Thanks to the New York Times and Matt Richtel for “Tainted Pork, Ill Consumers and an Investigation Thwarted.”

Like the story of another one of my clients by Michael Moss, “The Burger that Shattered Her Life,” I smell another Pulitzer Prize.

It is good to put human faces on how important food safety is.

Here is a bit more of the Porter story from my files and a different spin on the dangers of Salmonella:

The Porter Family and Salmonella I 4,[5],12:i-:

On the afternoon of June 28, 2015, Rose and Roger Porter hosted a going away party at their home in Rainier, Washington. The Porters planned on moving to Costa Rica the following day, so they wanted to celebrate with their family and friends one last time.

On June 27, Rose Porter picked up a whole hog from Stewart’s Meats in McKenna, Washington. The next day, Rose cooked the pig just the way she was told to by Stewart’s. Hours later, the Porters’ home was filled with friends and family, none of whom had any idea that many of them were about to become seriously ill with Salmonella poisoning. It all seemed so easy and  matter-of-fact in retrospect, as Rose recalls:

When [the whole roasted hog] was done, I served it up. After everyone left, I cleaned everything up and threw out any food that was left over. We packed everything up and went to bed. The next day, I woke up with explosive diarrhea. I had a very busy day because we were packing up to move to Costa Rica. I had to get out of our house because we had renters coming in. I had to find us a hotel and I was dealing with my daughter not feeling well at all. She went with me for the day because she wanted to sleep in a bed at a hotel. I had to stop every half hour to use the bathroom. The diarrhea kept up.

Once Rose and Mikayla arrived at the hotel, all Mikayla could do was lie down and watch television. She fell asleep at 6 PM. By 2:30 AM, she was up and vomiting. Mikayla woke her mom up and, at 4:30 AM on June 30, they both headed to Providence St. Peter Hospital in Olympia, Washington. Joseph Pellicer, MD was on duty in the emergency hospital and listed Mikayla’s chief complaints as “abdominal pain, emesis, diarrhea, and fever.” Rose explained that Mikayla had been sick since the morning before with severe diarrhea. By the evening, Rose stated that Mikayla “felt like she was on fire,” although she did not have a thermometer to measure her temperature due to the move. Mikayla also described having shaking chills with fever and Rose told Dr. Pellicer that she, herself, was having similar symptoms. Mikayla was miserable, wracked with body aches and pain that radiated up into both of her shoulders.

Dr. Pellicer did an exam and found Mikayla tachycardic with a heart rate of 125 and a diffusely tender abdomen. The doctor also observed that Mikayla was dehydrated with turbid urine, ketonuria, proteinuria, and dry mucus membranes. Despite these clinical symptoms, no cultures were sent to the lab and no stool sample was collected. Dr. Pellicer diagnosed Mikayla with “acute gastroenteritis.” Just after 8 AM, he discharged Mikayla from the ER with a prescription for an antiemetic drug and clearance to travel to Costa Rica.

On July 2, 2015, the Porters landed in Costa Rica. Mikayla was still suffering from frequent bouts of diarrhea. Upon logging in to a social media website, Rose discovered that a party attendee’s daughter was being hospitalized for Salmonella poisoning. Rose decided to take her daughter to the local ER—Beach Side Emergency Clinic in Santa Cruz Guancaste. Andrea Messeguer, MD, the medical director of the clinic, evaluated Mikayla and noted that she was lethargic with persistent abdominal pain in the periumbilical area. Because Mikayla was currently afebrile and able to orally hydrate, Dr. Messeguer told Rose she could watch her daughter at home.

Over the next day, Mikayla did little but drink ice water, sleep, and go to the bathroom. Unfortunately, things soon took a turn for the worse. Rose recalls:

She started crying in the bathroom that she could not bear the stomach pains anymore and needed to go back to the doctor. She told me that she had blood coming out of her butt, that it had been that way for a while, and that she didn’t know what to do. The amount of time between her going to the bathroom went from every 20 to 30 minutes to every five to 10 minutes. She was screaming in pain in the bathroom. She said that she felt like someone was stabbing her over and over again in the stomach.

On July 3, Rose brought Mikayla back to see Dr. Messeguer at the urgent clinic and told the doctor that there was now mucus and blood in her daughter’s stools. Dr. Messeguer examined Mikayla and performed a stool smear and culture. While at the clinic, Mikayla’s diarrhea decreased in frequency and she was still holding down fluids, so the doctor diagnosed her with “bacterial gastroenteritis” until proven otherwise and sent her home.

It was not long before it was clear that Mikayla’s condition was deteriorating. By the morning of July 4, her stools were entirely bloody. Rose, once again, rushed her back to the urgent care clinic. Upon their arrival, Dr. Messeguer asked to speak to Rose privately. She informed her that Mikayla was losing a lot of blood and may need a blood transplant. However, the clinic did not have the equipment or resources necessary to perform the procedure. Dr. Messeguer told Rose that her daughter could die on the four- to five-hour drive to Hospital CIMA San Jose, and therefore, Mikayla would need to be airlifted there.

