This column addresses Docket No. FSIS-2019-0023 “Changes to the Salmonella Verification Testing Program: Proposed Performance Standards for Salmonella in Raw Comminuted Pork and Intact or Non-Intact Pork Cuts and Related Agency Verification” For more information, or to comment on the docket, click here. Comments close on April 18.

The introductory paragraph, “Salmonella bacteria are among the most frequent causes of foodborne illness” is excellent in that it defines the problem that, “Currently, events that cause contamination of pork carcasses cannot be completely eliminated from commercial slaughter, fabrication, or further processing operations.” (FSIS 2022)

The proposal does not address preventing Salmonella contamination. A core principle of control programs, including HACCP, is prevention, not simply testing (Zwietering 2016). Although testing can provide a regulatory incentive, prescribing scientific risk-based preventive measures would offer needed improvement. FSIS could promote pathogen control incentives by modernizing inspection similar to current European Union initiatives, e.g. “Risk-based Meat Safety Assurance System” (RB-MSAS) (Cavalheiro, 2022, Alban 2021, Blagojevic 2021, Riess & Hoelzer, 2020). This would also promote USDA’s One Health approach. 

Preventive measures start with the hazard analysis (9 CFR 417.10(a)), identifying the sources. The hazard, Salmonella, and other enteric pathogens come from the preharvest environment. Food animals carry Salmonella and other enteric pathogens in their feces, lymph nodes (Harvey 2020) and tonsils: “Carcasses entering the clean area showed a Salmonella contamination rate of 96.7% in the oral cavity and 55.0% in the rectum content samples.” (Zeng 2021)

The problem(s):
The primary problem is the non-visible fecal material carrying enteric bacteria including Salmonella. The classic example is Blankenship (1993). The ARS project was to demonstrate that visible fecal contamination on broilers could be eliminated by washing and the bacterial load would be no more than the carcasses with no visible fecal contamination. The ARS researchers reported that the differences in bacterial counts and Salmonella prevalence between reprocessed and regular carcasses were not significant. Unsaid was the carcasses, with no visible fecal contamination, contained non-visible feces and the fecal bacteria.

To review the fecal contamination problem on pigs, start with the observation that during dehairing, “The carcass is subjected to vigorous treatment, and in the process, fecal leakage from the completely relaxed anus inevitably will occur.” (Galton 1954). And skip to a quantitative microbial risk assessment “. . . on Salmonella in slaughter and breeder pigs. . . . The model outcome represents an increase in average prevalence of Salmonella contamination and Salmonella numbers at dehairing and a decrease of Salmonella numbers at scalding. These results show good agreement when compared to several other QMRAs and microbiological studies. (Swart 2016). Then finish with a review “Several studies showed an increase in prevalence and level of Salmonella spp. contamination at the dehairing step and a decrease of Salmonella spp. level at scalding [23,25,32,35,50,58]…” (Hdaifeh 2020). 

Over the past two decades, FSIS has been discussing the problem of non-visible feces but has not taken the next step to solving the problem, detection. There are methods for detecting the non-visible fecal matter with fluorescence imaging devices that ARS has been developing for decades (Feng 2012). A recent paper shows some success (Gorji 2022). Detection would require removal. Removal using pulsed washes could work but have had limited success with poultry. Prevention such as ARS demonstrated with poultry carcasses by plugging the cloaca or eviscerating before defeathering might work (Berrang 2001, 2018). However, preventing or removing all fecal material from pig carcasses would not address the problem of lymph node and tonsil carriage. 

Preharvest controls would solve many problems. In 2013, FSIS wrote, “Control of Salmonella begins on the farm. A  review of Danish pork production has shown  that Salmonella prevalence in the herd is a  significant factor for determining the  Salmonella prevalence and levels on  carcasses (Alban and Stark, 2005).” In a review of strategies, PEW wrote, “Pre-harvest measures are the first step to effectively controlling food safety hazards and improving public health, and they should begin as far up the supply chain as possible. . .” (PEW 2019). There are numerous roadblocks to implement preharvest controls including regulatory, economic and logistical issues (PEW 2017). 

How to overcome the roadblocks and incentivize preharvest controls has been discussed for decades. One way could have FSIS identify which sources bring outbreak strains of Salmonella to slaughter. FSIS could assign analytical resources to sampling animals in lairage for Salmonella and link outbreak positives to sources. This would better enable FSIS to make three choices: 1. Prevent the hazards, 2. Remove the hazards, or 3. Negate the hazards.

1. Prevent the hazards
The hazards originate in the preharvest environment. FSIS has no jurisdiction there but can influence actions e.g. 9 CFR 310.21 “Carcasses suspected of containing sulfa and antibiotic residues; sampling frequency; disposition of affected carcasses and parts.” FSIS could tag future animals from preharvest sources that have been positive for outbreak strains and subject them to more intensive inspection to remove or negate the hazards similar to the EU’s RB-MSAS. 

Plugging the anus or eviscerating before dehairing could prevent fecal contamination but would not address pathogen carriage in the lymph nodes and tonsils.

A review of preharvest controls for pigs would require more words than this article allows but here is a list of recent reviews: (Koyun 2022, Bearson 2022, Rodrigues da Costa 2021, Bernad-Roche 2021, Sargeant 2021, Ostanello 2020, Peeters 2020, FAO/WHO 2016, FSIS 2013)

2. Remove the hazards
The dehairing process is a primary source of fecal contamination. It’s a well documented and ignored problem. The tumbling and paddling press fecal material out of the anus and the paddles press some fluid into the empty follicles. Thus, any enteric pathogens carried by this non-visible fecal material are protected from interventions such as singeing, polishing, and washing. Handling the carcass during cutting, presses some liquid from the follicles and increases the prevalence of Salmonella on parts. Implementing a fluorescence imaging device would aid verification that fecal material was not present (Gorji 2022, Sueker 2021).

Excising the lymph nodes, as described for cattle, might be practical or too intensive. (Koohmaraie and Wheeler 2019)

3. Negate the hazards
FSIS would tag carcasses from sources that have been positive for outbreak strains. Require all tagged carcasses and their parts to be treated to inactivate enteric pathogens. Treatment could be cooking, high hydrostatic pressure, irradiation, or other validated processes. 

The processes of negating or removing the enteric pathogens would likely reduce the value of the animals and thus provide an economic incentive for preventing the hazards. The costs for those producers who have implemented preharvest interventions would be justified and in the spirit of 21 USC 602.

References
Alban, L., Poulsen, M.K., Petersen, J.V., Lindegaard, L.L., Meinert, L., Koch, A.G. and Møgelmose, V., 2022. Assessment of risk to humans related to Salmonella from bile on pig carcasses. Food Control, 131, p.108415.

Bearson, S.M.D.. 2022. Salmonella in Swine: Prevalence, Multidrug Resistance, and Vaccination Strategies. Annual Review of Animal Biosciences.10:373-393 

Bernad-Roche, M., Casanova Higes, A., Marín Alcalá, C.M., Cebollada Solanas, A. and Mainar Jaime, R.C., 2021. Salmonella infection in nursery piglets and its role in the spread of salmonellosis to further production periods. Pathogens, 10:123.

Berrang,M. E., R. J. Buhr, J.A. Cason, and J.A.Dickens. 2001. Broiler carcass contamination with Campylobacter from feces during defeathering. J. Food Prot. 64:2063–2066.

Berrang, M. E., Meinersmann, R. J., & Adams, E. S. (2018). Shredded sponge or paper as a cloacal plug to limit broiler carcass Campylobacter contamination during automated defeathering. J. Applied Poultry Research, 27:483-487.

Blankenship, L.C., Bailey, J.S, Cox, N.A, Musgrove, M.T, Berrang, M.E, Wilson, R.L, Rose, M.J, Dua, S.K. 1993. Broiler Carcass Reprocessing, a Further Evaluation. J. Food Prot. 56:983-985. doi.org/10.4315/0362-028X-56.11.983

Cavalheiro, L.G., Gené, L.A., Coldebella, A., Kich, J.D. and Ruiz, V.L.D.A., 2022. Microbiological Quality of Pig Carcasses in a Slaughterhouse Under Risk-Based Inspection System. Available at SSRN 4011027. doi.org/10.2139/ssrn.4011027

Feng, Y.Z., Sun, D.W. 2012. Application of Hyperspectral Imaging in Food Safety Inspection and Control: A Review, Critical Reviews in Food Science and Nutrition, 52:1039-1058, DOI: 10.1080/10408398.2011.651542 

FSIS 2022a. Changes to the Salmonella Verification Testing Program: Proposed Performance Standards for Salmonella in Raw Comminuted Pork and Intact or Non-Intact Pork Cuts and Related Agency Verification Procedures. 02/16/2022 87 FR 8774

FSIS 2022b Changes to the Salmonella Verification Testing Program: Proposed Performance Standards for Salmonella in Raw Comminuted Pork and Intact or Non-Intact Pork Cuts and Related Agency Verification Procedures. A Notice by the Food Safety and Inspection Service on 02/16/2022  https://www.federalregister.gov/documents/2022/02/16/2022-03301/changes-to-the-salmonella-verification-testing-program-proposed-performance-standards-for-salmonella

FSIS 2021: FSIS Seeking Proposals for Pilot Projects to Control Salmonella in Poultry Slaughter and Processing Establishments  

https://www.fsis.usda.gov/news-events/news-press-releases/constituent-update-december-3-2021

FSIS 2013: Compliance Guideline for Controlling Salmonella in Market Hogs. First Edition December 2013. FSIS-GD-2013-0023 https://www.fsis.usda.gov/sites/default/files/import/Controlling-Salmonella-in-Market-Hogs.pdf

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.

