food could leave the Dixie Dew facility for sale or distribution while the food facility registration was suspended.
Specific problems noted in the suspension order and Form 483 included (blanks reflect redacted information):
- investigators observed grossly insanitary conditions that cause your firm’s soy nut butter products to be adulterated;
- food contact surfaces, floors, walls, and ceilings in the soy nut butter processing and packaging rooms were heavily coated with soy nut butter build-up from previous production runs;
- firm does not routinely wash and sanitize smaller pipes, pipe fittings, gaskets, seals, “or the rubber _____ plug” when broken down following a production run;
- firm does not conduct a kill step for SoyNut Butter product remaining in your firm’s mixing kettle leftover from a production run;
- plant Manager stated, up to _____ may remain in the kettle overnight or weekend prior to resuming production. You and your Plant Manager stated the kettle is shut off when product remains in the kettle overnight and/or over the weekend;
- plant manager and maintenance supervisor reported your _____ machine, used for fine mixing of the SoyNut Butter and ________, routinely shuts off during processing. Your Plant Manager stated this occurs one to two times per day and, this problem has persisted for approximately 15 years despite repeated maintenance intended to correct the problem;
- firm monitors the SoyNut ______ with a ______ thermometer, but plant manager stated he has never verified the accuracy of this instrument;
- you and your plant manager report, your temperature probe and chart recorder, initially engineered to verify and record _____ of product in the large mixing kettle, is not functioning properly and has not been used for well over a year.
FDA inspectors also noted problems with Dixie Dew’s food safety testing program, noting the company’s “failure to perform microbial testing where necessary to identify possible food contamination.” Inspectors found the testing materials on hand at Dixie Dew had expired in July 2016 and October 2015.
Problems in the Dixie Dew quality control lab were described in detail by FDA inspectors.
“An apparent fly infestation in your firm’s Quality Control and Product Development Laboratory was observed on 3/13/2017. Small apparent flies and fly larvae, too numerous to count, were inside an unplugged chest freezer,” according to the 483 report.
“A sealed blue plastic bag was inside the freezer and according to your plant manager, contained an egg product that became rotten when power was disconnected. The small apparent flies were observed along the laboratory counters and flying throughout the laboratory.”
Linda J. Harris, Ph.D., a well-known and respected expert from the University of California at Davis, critiqued the failure of Dixie Dew to have an adequate plan to control for the risk of bacterial contamination. Specifically, after visiting the facility, Dr. Harris commented:
The Dixie Dew documents and especially the FDA 483 report based on inspections conducted March 3 to 15, 2017 as well as the onsite tour of the facility May 9, 2019 clearly show that Dixie Dew had not implemented either basic Good Manufacturing Practices or best practices for low moisture foods. Outbreaks of foodborne illness from nut butters in the U.S. in 2006/2007, 2008/2009, 2013, and 2014 are well known among food industry professionals and food safety community. These outbreaks are frequently used as instructional tools that provide multiple examples of what not to do when producing food. The outbreaks have been influential in changing the way that the microbial safety of low moisture foods are viewed and have led to well documented and freely shared industry best practices. In 2016, IM Healthy and those buying from them should have been aware of the risks of foodborne pathogens (both Salmonella and E. coli O157:H7) in their products. Any reasonable audit or inspection would have identified substantial systemic food safety issues in the production of Soynut butter at Dixie Dew.
The issues were there to be seen.
PAST OUTBREAKS LINKED TO NUT BUTTERS
It is not as if, in 2017, contaminated nut butters were not a foreseeable issue for manufacturers, suppliers and retailers.
In November 2006, public health officials detected a substantial increase in reports of Salmonella Tennessee isolates. In February 2007, a multistate, case-control study linked the consumption of either Peter Pan or Great Value Peanut Butter brands to infection. As a result of that outbreak, 715 people were sickened and 129 required hospitalization. Subsequently the same strain of Salmonella Tennessee was isolated from unopened jars of peanut butter and from environmental samples collected from the processing plant. The product was recalled, and new illness reports declined. Unsanitary conditions at the Sylvester, Georgia, processing plant were known about since 2004. On April 5, 2007, ConAgra announced that inadvertent moisture from a leaking roof and sprinkler system could have promoted bacteria growth in the plant. Great Value brand was sold at Walmart stores.