Rose and Mikayla were both transported by helicopter to Hospital CIMA San Jose in Costa Rica. According to a memorandum written by Luis Picado, MD, Mikayla presented with a high-grade fever, bloody stools, general malaise, and moderate dehydration. He wrote, “On admission, she presented with clear signs of bacterial gastroenteritis and required intravenous rehydration and parenteral antibiotics to control the infection. Stool studies were positive for Salmonella.”

Rose does not require a formal medical record to recall how things went for her daughter over the next several days. The memory is still fresh in her mind:

For the next three days, I sat back and watched as my daughter cried in pain. I changed her bloody sheets when she couldn’t make it to the bathroom. I didn’t sleep for the first couple night because I was so scared that she wouldn’t wake up. [Mikayla] couldn’t process food or water. The doctor told me that the bacteria had gotten into her system and shut it down completely. When she ate or drank, it would go straight through her. She wasn’t getting any nutrition or hydration.

The good news is that she is out of the hospital now. We have cut all pork out of our diets and are fearful of chicken and eggs. I have dealt with a husband over in Afghanistan and this was still the scariest thing I have ever been through. I can’t say that I know what it is like to have a child die, but I do know what it is like to see a child on their deathbed.

I have spent the last couple of months going over every detail that has happened over those two weeks. I felt totally responsible when this happened. I had to question all of my decisions as a mother. I felt like I poisoned my own child and everyone else that ate at my house. I lost friends from all of this. It was weeks later that I found out that, in the end, it wasn’t my fault.

During the time of Mikayla’s illness, Rose and Roger had their own Salmonella illnesses to contend with. On the helicopter ride to the hospital in San Jose, Rose’s blood pressure plummeted and she lost consciousness. Roger had gastroenteritis with uncontrollable diarrhea for several days. Rose and Roger still suffer from periodic bouts of diarrhea to this day.

The Porters were three of 152 diagnosed victims of a nationwide outbreak of multidrug resistant Salmonella I 4,[5],12:i:-. Stewart Meats’ distributor of whole hogs was none other than Kapowsin Meats. Laboratory testing of environmental samples at Kapowsin Meats by the Washington State Department of Health confirmed the presence of Salmonella I 4,[5],12:i:- in the facility. As a result of the investigation, Kapowsin Meats voluntarily recalled  523,380 pounds of pork products.

Salmonella in Beef and Pork – A Public Health Threat

Salmonella illnesses and outbreaks are commonly attributed to raw meat and by-products of beef and pork. Between the years 1973 and 2011, one hundred of nearly 2,000 Salmonella outbreaks in the United States were traced back to beef, leading to 3,684 illnesses.^[1] Salmonella is omnipresent in feedlot cattle. A 2019 epidemiological study has revealed that 9.2% of cattle and 18.2% of beef contain the pathogen.[2] Another recent study has estimated that the Gram-negative bacteria is present in up to 16% of North American cattle.[3] In a 2007 study by Stephens et al., Salmonella was isolated from all of the animals sampled, while Escherichia coli O157:H7 was only isolated from 42.5% of the animals.^[4] Notably, 94% of oral cavity samples, 94% of hock samples, 88% of perineum samples, 86% of ventrum samples, 76% of back samples, and 74% of flank samples tested positive for Salmonella.

Contaminated pork also accounts for numerous foodborne Salmonella infections in the United States.^[5] The 2015 annual report on foodborne illnesses in the U.S., published by CDC, revealed that pork meat was the second most important source of foodborne Salmonella outbreaks.^[6] In pork meat, pigs and swine, and the swine farm environment, the prevalence of Salmonella is 39.6%, 17.7%, and 7.9%, respectively.[7]

Cargill, Inc., the largest private corporation in the United States,[8] has been implicated in several Salmonella outbreaks, particularly in ground beef and turkey products. In 2012, Salmonella Enteritidis-tainted ground beef produced by Cargill sickened 40 people in eight states. In August of 2011, Cargill Meat Solutions recalled 36 million pounds of Salmonella-contaminated ground turkey after 136 persons from 34 states fell ill. In 2009, Salmonella-tainted ground beef produced at Beef Packers, a California-based plant owned by Cargill, sickened 68 people in 15 states.

The industry giant generates a large portion of its 115 billion-dollar yearly revenue from the manufacture and sale of USDA-regulated products including meat, poultry, and egg products. Cargill supplies nearly a quarter of the domestic meat market. All eggs used in U.S. McDonald’s restaurants pass through their plants. It is safe to say that Cargill, Inc. has dealt with and felt the repercussions of foodborne illness. It is also safe to assume that Cargill has little financial incentive to advocate for more stringent food safety measures. However, Cargill has and continues to publicly promote the implementation of more modern, science-based measures.