Gorji, HT, Shahabi SM, Sharma A, Tande LQ, Husarik K, Qin J, Chan DE, Baek I, Kim MS, MacKinnon N, Morrow J. 2022. Combining deep learning and fluorescence imaging to automatically identify fecal contamination on meat carcasses. Scientific Reports. 12:1-1. doi.org/10.1038/s41598-022-06379-1 

Harvey, R.B., Norman, K.N., Anderson, R.C., Nisbet, D.J. 2020. A preliminary study on the presence of Salmonella in lymph nodes of sows at processing plants in the United States. Microorganisms. 8:1602. doi.org/10.3390/microorganisms8101602

Hdaifeh, A., Khalid, T., Boué, G., Cummins, E., Guillou, S., Federighi, M. and Tesson, V., 2020. Critical Analysis of Pork QMRA Focusing on Slaughterhouses: Lessons from the Past and Future Trends. Foods, 9:1704. doi.org/10.3390/foods9111704

FAO/WHO [Food and Agriculture Organization of the United Nations/World Health Organization]. 2016. Interventions for the control of non-typhoidal Salmonella spp. in beef and pork: Meeting report and systematic review. Microbiological Risk Assessment Series No. 30. Rome.

Koyun, O.Y., Callaway, T.R., Nisbet, D.J. and Anderson, R.C., 2022. Innovative Treatments Enhancing the Functionality of Gut Microbiota to Improve Quality and Microbiological Safety of Foods of Animal Origin. Annu. Rev. Food Sci. Technol., 13.

Ostanello, F. and De De Lucia, A., 2020. On-farm risk factors associated with Salmonella in pig herds. Large Animal Review, 26(3), pp.133-140.

Peeters, L., Dewulf, J., Boyen, F., Brossé, C., Vandersmissen, T., Rasschaert, G., Heyndrickx, M., Cargnel, M., Mattheus, W., Pasmans, F. and Haesebrouck, F., 2020. Bacteriological evaluation of vaccination against Salmonella Typhimurium with an attenuated vaccine in subclinically infected pig herds. Preventive veterinary medicine, 182, p.104687.

Riess, L. E., Hoelzer, K. 2020. Implementation of Visual-only Swine Inspection in the European Union: Challenges, Opportunities, and Lessons Learned. J Food Prot. 83:1918–1928. doi.org/10.4315/JFP-20-157

Rodrigues da Costa, M., Pessoa, J., Meemken, D. and Nesbakken, T., 2021. A Systematic Review on the Effectiveness of Pre-Harvest Meat Safety Interventions in Pig Herds to Control Salmonella and Other Foodborne Pathogens. Microorganisms, 9:1825.

Sargeant, J.M., Totton, S.C., Plishka, M. and Vriezen, E.R., 2021. Salmonella in animal feeds: A scoping review. Frontiers in veterinary science, p.1314.

Sueker, M., Stromsodt, K., Gorji, H.T., Vasefi, F., Khan, N., Schmit, T., Varma, R., Mackinnon, N., Sokolov, S., Akhbardeh, A. and Liang, B., 2021. Handheld Multispectral Fluorescence Imaging System to Detect and Disinfect Surface Contamination. Sensors, 21:7222. doi.org/10.3390/s21217222

Swart, AN, Evers EG, Simons RL, Swanenburg M. 2016. Modeling of Salmonella Contamination in the Pig Slaughterhouse. Risk Anal. 2016 Mar;36(3):498-515. doi: 10.1111/risa.12514. Epub 2016 Feb 9.

Zwietering, M.H., L. Jacxsens, J. Membré, M. Nauta, M. Peterz. 2016. Relevance of Microbial Finished Product Testing in Food Safety Management. Food Control. 60:31-43, 

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The theater building at Texas A&M College had an inscription “Ignorance Is the Curse of God,. Knowledge Is the Wing Wherewith We Fly to Heaven. Shakespeare”. That curse has resulted in thousands of illnesses and deaths due to ignorance of safe food handling procedures. 

A. Dr. Mindy Brashears speaks
In a recent column, Dr. Mindy Brashears she noted there is “… an insidious movement we have in society right now, one that undermines science. Not only has the meat and poultry industry been painted in a negative light recently, the scientific-community has also taken a hit. There is a trend, if not a solid perspective for some, that science isn’t real and data can’t be trusted.” Additionally, she noted in advocating consumer education that, “There was insistence by some of the groups that consumers had no responsibility for food safety and the food should be free from pathogens when it arrived to the consumer. There is no science in this approach and it overlooks an important point in the supply chain where risks can be mitigated.”

She concluded, “In 2022, we must stand resolute in science-based decisions, support the scientific community and protect the consumer and the safety of our food supply.”

Part of my comment to the article is: “Consumer education is ideal and has been ongoing for over a half century. It fails too often. In the 1970, “A Review of the NAS-NRC Report. An Evaluation of the Salmonella Problem” USDA’s Microbiological Subgroup of the USDA Food Safety Committee. They cited examples of current programs. Fifteen years later USDA formed the Hot Line to answer consumer questions and develop educational programs. 

B. Education is ideal and idealistic and alas has a history of failure.
The National Academy of Science (NAS) Committee on Salmonella published “An Evaluation of the Salmonella Problem” in 1969. In 1970, USDA scientists reviewed the NAS report in “A Review of the NAS-NRC Report. An Evaluation of the Salmonella Problem.”  All agreed that consumers needed more training in handling food safely. 

The NAS recommended, “The federal government should take the lead in developing a coordinated industry-professional-local-state-federal government plan for the control of salmonellosis that will generate the technical and financial support for the expansion of education efforts on a continuing basis…”

USDA commented, “The Department concurs with the recommendation in principle. It does not agree that a single agency be designated to coordinate training or act as a single authority” 

“The Department initiated coordinated educational programs to support its regulatory programs for the control and eradication of salmonellae in chickens and turkeys. The programs were inaugurated in 1935 and 1943, respectively…” USDA listed eight accomplishments and listed seven things that should be done including “Continue and intensify educational programs regarding salmonellae in the environment, their control in animal feeds and animal products used for human food.” and “Devote more educational effort to the urban sector of our society regarding salmonellae associated with foods, pets, and home sanitation.”

Given the scientific publications in the subsequent half century on consumer expertise, it’s evident the educational efforts have not been fully successful.

There are several papers on failures and the barriers to implementing safety practices. An  example is Feng and Bruhn (2019); they wrote, “Barriers to thermometer were categorized into two major groups: “the belief that a thermometer is not necessary” and “the difficulty of selecting and using a thermometer.” Each group has its unique aspects. Four barriers were recognized in the “not necessary” group: (I) preference for alternative techniques, (ii) mainstream media and food professionals seldom serve as role models and often negate the need for food thermometers, (iii) limited awareness of potential health issues associated with current practices, and (iv) limited knowledge and awareness related to thermometer usage for specific food groups. Six barriers were recognized in the “difficult to select and use” group” including “difficulties in selecting the type of food thermometers …”   

I recommend: “TABLE 4. Quotations identifying barriers to food thermometer use among consumers and food workers.” Ewen Todd in an email exchange wrote, “Some authors call this the anchoring effect where we tend to go back to our culture roots no matter what information we are given.” 

In a review of a journal issue, Todd (2020) wrote, “In conclusion, these five papers add to our knowledge of how to understand why preventing and controlling food-borne illness is so difficult. Consumers and the public in general react to broadcast news and nowadays social media, as well as their base culture, for setting their anchoring of how they perceive risks of illness from eating specific food items.”

Another example of ignoring science and education was after the Escherichia coli O157:H7 outbreak in salami. The industry contracted with the Food Research Institute to develop processing guidelines to prevent another outbreak. After several years, the USDA’s Food Safety and Inspection Service (FSIS) surveyed the industry to determine compliance and found 49 establishments not using the guidelines. They amended their processes only after microbiological analysis found pathogens in their finished products. Survival of enteric pathogens had been established in earlier by Smith and Palumbo (1975) but ignored by both the industry and USDA. 

Thus, food safety education programs will not be fully successful, especially by those who are ignorant of science. The opposition to Covid-19 vaccination and masks is an extreme example of civil ignorance.

Another consumer problem is the design of home kitchens. Few are designed to prevent cross contamination between raw and ready-to-eat. My own 1958 kitchen, while much larger than the one in the previous 1948 house, offers many opportunities for cross contamination. Most home kitchens would not pass local jurisdictions retail specifications and certainly not the FSIS requirements for separation. Thus, the occupants must be competent in aseptic technique, not buy raw poultry, or be very lucky. 

I discussed some of these problems in 2014. 

What are some solutions? The status quo is let the ignorant suffer. 

1. Licensing consumers to purchase raw meat or poultry similar to how some jurisdictions require certified food manager on site during all hours of operations. 