Beginning in November 2008, CDC PulseNet staff noted a small and highly dispersed, multistate cluster of Salmonella Typhimurium isolates. The outbreak consisted of two pulsed field gel electrophoresis (PFGE) defined clusters of illness. The first cluster displayed a unique primary enzyme (XbaI) restriction pattern and an uncommon secondary enzyme (BlnI) pattern. The second cluster had two closely related XbaI patterns that were very similar to the first cluster and a BlnI pattern that was indistinguishable from the first cluster. Illnesses continued to be revealed through April 2009, when the last CDC report on the outbreak was published. A total of 714 were sickened, with 171 hospitalized, and at least nine deaths. Peanut butter and peanut butter containing products produced by the Peanut Corporation of America plant in Blakely, Georgia, were implicated. King Nut brand peanut butter was sold to institutional settings. Peanut paste was sold to many food companies for use as an ingredient. Implicated peanut products were sold widely throughout the USA, 23 countries, and non-U.S. territories.
On September 22, 2012, the CDC announced a multistate outbreak of Salmonella serotype Bredeney linked to Trader Joe’s Valencia Creamy Salted Peanut Butter. Collaborative efforts by local, state, and federal public health and regulatory officials traced the product to Sunland, Inc., a Portales, New Mexico company. Sunland issued a recall of multiple nut butters and products made with nut butters. When the outbreak was declared over, a total of 42 people infected with the outbreak strain of Salmonella serotype Bredeney had been reported by 20 states. Among persons for whom information was available, illness onset dates ranged from June 14, 2012 to September 21, 2012. Ill persons ranged in age from less than 1 year to 79 years, with a median age of 7 years. Sixty-one percent of ill persons were children less than 10 years old. Among 36 persons with available information, 10(28%) patients had been hospitalized. The FDA confirmed that environmental samples collected at the Sunland facility had a DNA fingerprint that was indistinguishable to the DNA fingerprint found in outbreak associated patients.
On August 21, 2014, the CDC announced a multistate outbreak of Salmonella Braenderup involving 6 people residing in Connecticut (1), Iowa (1), New Mexico (1), Tennessee (1), and Texas (2). Almond and peanut butter manufactured by nSpired Natural Foods, Inc. was named as the likely source of this outbreak. The outbreak was declared over on October 16, 2014. Illness onset dates range from January 22, 2014 to May 16, 2014. Among 5 ill persons with available information, one person reported being hospitalized. During inspections at the nSpired Natural Food facility in Ashland, Oregon, between January 2014 and August 2014, the FDA isolated Salmonella Braenderup from environmental samples. A search of the PulseNet database linked ill patients to the environmental isolates taken from the nSpired production plant. On August 19, 2014 nSpired Natural Foods issued a voluntary recall of certain lots of almond and peanut butters because of potential contamination with Salmonella. The recalled brands include Arrowhead Mills, MaraNatha, and specific private label almond and peanut butters.
On December 2, 2015, JEM Raw Chocolate LLC (JEM Raw) of Bend, Oregon announced a recall of its full line of all nut butter spreads due to possible contamination with Salmonella. Health authorities at the FDA, Oregon Health Authority, Oregon Department of Agriculture and the CDC had linked illnesses in 13 persons who consumed nut spreads. Dates of onset ranged from July 18, 2015 to November 22, 2015. Cases were reported from California, Colorado, Georgia, Hawaii, Idaho, Illinois, Maine, North Carolina, New Jersey and Oregon.
 32 cases from 12 states. Twenty-six (81%) cases occurred in children,18 years old; 8 children developed hemolytic uremic syndrome. Twenty-five (78%) case patients ate the same brand of soy nut butter or attended facilities that served it. We identified 3 illness subclusters, including a childcare center where person-to-person transmission may have occurred. Testing isolated an outbreak strain from 11 soy nut butter samples. Investigations identified violations of good manufacturing practices at the soy nut butter manufacturing facility with opportunities for product contamination, although the specific route of contamination was undetermined. See, A Multistate Outbreak of E Coli O157: H7 Infections Linked to Soy Nut Butter – PEDIATRICS Volume 144, number 4, October 2019:e20183978.
 A 1996 Salmonella Mbandaka outbreak linked to peanut butter sickened at least 15 in Australia – Aust NZJ Public Health 1998; 22: 536-9.
See also – ATTACHMENT NO. 2 – J.-Pediatrics-Article-02178215xAD20B, ATTACHMENT NO. 5 – Suspension-of-Food-Facility-Registration-Order-to-Dixie-Dew-Products–Inc., ATTACHMENT NO. 6 – Dixie-Dew-Products-Inc.-Erlanger–KY.-483-Dated-03-15-17