In 2014, the Pew Charitable Trusts, a non-profit, non-governmental organization, partnered with Cargill, Inc. to develop a set of recommendations to “improve the food-safety oversight system for meat and poultry” and to “transform the current system into one that is more science- and risk-based.”^[9] The two companies enlisted Meridian Institute to design and facilitate a multi-stakeholder dialogue process, in which 20 high-ranking persons from different industry sectors would participate. Appendix A of Meridian Institute’s final report, published in June of 2017, identifies these participants—among them: Todd Bacon, Senior Director of Quality Systems (U.S. Supply Chain Management) for McDonald’s Corporation, Jon Hixson, Vice President of Corporate Affairs for Cargill, Mike Robach, Vice President of Corporate Food Safety (Quality and Regulatory Affairs) for Cargill, and Rick Roop, Senior Vice President of Food Safety and Quality Assurance for Tyson Foods. [10]

The final report also discloses the results of the dialogue. The executive summary states, “Cargill, Inc., and the Pew Charitable Trusts identified the following reasons for believing that the time was ripe for this initiative:

• Public-health-based: while there has been some progress, meat and poultry products remain significant vehicles for foodborne illnesses in the United States;
• Science-based: the inspection system developed more than 100 years ago does not employ the most science-based means to protect consumers from pathogenic contamination;
• Fiscal: taxpayers spend $1 billion each year on an inspection system that cannot effectively assure the desirable level of safety.”[11]

The 20 participants, from Cargill, McDonald’s, Tyson Foods, Hormel Foods, The Kroger Company, Keystone Foods, and Gunthorp Farms, among others, also discussed the state of the current regulatory system overlooking meat and poultry products in the United States. The report states that “many critics of the current meat and poultry oversight system believe that [the laws currently in place] are the major obstacles to significant reductions in foodborne disease linked to meat and poultry because they are outdated and inflexible.” Indeed, the current inspection activities, which are the same ones performed over a century ago, are vastly inadequate. At the beginning of the twentieth century, the largest food-safety risks—brucellosis, tuberculosis, and trichinellosis—could be detected and controlled using the “poke and sniff” method. However, as previously stated, Salmonella contamination cannot be detected organoleptically.

Salmonella is naturally occurring in the lymph nodes and intestinal tract of swine, steers, heifers, bulls, and cows raised for meat production. Numerous studies have revealed that beef-producing animals harbor Salmonella in various lymph nodes, particularly in deep tissue lymph nodes (DTLNs) such as iliofemoral, subiliac, and superficial cervical lymph nodes.^[12] A 2019 intervention study indicated that the prevalence of Salmonella in mesenteric, subiliac, mandibular, and mediastinal lymph nodes of cattle was 91.2%, 76.5%, 55.9%, and 7.4%, respectively.^[13] The probability of encountering Salmonella in swine lymph nodes is much lower. The prevalence of Salmonella in ileocecal, ventral thoracic, and subiliac lymph nodes of swine is 43.6%, 0.4%, and 0.4%, respectively.

Because deep tissue lymph nodes are embedded in the adipose tissues of cattle and swine, they are difficult to remove, more likely to be incorporated into ground meat, and thus more likely to cause contamination when compared to gut-associated lymph nodes.^[14] Additionally, Salmonella harbored in DTLNs are protected from traditional antimicrobial carcass surface interventions. Therefore, Outbreak Serotypes of Salmonella in ground meat products represent a significant safety hazard and are ordinarily injurious to consumers’ health.

Ground or minced meat products represent a significant hazard to public health. Research shows that 90% of salmonellae in a 2000-pound ground beef production lot originate from DTLN contamination, with relatively little contribution from carcass surface contamination.^[15] Overall, ground meat is much more susceptible to contamination than other types of meat. A single package of ground beef or pork may contain tissues from hundreds of animals, therefore, the probability of inclusion of contaminated tissues is high. During the grinding process, harmful pathogens can be transferred from contaminated to uncontaminated regions, further increasing the probability of contamination.

While gut-associated and deep tissue lymph nodes may contain Salmonella, the muscle masses of healthy cattle and swine are sterile with the exception of small amounts of Clostridia.^[16] Therefore, bacterial cross-contamination of intact muscle products must occur from extrinsic sources (e.g. lymph nodes, gastrointestinal tract, and external carcass surfaces) during the slaughtering process. Because the presence of Salmonella in meat end products is a result of cross-contamination, Salmonella is an “added substance” in whole muscle beef and pork per 21 U.S.C. § 601(m)(1).

Two of the slaughtering steps of cattle and swine, dehiding and evisceration, are particularly likely to cause cross-contamination and introduce harmful pathogens to whole muscle end products. In a study by Fegan et al., Salmonella was isolated from 68% of cattle hides in an abattoir.^[17] A larger study reported the results of numerous samplings; in nearly 100% of cases, cattle hides tested positive for the presence of Salmonella.^[18] The study, conducted by Narvaez-Bravo et al., also determined that there was a positive correlation between the prevalence of Salmonella on the hides and the prevalence of the pathogen on the carcasses. The dehiding, or skinning, process is considered to be the primary contamination factor of cattle carcass surfaces. Similarly, hide removal is a significant source of contamination in the pork production chain. A 2013 report published by the National Pork Board states that “[the hide removal process] offers many opportunities to contaminate the carcass, in part because there is no prior treatment of the hide to remove contamination. As a result, the mechanical process of removing the hide may result in sporadic, random contamination of the edible tissue underneath.”^[19]