2. Eliminate pathogens in slaughter establishments. Discussed in the next section.

3. Incentivize producers to eliminate zoonotic carriage in their animals. This option is ideal and idealistic but can be accomplished as Pomeroy did in the 1970’s. It is also similar USDA’s “One Health Approach: https://www.usda.gov/topics/animals/one-health 

Yes, keep educating consumers; there will always be wild zoonoses in the environment but, more can be done to reduce the pathogens from FSIS inspected products. Do not ignore that problem.

C. Slaughter Establishments Pass Pathogens
One source of pathogens entering home and retail operations is the failure of inspected slaughter establishments to eliminate the pathogens carried by entering animals. An illustration is the permitted Salmonella prevalence permitted by the FSIS Salmonella Performance Standard. The Standards, based on surveys, recognize the problem of eliminating pathogens from pork and poultry because of the presence of non-visible fecal material in the empty follicles. Beef carcasses, because they are skinned have lower standards. Because the older cows and bulls generally have greater pathogen carriage, they have a higher standard than the younger steers and heifers. The declaration that certain outbreak serotypes of Shiga Toxin positive Escherichia coli (STEC) are adulterants in ground beef and designated trim has provided an incentive for greater post harvest control.

Research has developed and evaluated many carcass interventions including, chlorine, acetic acid, peracetic acid, lactic acid, and hot water, sprayed and pulsed. Some are used alone or in combination and yet pathogens end up on product. 

D. Preharvest One Health
The failure to eliminate the pathogens entering on animals has stimulated decades of research in preharvest control by academia, industry, and the Agricultural Research Service (ARS). Similar research has demonstrated the environmental contamination originating from food animal production facilities sometime called Concentrated Animal Feeding Operations (CAFO) and dairies. The environment includes recreational waters, produce fields and orchards. The vectors include water runoff, wind, and wild animals, including insects and birds. 

Lacking is incentives for implementing the known interventions to reduce pathogen carriage. One incentive could be EPA regulation enforcement. Other incentives could be Congressional legislation to include human pathogens in APHIS’ jurisdiction or put the preharvest environment under FSIS jurisdiction. Another would be to declare outbreak strains of pathogens as adulterants as FSIS has done for certain STEC. 

Eliminating pathogens is practical Pomeroy (1989). He eliminated Salmonella carriage in turkeys in the 970’s, starting with Salmonella-free poults and used biosecurity, including feeding only grain and seafood protein. Currently growers also have vaccines, bacteriophage, prebiotics, probiotics, and other controls. What is lacking is incentives. 

A comment to Brashears’ article was, “How about educating those future consumers the concept of personal responsibility at some point K-12?” I replied, “… how about producers taking responsibility for the environmental contamination from their yards including manures? Lots of science about movement of pathogens vis air, water and birds.” and cited, Smith, O.M. et alia. 2022. A trait-based framework for predicting foodborne pathogen risk from wild birds. Ecological Applications. doi.org/10.1002/eap.2523”.

Conclusion
In conclusion, education is one of several pillars for food safety. In an ideal world it could be the sole pillar but that would require redesigning home and retail kitchens, mandatory training, and licensing. The One Health approach is needed to reduce environmental contamination from food animal production, fewer pathogens entering slaughter establishments, and fewer pathogens in produce fields and orchards. Thus, fewer pathogens entering home and retail kitchens where hopefully competent preparers would eliminate the hazards. Think of the combination of vaccination, masks, and distance. Each alone is imperfect in halting the COVID-19 viruses but together they reduce the hazard to de minimus. For food safety, a similar defense in depth approach is needed. 

References:
Brashears, M. 2022. A resolute focus. Food Safe and Sound. https://www.meatingplace.com/Industry/Blogs/Details/102854

Custer, C.S. 2014. Salmonellosis Prevention: Just Cook It. Food Safety News 

Feng, Y., C.M. Bruhn. 2019. Motivators and Barriers to Cooking and Refrigerator Thermometer Use among Consumers and Food Workers: A Review. 82:128-150. doi.org/10.4315/0362-028X.JFP-18-245 

Pomeroy B.S., Nagaraja K.V., Ausherman L.T., Peterson I.L., Friendshuh K.A. 1989. Studies on feasibility of producing Salmonella-free turkeys. Avian Dis. 33:1-7.

Smith, J.L., Palumbo, S.A., Kissinger, J.C, Huhtanen, C.N. 1975. Survival of Salmonella dublin and Salmonella typhimurium in Lebanon bologna.. J. Milk Food Technol. 38:150-154. 

Todd, E. 2020. Food-borne disease prevention and risk assessment. International Journal of Environmental Research and Public Health, 17(14):5129. doi.org/10.3390/ijerph17145129

During the past half century the Centers for Disease Control and Prevention’s annual reports show that salmonellosis has been the leading cause of foodborne death. Salmonellosis is caused by virulent serotypes of the bacterium Salmonella enterica. The sources include undercooked meat or poultry, cross contamination from raw meat or poultry, and poorly washed produce. The species varies in its virulence to humans and animals. Some serotypes are pathogenic to animals but less so to humans. Other serotypes are pathogenic to humans but not to animals, which become asymptomatic carriers.

Public health issues with asymptomatic carriers include:

1. The pathogens are undetectable during slaughter processing as is the non-visible fecal contamination;

2. Ordinary slaughter and dressing processing steps do not eliminate the pathogens from the product, they are in the non-detectible fecal contamination embedded in the follicles;

3. There is a tolerance for their presence based on surveys; thus,

4. The production facilities have no incentive to eliminate the pathogen which leads to environmental contamination, including produce.

On Jan. 19, 2020, attorney Bill Marler and others petitioned the Food Safety Inspection Service (FSIS) to declare the outbreak serotypes of Salmonella as adulterants. FSIS received 377 comments on the petition. Marler addressed those comments in a follow up supplement to the petition.  The Center for Science in the Public Interest (CSPI) also petitioned FSIS in January 2021 to “Establish Enforceable Standards Targeting Salmonella Types of Greatest Public Health Concern while Reducing all Salmonella and Campylobacter in Poultry, and to Require Supply Chain Controls.”

FSIS has taken no action. FSIS has written that it will respond after it has thoroughly evaluated the issues raised, as well as the comments submitted on the petitions and any supplement information. That is 16 months since the comments closed. In the meantime salmonellosis continues to sicken and kill people.

In an Oct. 29, 2021, article, ProPublica wrote, “Today, food poisoning sickens roughly 1 in 6 Americans every year, according to the CDC, and salmonella hospitalizes and kills more people than any other foodborne pathogen. Each year, about 1.35 million people get sick from Salmonella. While most recover, more than 400 people die and 26,500 people are hospitalized. Some are left with long-term conditions like severe arthritis and irritable bowel syndrome. Salmonella costs the economy an estimated $4. 1 billion a year, more than any other type of food poisoning.” https://www.propublica. org/article/salmonella-chicken-usda-food-safety

FSIS doesn’t lack for scientific expertise. There are numerous scientists, including chemists, staticians, and microbiologists. Additionally, there is a working relationship with USDA’s Agricultural Research Service (ARS). What the scientists seem to lack is effective communication and influence over the non-science managers. All managers are members of the Senior Executive Service and former members have described the political pressure they experienced. Kudos to the lawyers who have listened to the scientists, not the lobbyists, and implemented food safety reforms.

There is a cartoon by Julian Bilicki with a sign “SCIENCE IS IMPORTANT” but the sign has been amended to read “SCIENCE IS IMPO-TeNT” by a pencil labeled, “LOBBYISTS.”

A non-science FSIS Assistant Administrator recently responded that the Marler and CSPI petitions with their “new approaches” will be considered by the recently announced “plans to explore possible new approaches for addressing Salmonella in poultry.” Those petitions are not “new approaches” but based on decades of established science and previous FSIS actions. For example, after a serotype of Escherichia coli (E. coli) caused meat-borne outbreaks, FSIS declared that serotype, E. coli O157:H7, an adulterant. In response to additional illnesses, FSIS has added other serotypes of E. coli. It’s law based on science.

Decades ago, I congratulated a friend, a veterinarian, who had just finished Senior Executive Service training. I chided him by asking if part of the training was pithing his brain. He laughed and responded, “No, but they made us more politically aware.”

Salmonellosis is a serious food safety disease. The science in the petitions is solid. Outbreak serotypes are ordinarily injurious in the hands of ordinary citizens. It is long past time for FSIS managers to be less politically aware and more sensitive to the science and the legal requirement for food safety in the Food Safety Inspection Service.

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Not all Salmonella are alike. Camplyobacter likely similar.

Preharvest economic incentives haven’t eliminated STEC but imagine what the data would be like if there were none. Leafy greens anyone? Scandinavia has accomplished a lot and could do more if tourists would stay home.

Ideally, the best place to eliminate those pathogens would be the last steps before consuming, but not on this planet. Almost four decades of FSIS’ Hot Line, and two decades of Fight Bac have accomplished something but not enough. Slaughter houses cannot eliminate the pathogens coming in.

Maybe a 2Log reduction on a good day. (Cf Berrang’s “fun” paper) Too many slaughterers don’t lean on their suppliers — even the vertically integrated companies. Reminds me of the small grinders when they came under the Salmonella Performance Standard. Many followed the generic guideline and didn’t realize the bugs came in on the trim.

