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.

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  


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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