Evisceration takes place further down the slaughter line. Like in poultry production, this step also carries a sizeable risk of contamination in cattle and pork. In cattle production, workers must take great care during evisceration to ensure that the intestinal tract and rumen of the animals are not punctured. Punctures often lead to the release of feces and/or ingesta, which may cause gastrointestinal cross-contamination of sterile muscle tissues. Narvaez-Bravo et al. indicated that nearly half of the intestinal feces collected from cattle contain Salmonella.^[20]

During the slaughter of swine, the dehairing and polishing processes may also result in cross-contamination. Prior to being eviscerated, the animal carcasses undergo several sequential processing steps: scalding, dehairing, singeing, and polishing (in this order). Scalding loosens the hair in the follicle to allow for easy dehairing. While scalding reduces the microbial load, dehairing significantly increases it. The dehairing equipment is a known reservoir of bacterial contamination; its moving parts are notoriously difficult to clean. In 1993, Gill and Bryant reported that dehairing machines could contain populations of Salmonella as high as 100,000 per one gram of detritus material.^[21] Bacteriological examinations revealed that 41% of cultures taken from a dehairing machine in a large abattoir tested positive for Salmonella.^[22] In the same study, conducted in 1954, cultures taken from animals post-scalding (right before entering the dehairing machine) tested negative for salmonellae. Immediately after passing through the machine, a high percentage of the carcasses were positive for Salmonella. The researchers concluded that “it was apparent that the skins of many animals were inoculated with salmonellae as they passed through the dehairing machine.” They also stated that “the meat processing industry clearly has sanitary problems difficult to control.”^[23]

The high levels of contamination are attributed to the mechanical action of the dehairing paddles, which introduces bacteria into the skin surface by scratching.^[24] Furthermore, as each carcass passes through the machine, it is vigorously rotated with a tossing action. In the process, fecal material is “pressed out” of the completely relaxed anus, contaminating an otherwise uncontaminated carcass.

The following step in the slaughtering process, known as singeing or flaming, somewhat reduces the microbial load. Unfortunately, the polishing process severely recontaminates the carcasses immediately after. Polishing removes any residual hair from previous operations. It also severely increases the risk of surface contamination. Polished carcasses are four times more likely to be contaminated with Salmonella than carcasses that do not undergo polishing.^[25] The complex polishing machinery, composed of scrapers and other rubber elements, can accumulate large quantities of dirt (e.g. hairs, parts of the epidermis) if it is not effectively cleaned and/or disinfected.^[26] If the equipment is improperly sanitized, large numbers of bacteria can develop overnight, turning the scrapers into continuous sources of contamination.

Although the above information is alarming, research indicates that cross-contamination from gastrointestinal leakage, lymph nodes, or machinery may not be the most disconcerting cause of Salmonella contamination. Indeed, the fact that consumers, restaurant managers, and chefs do not know how to handle and cook meat adequately may be the most distressing of all potential contamination factors. The long-held speculation that mishandling is a prevalent cause of Salmonella contamination in home and restaurant settings has been extensively studied, especially in ground meat products.

Phang and Bruhn reported that close to 90% of people are unaware of the FSIS-recommended internal temperature of 160^oF, or 71.1^oC, for ground beef.^[27] In the study, participants were instructed to prepare burgers in the way that they normally would while knowingly being video recorded. The results were alarming: an average of 43 potential cross-contamination events were observed per household and consumers with and without food safety training exposed themselves to potential foodborne illness.

Another blanket study conducted by the Environmental Health Specialists Network (EHS-Net) uncovered staggering figures. The research study, conducted in restaurants from eight states (one restaurant per state), exposed the food handling practices of restaurant managers across the U.S. Many of the managers that were interviewed (65%) indicated that they had been working in the food service industry for over 15 years.^[28] Yet, the managers being interviewed also expressed that they “[do not] always measure the final cook temperature of hamburgers with a thermometer” (77%) or “never measure the final cook temperatures of hamburgers” (49%). In fact, over 80% of restaurants considered in the study determined doneness of hamburgers using subjective measures. Fifty-one percent of restaurant managers “always or often checked doneness by the color of the inside of the hamburger,” 61% “always or often checked the doneness by the external appearance of the hamburger,” and 37% “always or often checked doneness by the feel or texture of the hamburger,” but subjective measures, including texture and color indicators, have been proven ineffective and unreliable.^[29]

During the course of research, two or more risky handling practices were observed in over half of the restaurants being surveyed. In 62% of restaurants, food preparers did not wash their hands between handling raw beef and ready-to-eat or cooked beef products. In 42% of restaurants, the same utensils (without rinsing or sanitizing between uses) or gloved hands (without a glove change) were used on both raw and cooked ground beef. In 40% of restaurants, workers wiped their hands on aprons or wiping cloths immediately after handling raw meat. Because these erroneous food handling practices carry high potential risks for Salmonella cross-contamination, these findings are particularly worrisome. To make matters worse, over 80% of Americans report eating out at least once per week. The EHS-Net researchers responsible for conducting this study reported their results to CDC, FDA, USDA, and state and local health departments.