Too many consumers and retail operators are inept at handling food containing pathogens that are ordinarily injurious to public health. (Flippin, Kampelbacher, Woodburn, NAS etc.)

IMHO, more pressure needs to be put on producers. That would reduce the slaughter house burden and the environmental burden. Declare the bugs adulterants, and require slaughterers to send product from a repeat producer to cooking until the producer has a validated, verified control program.

About the author: Carl Custer is an independent consultant for food safety microbiology. He retired from USDA FSIS in 2007 after over 34 years as a bench and a desk scientist. Custer also served as a trainer for FSIS inspectors, the FSIS Hotline, retail processors and inspectors, small farm processors, and country ham processors. He is a lifetime member of the International Food Protection Association (IAFP) and the American Society for Microbiology. He was also a member of the Food Microbiology Research Conference executive board for twelve years and the Chair for two years. For additional details about Custer’s work, click here to read his full author profile.

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Editor’s note: One of our regular contributors, Carl Custer, has been closely watching the investigations into E. coli O157:H7 outbreaks associated with romaine lettuce in the past year. Here he discusses some of the research he has been reviewing in recent days on related topics.

An animal entering a feed lot or other CAFO is similar to your child entering kindergarten. Your child will pick up every cough, cold, or disease — including head lice — prevalent in that facility. For CAFOs, there is an economic and regulatory incentive to prevent and correct any animal diseases and prophylactic antibiotics are frequently administered.

However, for human pathogens, there is little to no incentive for interventions. Thus, these concentrated animal feeding operations (CAFOs) become centers for concentrating human pathogens.

Carlson et al. (1) reported, “Our data contribute to the growing body of evidence indicating that E. coli O157:H7 persists in cattle populations.”

They averred in the conclusion, “Finally, our findings provide evidence that cattle may be more likely to be colonized by E. coli O157:H7 molecular subtypes that demonstrate accentuated human-pathogenic potential, as shown by the enhanced ability of persistent strains to adhere to human intestinal epithelial cells. Additionally, it stands to reason that there is an increased likelihood that these E. coli O157:H7 subtypes are transferred through the production continuum and subsequently into the human population because of their increased prevalence in feedlot cattle. Our results highlight the importance of preharvest food safety interventions to reduce the load of E. coli O157:H7 that enters the human food supply and support the conclusion that such efforts should be targeted at strains that persist in cattle populations which seem to represent the greatest risk to human health.”

Supporting Carlson, Worley et al.(18) reported in 2017, “Within farms, generally one or a few lineages were found, even when the rate of isolation was high. On farms with high isolation rates, a single clonal lineage accounted for most of the isolates.”

Pianciola and Rivas, in a 2018 review (12) comparing the genes of E. coli O157 strains in humans and cattle wrote, “The characteristics of the strains that cause disease in humans reflect the predominant genotypes in cattle in each of the countries analyzed.”

These three papers show that CAFOs for cattle are reservoirs for human pathogens, especially Shiga Toxin positive Escherichia coli (STEC).

Carlson, Brandon A., Kendra K. Nightingale, Gary L. Mason, John R. Ruby, W. Travis Choat, Guy H. Loneragan, Gary C. Smith, John N. Sofos, Keith E. Belk. 2009. “Escherichia coli O157:H7 Strains That Persist in Feedlot Cattle Are Genetically Related and Demonstrate an Enhanced Ability To Adhere to Intestinal Epithelial Cells” Applied and Environmental Microbiology. 75: 5927–5937 doi:10.1128/AEM.00972-09

Pianciola, Luis, and Marta Rivas. 2018. “Genotypic Features of Clinical and Bovine Escherichia coli O157 Strains Isolated in Countries with Different Associated-Disease Incidences, Microorganisms” 10.3390/microorganisms6020036, 6, 2, (36).

Worley JN, Flores KA, Yang X, Chase JA, Cao G, Tang S, Meng J, Atwill ER. 2017. “Prevalence and genomic characterization of Escherichia coli O157:H7 in cow-calf herds throughout California” Appl Environ Microbiol 83:00734-17. https://doi.org/10.1128/AEM.00734-17.

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Editor’s note: This is the second of a two-part opinion piece. To read part one, please click here.

In the previous article, I wrote about the decades-old public health problem of poultry-borne salmonellosis. This article will propose declaring the virulent strains that are pathogenic to humans as adulterants and the benefits of doing so.

Regulatory policies for other foodborne pathogens recognize consumer’s inability to handle them. The Code of Federal regulations, 9 CFR 311.2-39 describes a number of conditions for declaring meat carcasses adulterated, including: tuberculosis, arthritis, and odors. The poultry regulations 9 CFR, 381.80 et seq are similar. The Meat Inspection Regulations, 9 CFR 315.2 permit some meat products that are found adulterated under 311 to be passed for cooking – under the oversight of federal inspections, not in consumers’ kitchens. In 1995, the top administrator of the USDA’s Food Safety and Inspection Service (FSIS), Craig Reed, use that principle in his letter permitting lots of ground beef containing Escherichia coli O157:H7 to be cooked in a federal establishment – not in consumers’ kitchens.

Treatment of raw meat and poultry by cooking, irradiation, or high pressure processing would eliminate consumer exposure to those pathogens. However, one of the primary sources of foodborne pathogens now is contaminated produce. A growing body of scientific literature indicates a major source of these pathogens is food animal production via air ², water ¹, and manure ⁴. (These are only three recent papers of many). The 2018 meeting of the International Association for Food Protection (IAFP) in Salt Lake City had more than 20 sessions addressing preharvest contamination of soil, water and produce. There is also a large body of scientific literature on preharvest interventions in animals including isolation, competitive exclusion, probiotics, prebiotics, and vaccination. 

Interventions cost and thus, producers need incentives. Incentives include altruism, regulations, customer specifications, and litigation. A 2018 IAFP Round Table “RT9: Do Lawsuits Play a Productive Role in Advancing Food Safety?” suggested that customer specifications and regulations produced faster results; lawsuits were too far in the future. The COSTO and Walmart speakers said customer specifications are effective. Regulation has had some effect on E. coli O157:H7 in beef, but certainly not eliminated it in either commerce or preharvest.⁶ One can only speculate what the results would be if FSIS had not declared it an adulterant in 1994. We know more each year what the effect is of not declaring outbreak strains of Salmonella as adulterants.

The FSIS has the legal means to prevent these adulterants from entering commerce. The Meat and Poultry Inspection Acts ^8-9 empower FSIS inspectors to conduct ante mortem and post mortem inspection of all animals before processing them into food. Traditionally, that has been visual inspection but not always. FSIS’s 2013 “Compliance Guide For Residue Prevention” uses laboratory results to compile a list, “The Residue Repeat Violator List.” It is composed of suppliers who have had more than one residue violation in the preceding 12 months. Thus, animals from a producer on that list present a “hazard reasonably likely to occur.” The HACCP (Hazard Analysis and Critical Control Point) rules require establishments to have controls to prevent any product with violative residues from entering commerce. Failure to do so is a violation of 9 CFR 417.6. FSIS can sample carcasses or live animals and the laboratory will report any violation to Field Operations for action. 

The principle used for residues could be applied to outbreak strains of certain bacterial pathogens also. These strains are adulterants as defined by both the Inspection Acts and the Code of Federal Regulations. FSIS routinely samples carcasses and products for pathogenic bacteria. When an outbreak strain is detected and traced back to an establishment, the establishment can identify the producer and that producer would be put on a “Adulterant Carrier List.” Future animals from that producer and their products must either be treated to inactivate any adulterants or tested (ICMSF Case 15) until the producer has implemented validated controls and verified their effectiveness to prevent future contamination. If the establishment cannot identify the producer, then all product from that establishment would be treated or tested under ICMSF Case 15 to prevent any adulterants from entering commerce.

This would be a harsh rule and FSIS would likely be sued by the industry. The outcome should be similar to Texas Food Industry Ass’n v. Espy⁷ where E. coli O157:H7 was found to be an adulterant in ground beef because consumers would eat the product rare. So why not Salmonella? The difference would be that FSIS could use the half century of scientific findings that cross contamination within consumer’s kitchens is a major source of foodborne illnesses, not just undercooking. Thus poultry and other meat products would be included.

The outcome of FSIS promulgating such a regulatory policy would be that preharvest control of pathogenic bacteria in food animal production would begin to be addressed. This action would begin to reduce the environmental contamination that reaches produce fields via waterways and even highways⁵.

Assays for pathogens have advanced rapidly in the past decade³. Methods are more rapid, sensitive, and specific. The FSIS, processors, and producers can use these methods to rapidly verify that interventions are working and adulterants are not being found in products.

It would be wonderful if altruism was the incentive for preventing adulterants from entering commerce. Alas, we do not live in that world. But let us take USC 602 to heart and apply it to preharvest control.

 References

¹. Alegbeleye OO, Singleton I, Sant’Ana AS. 2018. Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: A review. Food Microbiology. 73: 177-208. https://doi.org/10.1016/j.fm.2018.01.003

². Berry ED, Wells JE, Bono JL, Woodbury BL, Kalchayanand N, Norman KN, Suslow TV, López-Velasco G, Millner PD. 2015. Effect of proximity to a cattle feedlot on Escherichia coli O157:H7 contamination of leafy greens and evaluation of the potential for airborne transmission. Appl Environ Microbiol 81:1101–1110. doi:10.1128/AEM.02998-14.