Cross-contamination is a significant source of Salmonella on ready-to-eat foods. In addition to the studies showing consumer ineptitude, FSIS has also concluded that cross-contamination occurs in federally inspected establishments. Salmonellosis outbreaks in the mid-1970s prompted the Food Safety and Quality Service (FSQS) to pass a rule[30] requiring roast beef to be cooked. However, after the passage of the 1978 rule, additional outbreaks of salmonellosis from inspected roast beef occurred, prompting the same Agency (now FSIS) to amend the cooking rule and publish an interim rule.[31] In the introduction to the 1982 Interim final rule for roast beef, FSIS wrote, “Following the implementation of the cooking requirements, one outbreak of salmonellosis occurred in 1978 due to a deviation from the cooking requirements. No further outbreaks occurred until 1981, when a number of additional outbreaks occurred. In addition, recent surveys revealed the presence of salmonellae in cooked corned beef. Investigation has shown that the recent outbreaks of salmonellosis resulted because the processors did not use one of the prescribed cooking time and temperature combinations, or failed to maintain good sanitary practices or failed to maintain adequate separation of raw and cooked product, thus permitting cooked product to become recontaminated and adulterated.” Note that this contamination occurred (and still occurs) in a plant under inspection. Many home kitchens are not as well-designed as federal establishments or restaurant kitchens; in fact, many are crowded. Thus, preventing cross-contamination is difficult, even for aware consumers.

USDA-FSIS is aware that most consumers and restaurant managers are uneducated, inept, and, in some cases, powerless, when it comes to implementing proper meat handling and cooking practices. Yet, despite overwhelming evidence, FSIS deliberately chooses to continue placing the burden on consumers and remain idle even in the face of severe illness and, in certain cases, impending death.

In the 1974 American Public Health Association (APHA) v. Butz case, APHA, a key public health association in the U.S., accused USDA of “misbranding” because the Agency was placing its mark of inspection on potentially compromised meat and poultry products. APHA argued that meat was commonly contaminated with Salmonella, yet it was being passed as “USDA inspected and passed” without the addition of a warning label or cooking instructions. Predictably, USDA and the meat industry vehemently opposed the APHA. The USDA claimed that “it would be unjustified to single out the meat industry and ask that the [USDA] require it to identify its raw products as being hazardous to health.”^[32]

The D.C. Circuit Court of Appeals upheld the USDA’s position, doing so in a nonsensical and rather sexist way. The court ruled that the presence of salmonellae on meat does not constitute adulteration and stated, “As the Department said in its letter of August 18, 1971, ‘the American consumer knows that raw meat and poultry are not sterile and, if handled improperly, perhaps could cause illness.’ In other words, American housewives and cooks normally are not ignorant or stupid and their methods of preparing and cooking of food do not ordinarily result in salmonellosis.”^[33] During court proceedings, Circuit Judge Robinson wisely dissented:

The court apparently takes the position that meat and poultry ‘ordinarily’ pose no threat of salmonellosis, because American consumers are aware of the problem and familiar with the precautions necessary to prevent its occurrence. That, however, is a debatable proposition, and appellants, with substantial backing, seriously dispute it. The record contains facts supporting appellants’ assertion that people are not generally aware of the danger of salmonellae, much less of the safeguards required to avoid salmonellosis. Moreover, a study conducted for the Department of Agriculture and the Food and Drug Administration states that ‘the vast majority of the public and personnel of various food-associated industries barely know that salmonellae exist. Many of them have suffered from salmonellosis, but they do not know why or how to avoid future incidents.’ Nor is it any clearer that salmonellae in food do not ordinarily render it injurious to health. Meat, particularly pork, and poultry are likely to contain salmonellae when they reach the kitchens of our homes and restaurants, and each year more than two million people in this country contract salmonellosis.^[34]

Ironically enough, the USDA’s ironclad stance in APHA v. Butz eventually backfired. In 1999, a Supreme Beef Processors plant failed three consecutive USDA Salmonella Performance Standards inspections in an eight-month span. In one test, nearly half of the ground beef samples from the plant tested positive for Salmonella. According to the Agency, the high levels of Salmonella indicated that the ground beef at the plants was produced under “insanitary conditions.” When the USDA attempted to shut down Supreme Beef, however, the company immediately filed suit, claiming that the Agency did not have the authority to set limits on the allowable levels of Salmonella in meat. Supreme Beef argued that the pathogen is naturally occurring and is not an “adulterant” substance subject to government regulation. The court agreed that “because normal cooking practices for meat and poultry destroy the Salmonella organism,” its presence does not render the food products “injurious to health,” and cited the 1974 APHA v. Butz case. Besides, USDA itself was regularly passing Salmonella-tainted meat.