³. Besser, John M. 2018. Salmonella epidemiology: A whirlwind of change. Food Microbiology 71:55-59.

⁴. Heredia, Norma, Santos, García. 2018. Animals as sources of food-borne pathogens: A review. Animal Nutrition. In Press  https://doi.org/10.1016/j.aninu.2018.04.006

⁵. Seedorf J, Schmidt RG.. 2017.  The simulated air flow pattern around a moving animal transport vehicle as the basis for a prospective biosecurity risk assessment. Heliyon 3:00358

⁶. Swaggerty, Christina L., Ester Grilli, Andrea Piva, Nicolae Corcionivoschi, Steven C. Ricke, Todd R. Callaway. 2018. The First 30 Years of Shiga Toxin–Producing Escherichia coli in Cattle Production: Preharvest Intervention Strategies.  Food and Feed Safety Systems and Analysis- Chapter 8. Pages 133–151 https://doi.org/10.1016/B978-0-12-811835-1.00008-7

⁷. Texas Food Industry Ass’n v. Espy, 870 F. Supp. 143 (W.D. Tex. 1994) US District Court for the Western District of Texas – 870 F. Supp. 143 (W.D. Tex. 1994) December 13, 1994

⁸. 21 U.S. Code § 455. Inspection in official establishments (Poultry Inspection)

⁹. 21 U.S. Code § 603 – Examination of animals prior to slaughter; use of humane methods (Meat Inspection)

About the author: Carl Custer is an independent consultant for food safety microbiology. He retired from The U.S. Department of Agriculture’s FSIS in 2007 after more than 34 years as a bench and a desk scientist. The food safety issues he worked on include:

• 

  Inhibition of Clostridium botulinum;

• Inhibiting nitrosamine formation;
• Analysis and inactivation of Trichinella spiralis;
• Physics and microbiology of cooling heated foods;
• Thermal and non-thermal inactivation of bacterial pathogens in traditional and ethnic foods;
• Predictive microbiology;
• The microbiology and safety of fermented and dry-cured meat products; and
• HACCP development and implementation for both processing and slaughter

These issues included developing the scientific basis for regulatory policy development and rule promulgation. Carl also served as a trainer for FSIS inspectors, the FSIS Hotline, retail processors and inspectors, small farm processors, and country ham processors. Custer is a lifetime member of the International Food Protection Association (IAFP) and the American Society for Microbiology.  He was also a member of the Food Microbiology Research Conference executive board for twelve years, serving as the chair for two years.

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Editor’s note: This is the first of a two-part opinion piece.

In recent days the CDC and FSIS updated information on a continuing salmonellosis outbreak connected to raw and live turkeys. Since July 19 announcement of the outbreak, 74 more people from 26 more states have been reported.

That brings the totals, as of Nov. 5, to 164 infected people from 35 states. Sixty-three have been hospitalized and one person has died. Of 135 people with information available, 63 of them, or 47 percent, have been hospitalized. That is a high rate; this is a virulent strain highly pathogenic to humans. 

This outbreak is similar to the 2013-2014 outbreak from Salmonella Heidelberg. CDC reported 634 persons were infected with seven outbreak strains in 29 states and Puerto Rico; 38% of ill persons were hospitalized, and no deaths.

Salmonellosis from virulent strains borne by poultry is a decades old continuing problem. According to the definitions in the meat and poultry inspection acts,^1.2. these Salmonella strains pathogenic to humans are adulterants. The cases and outbreaks prove they are ordinarily injurious to public health. FSIS has been reluctant to name them as adulterants, sometimes citing APHA vs Butz.³ However, that court decision was based in part on a letter written by USDA in August 1971. That letter wrongly averred that consumers were knowledgeable and competent. It had no scientific validity and was contrary to a 1970 USDA committee’s finding on a 1969 NAS report “An Evaluation of the Salmonella Problem.”¹¹ and a USDA report evaluating that NAS report.¹⁰

Depending on consumers to safely handle raw meat and poultry contaminated with virulent pathogens has failed time and again. The CDC report continues with “Advice to Consumers and Retailers.” This is helpful to CDC, FSIS, and the poultry industry. Decades of educational programs by federal, state and private entities show little progress. A half century of scientific opinion and research demonstrate that most consumers are inept. Here are a few examples:

In 1963 Kampelmacher ⁴ wrote, “The real problem under discussion is: are poultry products a potential danger to public health, and if so, what objective criteria can be applied in the assessment of this danger? … However, the public is usually badly informed on the possible danger of poultry and poultry products to public health. Educating the public on these matters is a  difficult task. ” “In contrast to red meat, raw poultry is not consumed or prepared in any country. The danger lies in the processing, starting with the producers of poultry products and ending with the consumer.” 

Decades later, Kosa concluded “Based on the survey findings, we conclude that education is needed to improve consumer handling practices for raw poultry to decrease illness attributed to Salmonella and Campylobacter in raw poultry products.”⁹ 

This summer, at the 2018 International Association for Food Protection meeting, Quinlan presented: “Mishandling of Poultry Products by Consumers: Identification of Gaps in Knowledge and Safe-handling Practices of Raw Turkey.” ⁸ The talk focused on a survey of consumers cooking turkey. Contrary to recommendations, a significant number washed turkeys, cooked with stuffing inside the bird, and held the cooked turkey at room temperature for more than two hours before serving. 

These three examples underline the need for better consumer education and training. There are many other scientific papers on consumer mishandling and – even after more than three decades of USDA’s Hot Line and others’ initiatives. These scientific results give lie to the frequent chant “just cook it” often on the internet. 

The attention given to cooking ignores the greater threat of cross contamination in kitchens. Echoing Kampelmacher, in 2009, Luber, citing 58 papers, wrote, “In conclusion, cross-contamination events from activities such as use of the same cutting board for chicken meat and salad without intermediate cleaning or spreading of pathogens via the kitchen environment seem to be of greater importance than the risk associated with undercooking of poultry meat or eggs.” Her paper currently has 108 citations, eight in 2018 so far. 

Virulent strains of Salmonella pathogenic to humans is an old problem. One solution would be to declare them adulterants and thus provide a regulatory incentive for control.

References

^1.21 U.S.C. 453 – Definitions: (g) The term “adulterated” shall apply to any poultry product under one or more of the following circumstances:

(1) if it bears or contains any poisonous or deleterious substance which may render it injurious to health; but in case the substance is not an added substance, such article shall not be considered adulterated under this clause if the quantity of such substance in or on such article does not ordinarily render it injurious to health;

^2. 21 USC § 601 – Definitions (m) The term “adulterated” shall apply to any carcass, part thereof, meat or meat food product under one or more of the following circumstances:

(1) if it bears or contains any poisonous or deleterious substance which may render it injurious to health; but in case the substance is not an added substance, such article shall not be considered adulterated under this clause if the quantity of such substance in or on such article does not ordinarily render it injurious to health; 

^3. American Public Health Association et al., Appellants, v. Earl Butz, Secretary of Department of Agriculture, et al.. United States Court of Appeals, District of Columbia Circuit. – 511 F.2d 331. Argued Jan. 22, 1974.Decided Dec. 19, 1974.Rehearing En Banc Denied April 9, 1975

^4. Kampelmacher, E. H. (1963). Public health and poultry products.  British Veterinary Journal 119, 110.

^5. 9 CFR 311 Disposal of Diseased or Otherwise Adulterated Carcasses and Parts. 

^6. 9 CFR 315.2  Carcasses and parts passed for cooking; utilization for food purposes after cooking.

^7. Luber, Petra. 2009. Cross-contamination versus undercooking of poultry meat or eggs — which risks need to be managed first?.  International Journal of Food Microbiology 134 (2009) 21–28. 

^8. Quinlan, Jennifer J. 2018. Mishandling of Poultry Products by Consumers: Identification of Gaps in Knowledge and Safe-handling Practices of Raw Turkey. T6-07 Tuesday, July 10, 2018 10:30 AM – 10:45 AM. International Association for Food Protection. Salt Palace Convention Center – Room 151 D-G

^9. Kosa, Katherine M.; Cates, Sheryl C.; Bradley, Samantha; Chambers IV, Edgar; Godwin, Sandria. 2015. Consumer-Reported Handling of Raw Poultry Products at Home: Results from a National Survey. J. Food Prot. 78:180-186. 

^10. Microbiological Subgroup of the USDA Food Safety Committee.  1970.  Food Protections by the Department of Agriculture.  A Review of the NAS-NRC Report. “An Evaluation of the Salmonella Problem”

^11. National Academy of Sciences/National Research Council/Committee on Salmonella. 1969. An Evaluation of the Salmonella Problem. Prepared by the Salmonella Committee of the National Research Council, Washington, DC.: National Academy of Sciences, Publication No. 1683.

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In the Spring of 2017 while sprinkling balsamic vinegar over chopped romaine lettuce, I wondered if anyone had published on the bactericidal effect of vinegar on lettuce. That acetic acid is the most lethal of the organic acids is well known.