Based on law, the court’s decision in favor of Supreme Beef was sound. Based on the then-current science, the ruling was obsolete and naive. In April 2015, the Consumer Federation of America discussed the APHA v. Butz and Supreme Beef v. USDA court cases. They wrote, “This legal interpretation relies on outdated precedent—particularly the D.C. Circuit Court’s 1974 decision in American Public Health Association v. Butz—that is unsupported by science.”^[35] If thorough cooking was effective, poultry and pork, ordinarily well-cooked, would not be at the top of the CDC’s salmonellosis attribution list. Research has further reinforced the supposition that cross-contamination must be a priority. A review paper, published in 2009, concluded that cross-contamination seems to be “of greater importance than the risk associated with undercooking of poultry, meat, or eggs.”^[36]

The August 18, 1971 letter referenced by the D.C. Circuit Court of Appeals was the first of its kind. Prior to the letter, USDA had acknowledged the need for training of food service workers and consumers. In 1969, the National Academy of Sciences (NAS), at the request of FDA and USDA, released a comprehensive report titled “An Evaluation of the Salmonella Problem.” In the 200-page document, NAS investigated the nature of the U.S. Salmonella problem and made recommendations to USDA to mitigate the contributing factors. The half-a-century-old report addresses many of the concerns discussed in this petition including cross-contamination,[37] hazardous slaughtering practices,[38] consumer mishandling and miseducation,[39] and genetic plasticity,[40] among others.

The report states that the Salmonella problem is “exacerbated by traditional slaughtering and handling practices that help to spread the contaminants from one carcass to another.”[41] In order to solve this issue, one of the recommendations made by NAS was to implement a “massive educational program.” A 1970 letter written by USDA in response to the NAS report shows that the Agency “[concurred] in this recommendation” and agreed that it “should continue and intensify educational programs” and “expand educational efforts.”[42] The NAS report also confirms that USDA is well aware that consumers have very little knowledge of foodborne illnesses and food safety handling practices. The report states that “the vast majority of the public and personnel of the various food-associated industries barely know that salmonellae exist” and that “they do not know why or how to avoid future incidents.” USDA is cognizant of consumer ineptness and has previously agreed that additional education is required, yet a year after concurring with nearly all of the NAS report’s recommendations, the Agency changed its stance, stating that “the American consumer knows that raw meat and poultry are not sterile and, if handled improperly, perhaps could cause illness.” The 1974 GAO Report to Congress confirmed that “American housewives and cooks” are, in fact, “ignorant,” or at least vastly uninformed, about the potential hazards of Salmonella contamination.[43] Results of the GAO study showed that 74% of women did not know that Salmonella was a bacterium that could cause food poisoning. Sixty-six percent of women indicated that they did not know how to minimize the spread of Salmonella within their homes.

Following the tragic 1993 Jack in the Box E. coli O157:H7 outbreak, which killed four children, Michael Taylor, then-current FSIS Administrator, made a brave step in the right direction; he announced that E. coli O157:H7 would be deemed an adulterant in raw ground beef. In Texas Food Industry Association, et al., v. Mike Espy, the court found that “E. coli O157:H7 fits the definition of an adulterant under the Federal Meat Inspection Act” and cited “relatively low infectious dose,” “serious illness conditions,” and survival in “what many consumers consider to be proper cooking of ground beef products” as reasons for the change.^[44] The dangers of Salmonella, still, were completely and utterly ignored even though the cited reasons clearly apply to Outbreak Serotypes of Salmonella as well.

While most Salmonella outbreaks occur from infectious doses over 100 CFU, low level exposure has been proven to result in sporadic disease.^[45] Additionally, the prevalence of Salmonella in North America is speculated to be greater than that of any Shiga toxin-producing E. coli (STEC).^[46] Salmonellosis has been associated with long-term sequelae including reactive arthritis, Irritable Bowel Syndrome, and life-threatening bacteremia. Finally, research on the ten most predominant Salmonella serotypes from ground beef has revealed that each individual serotype can survive internal temperatures below, and sometimes at, the FSIS-recommended “doneness” temperature of 71.1^oC.^[47] In the study, each serotype survived rare, medium rare, medium, and medium well levels of cooking.^[48] Salmonella Agona, a particularly heat-resistant serovar, survived in ground beef cooked to an internal temperature of 71.1^oC (equivalent to a “well done” degree of doneness). In a second study, pork loin chops were cooked to various levels of doneness (rare, medium, and well-done) in either a gas hob or a traditional static oven—two of the most common cooking methods for pork meat. The results indicated that well-done cooking in a static oven was the only treatment that could completely inactivate Salmonella.^[49] Pork loin chops cooked “well done” in a gas hob still tested positive for the pathogen.

In summary, Cargill, the largest private corporation in the United States, continues to advocate for a more modern and science-based regulatory system for meat, poultry, and egg products—and for good reason. Salmonellae in raw ground beef and pork products are “ordinarily injurious.”[50] Because deep tissue lymph nodes often cannot be removed and are protected from antimicrobial surface interventions, the pathogen, in many cases, cannot be avoided. In whole muscle beef and pork products, salmonellae are “added substances.”[51] Bacterial contamination of intact meat end products originates from extrinsic sources (e.g. lymph nodes, gastrointestinal tract, external carcass surfaces) and occurs during the slaughter and dressing of carcasses. In cattle processing, dehiding and evisceration increase the risk for cross-contamination. In swine production, scalding and singeing reduce the microbial load, while dehairing, polishing, and evisceration recontaminate the carcasses. Cross-contamination within home and restaurant settings is equally important, frequently underestimated, and, according to qualified researchers, impossible to control.[52] Poor hygiene and unsafe food handling practices are rampant. Consumers are unaware of the risks of foodborne illness and use unreliable subjective measures to determine doneness. Furthermore, certain Salmonella serotypes can survive the FSIS-recommended internal temperatures.