In addition to the most recent outbreak, (Marler 2018b) there have been several outbreaks involving lettuce (Marler 2018a). Thus a quick search of: Salmonella Vinegar Salad yielded Faith et alia 2012. Because they didn’t include Escherichia coli O157:H7 and the recent popularity of that pathogen in lettuce, there is room for additional work.

Therefore, I emailed some fellow food microbiologists with my findings averring there is still room for advancement of the science. It would be a good project for Extension and they might become as famous as Jillian Clarke or Robyn C. Miranda for their work on the “five second rule.” (Co-authors were Hans Blaschek and Don Schaffner.) 

As the responses were lukewarm, I pursued this literature search. My fellow food microbiologists recommended that I develop the article into a paper for “Food Protection Trends.” Alas, requests for comments on FSIS’ proposed poultry and swine modernization have taken my free time until this outbreak.

Thus, this short article on making lettuce safer in the home. There are many opportunities and challenges to make lettuce safer at preharvest and before it enters homes but that is another project the Berry Et alia 2015 stimulated for me.

This is not a complete review but papers that would be useful to consumers. They are summarized in chronological order.

First:
Before treating your lettuce or other fresh greens, remove broken or bruised leaves. The breaks enable pathogens to enter the cells and thus, become protected from the lethal effect of the vinegar or whatever antimicrobial you use. Additionally, the liquid from broken or bruised leaves aids the multiplication of both good and bad bacteria associated with the produce (Takeuchi & Frank 2000, Brandl 2008).

Washing the leaves may reduce any unattached bacteria but has a poor effect on removing attached bacteria. There are many ways to sanitize or disinfect salad greens. Irradiation, cold plasma, electrolyzed water, and chlorine come to mind. But these are not readily available in most home kitchens. Thus, the purpose of this article: To review current science and offer practical recommendations to improve the safety of salads.

Second:
Spoiler alert, vinegar kills pathogenic bacteria. Fans of the Law of Mass Action, will be happy that vinegar’s lethal effect is dependent on time, temperature, and the concentration of acetic acid (usually 6%). Balsamic vinegar, with its additional phenols is the cat’s pajamas of lethality. 

Third:
There’s plenty of science on the effect of vinegar. 

Entani et alia 1998, was a Japanese team concerned about a 1996 outbreak of Escherichia coli O157:H7. They wrote, “Vinegar had a bactericidal effect on food-borne pathogenic bacteria including EHEC 0157:H7.” They tested the vinegars on the surface of nutrient agar, not lettuce.

“Among three kinds of vinegar solutions, vinegar stock solution (acetic acid concentration 10%), a twofold dilution (5% acetic acid) and a fourfold dilution (acetic acid concentration 2.5%), the time necessary for inactivation of EHEC 0157:H7 NGY-lO at 30°C was 1 min, 25 min, and 150 min, respectively (measured as the time required to decrease colony forming units from 2.0 x 10⁶ CFU/ml to <2.0 x 10¹ CFU/ml).”

Wu et alia 2000, at the University of Georgia and the Centers for Disease Control and Prevention, prompted by a 1998 shigellosis outbreak, treated parsley. The parsley, either chopped or whole was inoculated with three strains of Shigella sonnei. The treatments were straight vinegar, diluted vinegar or Na hypochlorite 0 to 200 ppm free chlorine for 5 min at 4°C or 21°C. Undiluted vinegar (5.2% or 7.6%) or > 150 ppm Cl reduced the S. sonnei population on whole leaves by over 6 Log₁₀. 

Vijayakumar and Wolf-Hall 2002, tested three organic acids and diluted bleach on iceberg lettuce leaves in flasks at room temperature and at 4°C. “Diluted solutions of various household sanitizers (apple cider vinegar , white vinegar , bleach, and a reconstituted lemon juice product) . . . 35% white vinegar (1.9% acetic acid) was the most effective in reducing E. coli levels (with a 5-log 10 reduction after 5 min with agitation and after 10 min without agitation),” they wrote. 

Chang and Fang 2007, from the Department of Health, Taiwan, treated shredded iceberg lettuce with full strength rice vinegar (5% acetic acid) and dilutions on E. coli O157:H7. Five minutes at 25°C yielded a 3 Log₁₀ reduction. Diluted vinegar containing 0%, 0.05%, or 0.5% acetic acid had no effect in eliminating E. coli O157:H7. 

Yang et alia 2009, at Colorado State University, tested several household chemicals in suspensions against Listeria monocytogenes, E. coli O157:H7, and Salmonella Typhimurium. “The efficacies of household compounds against pathogens decreased in the following order: 0.0314% sodium hypochlorite > 3% hydrogen peroxide > undiluted vinegar and 5% acetic acid > 5% citric acid > baking soda (50% sodium bicarbonate). The sensitivity of the tested pathogens to all tested household compounds followed the sequence of Salmonella Typhimurium > E. coli O157: H7 > L. monocytogenes.” 

Faith et alia 2012, used cocktails of either Salmonella sp. or L. monocytogenes on intact spinach leaves. The commercial vinegars were: rice vinegar, distilled white vinegar, white wine vinegar, apple cider vinegar, red wine vinegar, and balsamic vinegar with a commercial 100% natural canola oil. The spinach was treated in a Whirl-Pak bag by adding 20 ml of vinegar (diluted 50% with either water or oil) and held at room temperature for 30 minutes. The vinegars reduced the resident microbiota, primarily Gram -, about 3 logs₁₀. For the pathogen trials, they diluted the vinegar 1:2 with oil. Traditionally, a vinaigrette consists of 3 parts oil and 1 part vinegar.

The authors wrote, “Allowing the mixture to sit at room temperature for at least 20 min resulted in a substantial reduction (up to 2.0 log CFU) in numbers of S. enterica. Vinegar and oil caused a limited reduction in CFU (0.5 log) for spinach leaves inoculated with a cocktail of Listeria monocytogenes strains.”

Sirsat and Neal 2013, promoted Aquaponics over soil grown lettuce. They tested undiluted white vinegar, apple cider vinegar, red wine vinegar and lemon juice. Adding Salmonella or E. coli cocktails to undiluted vinegar or juice showed white vinegar was the most lethal. Treating inoculated lettuce with straight or diluted white vinegar (5% or 2.5% acetic acid) for 60 seconds resulted in a 2-3 Log₁₀ reduction of Salmonella, E. coli, and coliforms. Their paper is open access so you can look at their Fig 3. 

Ramos et alia 2014, used L. monocytogenes on iceberg lettuce. Rice, fruit, white, red wine, cider and balsamic vinegar were tested with the agar diffusion method. Balsamic vinegar was superior. The treatment solutions were: balsamic vinegar, white vinegar, and acetic acid diluted to 5.87%. The balsamic vinegar was also 5.87% acetic acid and the white vinegar 6.15%. These solutions were further diluted by 15, 20, 37 and 50% (v/v). The inoculated lettuce (~50 g) was added to one liter of a diluted vinegar for 15 minutes at room temperature, then removed and placed on sterile absorbent paper. All trials were in triplicate. 

The results show that balsamic vinegar produced the greatest reduction except when diluted by 15% where white vinegar was better (0.9 Log₁₀ vs 0.9 Log₁₀). The greatest reductions were with the 50% vinegar dilutions.

The authors wrote, “The maximum observed log reduction of L. monocytogenes was 2.15 ± 0.04 for balsamic vinegar (50% (v/v)), 1.18 ± 0.06 for white wine vinegar ((50% (v/v)) and 1.13 ± 0.06 for acetic acid ((50% (v/v)). Washing with water only reduces 0.05 ± 0.04 log CFU/mL of L. monocytogenes numbers.” The authors citing previous papers opined that, “The stronger bactericidal effect of balsamic vinegar may be also related to the presence of compounds with antimicrobial properties resulting from the fermentation of grape juice and from grape juice itself. It is known that grapes contain a number of phenolic compounds that exhibit antilisterial activity, particularly polymeric phenolic compounds: resveratrol, vanillic acid, caffeic acid, gallic acid and flavonoids (rutin and quercetin)”

Poimenidou et alia 2016, treated cut strips of romaine lettuce or spinach by washing with several solutions. The solutions were: water, a distilled aqueous extract of oregano, Na hypochlorite (60 and 300 ppm free chlorine), Citrox® (0.5%), vinegar (6% acetic acid), 2% lactic acid, and double combinations of Citrox, lactic acid and oregano. The treatment was immersing 310g of inoculated leaves in two liters of solution for either 2 or 5 minutes at room temperature. After treatment, half of the leaves were rinsed in ice water. All trials were repeated twice in triplicate. They measured both E. coli O157:H7 and the resident microbiota.

“For each treatment, samples of 20 g each were analyzed: (i) before treatment to estimate the attached population; (ii) after treatment, to assess the immediate antimicrobial effect of the washing solutions, and (iii) after 7-day storage at 5 °C.” Thus, 18 samples per treatment. 

The E. coli O157:H7 (log CFU/g) reductions were:

• Water: 0.7 ± 0.1 on spinach and 0.7 ±0.5 on lettuce
• Na hypochlorite 60 ppm: 0.5–1.3 log CFU/g. 
• Na hypochlorite 300 ppm: 1.7 on spinach
• 2% lactic acid: 3.6 on spinach, 2.1 on lettuce, after 7 days 2.3.
• Citrox: 0.7–1.3 on spinach, 0.9–1.5 on lettuce, after 7 days 1.3 spinach 1.8 lettuce
• Oregano: ~0.7 on spinach, 1.5–2.1 on lettuce, after 7 days on lettuce undetectable 

Vinegar gave the greatest Log₁₀ reductions: 

• 2.0–2.4 on rinsed spinach, 4.2-4.3 on non-rinsed spinach, undetectable after 7 days.
• 1.8-2.3 on rinsed lettuce, 2.5-3.9 on non-rinsed lettuce, undetectable after 7 days.

The treatments similarly reduced the resident microbiota.

Park et alia 2016, treated laver, a seaweed with dilutions (5%, 10%, & 15%) of vinegar containing 6% acetic acid. They inoculated the laver with MNV-1, a Norovirus surrogate, or E. coli. Treated lavers were sampled after 1, 3, 5, and 7 days of storage at 4°C. The MNV-1 titer gradually decreased with time and vinegar concentration but there was little difference between treatments and water only. OTOH, E. coli survival was greatly affected by the vinegar concentration and time. The E. coli count in 0% vinegar increased slightly, 0.6 Log₁₀ in 7 days. For vinegar-treated laver the reductions were 3.4 Log₁₀ for 15%, 2.5 Log₁₀ for 10%, and 2.0 Log₁₀ for 5% vinegar after 7 days. 

Bakir et alia 2017, tested 18 vinegars with the disc diffusion method. They used Salmonella Typhimurium, Staphylococcus aureus, and Escherichia coli. The vinegars included 15 different fruits or substrates from three different companies using commercial submerged fermentation of diluted juice or a traditional method. Balsamic vinegar also had the highest antimicrobial activity. The authors concluded, “Antibacterial activities of vinegars could partly be related to both their acetic acid contents and the pH values, and also to their phenolic contents.”

Gómez-Aldapa et alia 2018, compared the antibacterial effect of Hibiscus sabdariffa calyx extracts (water, methanol, acetone, and ethyl acetate), sodium hypochlorite (200 mg/L), acetic acid (0.5%), and colloidal silver (~3.5 mg/L)). The produce was romaine lettuce, spinach, and coriander leaves (A.K.A. cilantro). They used thirteen different bacteria including: five E. coli pathotypes, L. monocytogenes, Shigella flexneri, Salmonella, and Vibrio cholerae O1. Their tables 1-3 present the extensive results. Their extracts produced 2-3 Log₁₀ reductions. Diluted acetic acid reduction were ~1 Log₁₀, similar to those of Chang and Fang 2007 where diluted vinegar containing 0%, 0.05%, or 0.5% acetic acid had no effect. 

My conclusions
Vinegar is a useful household sanitizing agent for leafy greens and other produce. But: What about blue cheese or Russian dressing? I don’t know. Haven’t seen any research. Personally, I would douse the lettuce with plain white vinegar then finish chopping the other salad ingredients. Finally give the greens a quick water rinse, shake (or spin), then toss the remaining ingredients with your favorite creamy dressing.  

Greater time, temperature, or concentration increases the bactericidal effect. There are differences in the effect on leaves. Leaf surfaces differ in hydrophobic and hydrophilic substances. These affect both bacterial attachment and the ability of the treatment to contact the attached bacteria – or – virus.  

REFERENCES:

Bakir, S., Dilara Devecioglu, Selma Kayacan, Gamze Toydemir, Funda Karbancioglu-GulerEsra Capanoglu. 2017. Investigating the antioxidant and antimicrobial activities of different vinegars. Eur Food Res Technol. 243: 2083. https://doi.org/10.1007/s00217-017-2908-0

Berry ED, Wells JE, Bono JL, Woodbury BL, Kalchayanand N, Norman KN, Suslow TV, López-Velasco G, Millner PD. 2015. Effect of proximity to a cattle feedlot on Escherichia coli O157:H7 contamination of leafy greens and evaluation of the potential for airborne transmission. Appl Environ Microbiol 81:1101–1110. doi:10.1128/AEM.02998-14. OPEN ACCESS

Brandl MT. 2008. Plant lesions promote the rapid multiplication of Escherichia coli O157:H7 on postharvest lettuce. Appl Environ Microbiol. 74: 5285-9. doi: 10.1128/AEM.01073-08. OPEN ACCESS “The results of this study indicate that plant tissue damage of various types can promote significant multiplication of E. coli O157:H7 over a short time and suggest that harvesting and processing are critical control points in the prevention or reduction of E. coli O157:H7 contamination of lettuce.”

Chang JM, Fang TJ. 2007. Survival of Escherichia coli O157:H7 and Salmonella enterica serovars Typhimurium in iceberg lettuce and the antimicrobial effect of rice vinegar against E. coli O157:H7. Food Microbiol. 2007 Oct-Dec;24(7-8):745-51. Epub 2007 Mar 15.

Critzer FJ, Doyle MP. 2010. Microbial Ecology of Foodborne Pathogens Associated with Produce. Curr Opin Biotechnol. 2010 Apr;21(2):125-30. doi: 10.1016/j.copbio.2010.01.006. Epub 2010 Feb 9.

Entani E, Asai M, Tsujihata S, Tsukamoto Y, Ohta M. 1998. Antibacterial action of vinegar against food-borne pathogenic bacteria including Escherichia coli O157:H7. J. Food Prot. 61:953–959. OPEN ACCESS

Faith, Nancy G.; Waldron, Toria; Czuprynski, Charles J. 2012. Reduction in Resident Microflora, and Experimentally Inoculated Salmonella enterica, on Spinach Leaves Treated with Vinegar and Canola Oil. J. Food Protec. 75: 567-572. OPEN ACCESS

Gómez-Aldapa, Carlos A., Esmeralda Rangel-Vargas, Ma. Refugio Torres-Vitela, Angélica Villarruel-López, Otilio A. Acevedo-Sandoval, Alberto J. Gordillo-Martínez, Angélica Godínez-Oviedo, and Javier Castro-Rosas. 2018. Antibacterial Activities of Hibiscus sabdariffa Extracts and Chemical Sanitizers Directly on Green Leaves Contaminated with Foodborne Pathogens. J Food Protec. 81:209-217. 

Kelebek, H., Kadiroğlu, P., Demircan, N.B., Selli, S. 2017. Screening of bioactive components in grape and apple vinegars: Antioxidant and antimicrobial potential. Journal of the Institute of Brewing. Volume 123, Issue 3 July 2017 Pages 407–416. http://onlinelibrary.wiley.com/doi/10.1002/jib.432/abstract

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Poultry slaughter would flunk HACCP 101. The primary hazards from raw poultry are the pathogens Salmonella and Campylobacter spp. FSIS visible poultry inspection does not yet detect those hazards. The visible conditions that FSIS inspectors can detect are based on 19th and 20th century paradigms that visible disease conditions are the public health hazards. Four decades of CDC data refute that.

Regarding fecal contamination, in consumers’ kitchens, it’s not undercooking poultry, it’s cross contamination Here is one review: Luber, Petra. 2009. Cross-contamination versus undercooking of poultry meat or eggs — which risks need to be managed first? Intl. J. Food Microbio. 134: 21–28. That review is supported by other papers demonstrating the incompetence of ordinary consumers.

Additionally, much of the fecal contamination is invisible. When the defeathering machine removes feathers, the fingers compress the carcasses pumping out feces from the cloaca. The fingers then press some of that fecal material into the emptied feather follicles — where it remains invisible to inspectors.

A USDA Agricultural Research Service (ARS) paper supporting washing visible feces from chicken carcasses indicates invisible feces contaminate carcasses (Blankenship, L. C. et al. 1993. Broiler Carcass Reprocessing, a Further Evaluation. J. Food Prot. 56: 983-985.).

In the early 90’s, I proposed a research project for ARS using a chemical indicator such as coprostanol to detect invisible fecal contamination on beef carcasses. Coprostanol is used as a biomarker for human fecal matter in the environment. One ARS microbiologist commented that assay could destroy the poultry industry.

I replied yes, that is why I’ve emphasized beef. Jim Kemp later developed an assay for bovine feces based on a grass metabolite.

Those invisible feces and bacteria are the reason that ARS and others have indicated for over three decades that pathogens entering a slaughter establishment will emerge on the product. Here is a recent paper: Berghaus, Roy D.et al. 2013 Enumeration of Salmonella and Campylobacter spp. in Environmental Farm Samples and Processing Plant Carcass Rinses from Commercial Broiler Chicken Flocks. Appl. Env. Microl.79:4106-4114.

So, those are some of the problems. What are some solutions?

The pathogen problem starts on the farm, grow out, and the hatcheries. Solve that and I suggest that line speeds and visible issues are secondary.  Here is an “ancient” paper on preharvest control: Pomeroy BS, et al. 1989, Studies on feasibility of producing Salmonella-free turkeys. Avian Dis. 33:1-7. There are many other papers.

The problem of implementing preharvest controls is cost. How do you create financial incentives for implementing controls?

I suggest let slaughter establishments bump up line speeds but only for sources that are free of the primary hazards, Salmonella and Campylobacter spp., or, at least free of the clinical strains (Salmonella Kentucky, if free of the virulence genes may be a probiotic). That would provide the financial incentive for implementing controls — and reduce the environmental public health burden of poultry production (many papers on this additional problem.