In the 1974 case of American Public Health Association v. Butz, the United States Department of Agriculture fervently professed that the presence of salmonellae in and on intact animal tissues did not constitute adulteration and that it would be unjustified to “single out” the meat industry. Several years later, however, the Agency recanted in Supreme Beef v. USDA, claiming that a non-compliant Supreme Beef plant should be shut down because it was producing meat in “unsanitary conditions.” In the 1994 Texas Food Industry Association v. Espy ruling, the court failed to address the Salmonella problem in ground meat products. The then-current scientific evidence had already proven that the pathogen met all of the criteria that Escherichia coli O157:H7 did to be declared an adulterant (i.e. low infectious dose, association with severe illnesses, and survival in what consumers consider to be proper cooking), yet Salmonella was not declared an adulterant.

More to come.

___________

[1] Laufer, A. S., J. Grass, K. Holt, J. M. Whichard, P. M. Griffin, L. H. Gould. (2015). Outbreaks of Salmonella Infections Attributed to Beef – United States, 1973-2011. Epidemiol Infect. 143(9):2003-2013.

[2] Tegegne, F. M. (2019). Epidemiology of Salmonella and its serotypes in human, food animals, foods of animal origin, animal feed and environment. J Food Nutr Health. 2(1):7-14.

[3] Gutema, F. D., et al. (2019). Prevalence and Serotype Diversity of Salmonella in Apparently Healthy Cattle: Systematic Review and Meta-Analysis of Published Studies, 2000-2017. Front Vet Sci. 6:102.

[4] Stephens, T. P., et al. (2007). Distribution of Escherichia coli O157 and Salmonella on Hide Surfaces, the Oral Cavity, and in Feces of Feedlot Cattle. J Food Prot. 70(6):1346-1349.

[5] Pires, S. M., A. R. Vieira, T. Hald, D. Cole. (2014). Source Attribution of Human Salmonellosis: An Overview of Methods and Estimates. Foodborne Pathog Dis. 11(9):667-676.

[6] Campos, J., J. Mourao, L. Peixe, P. Antunes. (2019). Non-typhoidal Salmonella in the Pig Production Chain: A Comprehensive Analysis of Its Impact on Human Health. Pathogens. 8(1):19.

[7] Tegegne, F. M. (2019). Epidemiology of Salmonella and its serotypes in human, food animals, foods of animal origin, animal feed and environment. J Food Nutr Health. 2(1):7-14.

[8] “America’s Largest Private Companies.” Forbes, 2018.

[9] “Recommendations to Modernize the Meat and Poultry Oversight System in the United States – Developed by the Meat and Poultry Dialogue Group.” Meridian Institute, 2017.

[10] Id. at 38.

[11] Id. at 2.

[12] Li, M., et al. (2015). Salmonella spp. in lymph nodes of fed and cull cattle: Relative assessment of risk to ground beef. Food Control. 50:423-434.

[13] Zhang, Y., et al. (2019). Interventions Targeting Deep Tissue Lymph Nodes May Not Effectively Reduce the Risk of Salmonellosis from Ground Pork Consumption: A Quantitative Microbial Risk Assessment. Risk Anal. Epub ahead of print.

[14] Brashears, M. M., B. D. Chaves. (2017). The diversity of beef safety: A global reason to strengthen our current systems. Meat Sci. 132:59-71.

[15] Li, M., et al. (2015). Salmonella spp. in lymph nodes of fed and cull cattle: Relative assessment of risk to ground beef. Food Control. 50:423-434.

[16] Gill, C. O. (1979). A Review: Intrinsic Bacteria in Meat. J Appl Bacteriol. 47:367-378.

[17] Stephens, T. P., G. H. Loneragan, T. W. Thompson, A. Sridhara, L. A. Branham, S. Pitchiah, M. M. Brashears. (2007). Distribution of Escherichia coli O157 and Salmonella on Hide Surfaces, the Oral Cavity, and in Feces of Feedlot Cattle. J Food Prot. 70(6):1346-1349.

[18] Narvaez-Bravo, C., et al. (2013). Salmonella and Escherichia coli O157:H7 Prevalence in Cattle and on Carcasses in a Vertically Integrated Feedlot and Harvest Plant in Mexico. J Food Prot. 76(5):786-795.

[19] “Salmonella in the Pork Production Chain.” National Pork Board, 2013.

[20] Narvaez-Bravo, C., et al. (2013). Salmonella and Escherichia coli O157:H7 Prevalence in Cattle and on Carcasses in a Vertically Integrated Feedlot and Harvest Plant in Mexico. J Food Prot. 76(5):786-795.

[21] Gill, C. O., J. Bryant. (1993). The contamination of pork with spoilage bacteria during commercial dressing, chilling and cutting of pig carcasses. Int J Food Microbiol. 16:51-62.

[22] Galton, M. M., W. V. Smith, H. B. McElrath, A. B. Hardy. (1954). Salmonella in Swine, Cattle and the Environment of Abattoirs. J Infect Dis. 95(3):236-245.

[23] Galton, M. M., W. V. Smith, H. B. McElrath, A. B. Hardy. (1954). Salmonella in Swine, Cattle and the Environment of Abattoirs. J Infect Dis. 95(3):236-245.

[24] “Salmonella in the Pork Production Chain.” National Pork Board, 2013.

[25] Sanchez-Rodriguez, J. A., et al. (2018). New insights on the risk factors associated with the presence of Salmonella on pig carcasses—Lessons from small slaughterhouses. Food Control. 87:46-52.

[26] Huis in’t Veld, J. H. J., R. W. A. W. Mulder, J. M. A. Snijders. (1993). Impact of Animal Husbandry and Slaughter Technologies on Microbial Contamination of Meat: Monitoring and Control. Meat Sci. 36:123-154.

[27] Phang, H. S., C. M. Bruhn. (2011). Burger Preparation: What Consumers Say and Do in the Home. J Food Prot. 74(10):1708-1716.

[28] Bogard, A. K., C. C. Fuller, V. Radke, C. A. Selman, K. E. Smith. (2013). Ground Beef Handling and Cooking Practices in Restaurants in Eight States. J Food Prot. 76(12):2132-2140.

[29] “Color of Cooked Ground Beef as It Relates to Doneness.” United States Department of Agriculture, 2013.

[30] 9 CFR § 318.17 (1978).

[31] “Interim final rule – Production Requirements for Cooked Beef, Roast Beef, and Cooked Corned Beef.” Food Safety and Inspection Service, USDA. FR 47142, pages 31854-31855 of the July 23, 1982, Federal Register. Docket No. 82-00411.

[32] Nestle, M. (2003). Safe Food: Bacteria, Biotechnology, and Bioterrorism. California: University of California Press. 66. Web.

[33] American Public Health Association et al. v. Earl Butz, 167 U.S. App. D.C. 93. United States Court of Appeals, District of Columbia Circuit. (1974). Point 27. Web.

[34] American Public Health Association et al. v. Earl Butz, 167 U.S. App. D.C. 93. United States Court of Appeals, District of Columbia Circuit. (1974). Point 35. Web.

[35] “Taking Salmonella Seriously: Policies to Protect Public Health under Current Law.” Consumer Federation of America, 2018.

[36] Luber, P. (2009). Cross-contamination versus undercooking of poultry meat or eggs – which risks need to be managed first? Int J Food Microbiol. 134:21-28.

[37] Id. at 2, 121, 122.

[38] Id. at 2, 118, 121, 122.

[39] Id. at 13, 16.

[40] Id. at 4, 7, 60, 61.

[41] Foster, E. M., et al. An Evaluation of the Salmonella Problem. Washington D.C.: National Academy of Sciences, 1969. Web (Google eBook).

[42] “A Review of the NAS-NRC Report.” Microbiological Subgroup of the USDA Food Safety Committee, 1970.

[43] Anon., 1974a. Salmonellae in raw meat and poultry – An assessment of the problem. GAO Report to the Congress. Comptroller General of the United States, Washington D.C. Publication No. B-154031 (2).

[44] Texas Food Industry Association, et al., v. Mike Espy, 870 F. Supp. 143. United States District Court, W.D. Texas, Austin Division. (1994).

[45] Teunis, P. F. M., F. Kasuga, A. Fazil, I. D. Ogden, O. Rotariu, N. J. C. Strachan. (2010). Dose-response modeling of Salmonella using outbreak data. Int J Food Microbiol. 144:243-249.

[46] Brashears, M. M., B. D. Chaves. (2017). The diversity of beef safety: A global reason to strengthen our current systems. Meat Sci. 132:59-71.

[47] Stopforth, J. D., R. Suhalim, B. Kottapalli, W. E. Hill, M. Samadpour. (2008). Thermal Inactivation D- and z-Values of Multidrug-Resistant and Non-Multidrug-Resistant Salmonella Serotypes and Survival in Ground Beef Exposed to Consumer-Style Cooking. J Food Prot. 71(3):509-515.

[48] “Degree of Doneness.” Certified Angus Beef.

[49] De Cesare, A., E. Domenech, D. Comin, A. Meluzzi, G. Manfreda. (2018). Impact of Cooking Procedures and Storage Practices at Home on Consumer Exposure to Listeria Monocytogenes and Salmonella Due to the Consumption of Pork Meat. Risk Anal. 38(4).

[50] Per 21 U.S.C. § 601(m)(1).

[51] Per 21 U.S.C. § 601(m)(1).

[52] Carrasco, E., A. Morales-Rueda, R. M. García-Gimeno. (2012). Cross-contamination and recontamination by Salmonella in foods: A review. Food Res Int. 45:545-556.