Happy new year and thanks for bringing this up.

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1. Treat all raw meat and poultry products: In addition to cooking and producing “value added” ready-to-eat products, there are other methods such as high-pressure processing and irradiation. High-pressure processing has come of age in the past decade and is used commercially by several companies. For instance, Cargill reported in December 2011 that it had implemented high-pressure processing to reduce Salmonella in its ground turkey. Irradiation, however, remains controversial in the U.S.
2. Require consumers to be licensed before they can purchase raw meat or poultry products: Many jurisdictions already require retail food establishments to have a person on hand who has successfully received a safe food handling certificate. Extending this to all persons would be a political “hot potato.”
3. Continue to push for lower levels of pathogens on raw meat or poultry products: FSIS has done that for poultry with the new Salmonella Performance Standards and adding a standard for Campylobacter. And, yet, the recent outbreak from Salmonella Heidelberg was traced back to an establishment that met and exceeded the new standard. The standards for meat have not been tightened.
4. Continue the status quo and let the incompetent suffer the consequences: While seeming cruel, it would provide continuing incentives for educational efforts such as those at CDC, FSIS and FDA. It would also not impose a greater burden on producers and growers, and, thus, raise the cost of food.

There are no easy answers, but there are precedents. The U.S. Code of Federal Regulations prescribes keeping some potentially hazardous raw meat and poultry products that could be made safe by cooking out of the hands of ordinary consumers. In 9 CFR 311 and 9 CFR 381K (381.79-381.93), are lists of carcass defects that must be prevented from entering commerce and consumer exposure.  The Meat Inspection Regulations, 9 CFR 315, permit some carcass defects to be cooked in an official establishment but not in consumers’ kitchens. The same could be required of meat and poultry containing known human pathogens. It has been done for STEC in certain beef products and for Salmonella in many products under FDA’s jurisdiction. In a January 10, 2014, article in Food Safety News, reporter Lydia Zuraw wrote, “An agency source told Food Safety News that although some have argued the number of illnesses would have justified action, the law would not have supported it solely because of Salmonella contamination. Zuraw then quoted the source: “The agency is unable to make regulations accomplish goals that the underlying law prohibits us from doing. … The statutory criteria and the court decisions that dictate FSIS’ authority on Salmonella cannot be simply overturned through regulatory action or approving a petition.” Hanlon’s Razor seems applicable; the FSIS source is either ignorant of the law or repeating outdated political opinions. Recommendation FSIS can, and should, declare Salmonella strains linked to CDC outbreaks as adulterants. That these strains are linked to outbreaks demonstrates that they are “ordinarily” injurious to consumers. CDC currently identifies outbreak strains by their PFGE profile. Currently FSIS runs PFGE on all Salmonella isolates from its testing programs and uploads the results to the CDC PulseNet database. Through PulseNet, the agencies may quickly identify any Salmonella strain from a product linked to an outbreak. Whole genome sequencing will offer greater specificity in the near future. FSIS can, and should, adopt the current policy for controlling multiple residue violations (FSIS NOTICE 52-13 and “Compliance Guide For Residue Prevention 2013”) to controlling these pathogens. The program would work the same as the residue control program that has been in effect for decades: When linked to an outbreak strain, the establishment’s product now has that pathogen as a “hazard reasonably likely to occur” under the HACCP regulation, 9 CFR 417. Thus, the establishment’s HACCP program would hold future product until it can either certify that its product does not contain the outbreak strain or the identified product has been designated for a bactericidal treatment in an Official Establishment. When FSIS takes samples for Salmonella testing, the establishment would have the option to identify the producer or producers represented in that sampled lot. Identifying the source of the outbreak strains would lower the establishment’s economic risk by facilitating the future isolation of the producer’s animals from the rest of the establishment’s products. Selecting out positive animal producers would reduce the chance of recalls of adulterated product. It would also enable slaughterhouses to implement procedures such as scheduling positive animals at the end of shifts and designating their products for treatment. The probable outcomes would be that processors would stop buying animals from implicated producers and require that producer to implement programs to eradicate the pathogen, or the producers’ animals would be processed at the end of a shift and sent for cooking or another bactericidal process. By putting the burden on the producer, the source of the adulterating pathogen, it will give producers an economic incentive to begin controlling human pathogens. A side benefit of eliminating outbreak strains in production facilities would be to lessen the exposure of these strains to the environment, including fields, orchards, and waterways. Some producers currently use rapid assays for animal pathogens. Faster and more specific assays can enable producers to test their animals before submitting them for slaughter. Examples of these assays abound in trade shows and the scientific literature. For instance: http://www.ncbi.nlm.nih.gov/pubmed/21908327 and http://www.gapoultrylab.org/wp-content/uploads/2012/08/Waltman%20AVMA%202012.pdf   It is long past time for FSIS to implement the acts, adopt current regulations and policy, and declare those virulent pathogenic strains of Salmonella as adulterants in raw meat and poultry products. The burden for control should be upon the producers. While slaughter establishments can reduce the pathogen load, they do not eliminate the load. USDA’s Agriculture Research Service RRRC has averred for more than two decades that what goes into a poultry slaughter facility comes out. In a recent paper, Berghaus, et al, wrote, “In conclusion, Salmonella and Campylobacter prevalences and loads on the farm were significantly associated with prevalences and loads of the same pathogens at processing. Consequently, management practices that reduce pathogens on the farm would be expected to reduce contamination at processing.” Declaring outbreak strains as adulterants would provide an economic incentive to control them and reflect the Congressional statement of findings in 21 USC 451 and 602: “Unwholesome, adulterated, or misbranded … products impair the effective regulation of … products in interstate or foreign commerce, are injurious to the public welfare, destroy markets for wholesome, not adulterated, and properly labeled and packaged … products, and result in sundry losses to … producers and processors of … products, as well as injury to consumers.” Reference: Berghaus, Roy D., Stephan G. Thayer, Bibiana F. Law, Rita M. Mild, Charles L. Hofacre and Randall S. Singer. 2013 Enumeration of Salmonella and Campylobacter spp. in Environmental Farm Samples and Processing Plant Carcass Rinses from Commercial Broiler Chicken Flocks. Appl. Env. Microl.79:4106-4114

Foodborne Illnesses Attributable to FSIS products/100,000 persons Salmonella 4.88 Lm 0.13 E. coli O157:H7 (sic) 0.32

Thus, the goal for salmonellosis is 15 times greater than the next highest goal. Sadly, one of the actions for the Office of Public Affairs and Consumer Education appears to be apologize for failure: “Implement at least two tactics for providing Salmonella-related food safety messages to the public, including why Salmonella is more challenging to control than other pathogens.” Strains of Salmonella are the most deadly foodborne pathogens. In a 2011 paper on deaths associated with foodborne bacterial pathogens, Barton Behravesh, et alia, stated, “Conclusions. Salmonella and Listeria remain the leading causes of death in the United States due to bacterial pathogens transmitted commonly through food.” In a 2013 update, CDC’s 2011 estimates showed nontyphoidal Salmonella topped the chart of “Domestically Acquired Foodborne Illnesses Resulting In Hospitalization,” with 35 percent of hospitalizations, and the chart of “Illnesses Resulting In Death,” with 28 percent. Those data were taken from FoodNet, but it is not new information. CDC annual reports over the past three decades have shown that salmonellosis is the leading cause of foodborne bacterial deaths. The “specter of botulism” was used to secure the continued use of nitrites, but salmonellosis was deadlier. Before and after E. coli O157:H7 came to regulatory attention, salmonellosis still caused more annual deaths. Listeria monocytogenes dominated the 1990s and is still a tough problem, but the industry has developed and implemented controls. Salmonellosis still reigns supreme. It’s time to dethrone Salmonella. References: Barton Behravesh, Casey; Timothy F. Jones, Duc J. Vugia, Cherie Long, Ruthanne Marcus, Kirk Smith, Stephanie Thomas, Shelley Zansky, Kathleen E. Fullerton, Olga L. Henao, Elaine Scallan, and FoodNet Working Group. 2011. Deaths Associated With Bacterial Pathogens Transmitted Commonly Through Food: Foodborne Diseases Active Surveillance Network (FoodNet), 1996-2005 J Infect Dis. (2011) 204 (2): 263-267 doi:10.1093/infdis/jir263) Flippin, Harrison F. and George M. Eisenberg. 1960. The Salmonella Problem. Trans Am Clin Climatol Assoc. 1960; 71: 95-106. Hornick, R. B. 1974. Jeremiah Metzger lecture: Salmonella infections–newer perspectives of an old infection. Trans Am Clin Climatol Assoc. 1974; 85: 164-174. Microbiological Subgroup of the USDA Food Safety Committee. 1970. Food Protections by the Department of Agriculture. A Review of the NAS-NRC Report. National Academy of Sciences/National Research Council/Committee on Salmonella. 1969. An Evaluation of the Salmonella Problem. Prepared by the Salmonella Committee of the National Research Council, Washington, DC.: National Academy of Sciences, Publication No. 1683. Silliker, J.H. 1982.The Salmonella problem: current status and future direction. Journal of Food Protection. May 1982. v. 45 (7).