Modernization of Poultry Slaughter Inspection



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Comments on USDA Proposed Rule “Modernization of Poultry Slaughter Inspection”


Comments on USDA proposal RIN 0583-2011-0012

Modernization of Poultry Slaughter Inspection

77 Fed Ref 24,873 (April 26, 2012 and 77 Fed Reg, 4,408 (January 27, 2012)

Docket No. FSIS 2011-2012
submitted by Ellen Silbergeld, PhD
I am Ellen K Silbergeld, PhD, and I am submitting these comments as a private citizen who has stakes in this proposed rule as a consumer of US produced poultry products and also as an expert in public health with particular knowledge of food borne illnesses and occupational health and safety in US meatpacking and poultry processing operations For identification purposes I am a professor in environmental health sciences and epidemiology at the Johns Hopkins Bloomberg School of Public Health (JHSPH) in Baltimore MD. Dr Silbergeld has conducted research over the past 10 years, with funded from USFDA, NIH, CDC, and other sources, on exposes to pathogens associated with intensive broiler production in the US. Her laboratory group’s studies have examined exposures to farmers and slaughterhouse workers and consumers and included studies on Enterococci, Staphylococci, E coli, and Campylobacter. This research has been published In leading peer-reviewed journals and it has been presented by invitation at CDC and ICOH (an official organization of the ILO-WHO). We are currently conducting the first analysis of OSHA data on workplace injury and infections among workers in US poultry slaughter and processing plants. A copy of Dr Silbergeld’s professional resume is attached.
I appreciate the extended opportunity to submit comments on this Proposed Rule. I have several concerns about the Rule as proposed with respect toits potential impacts on worker health and safety as well as increased risks of consumer exposure to and infection by pathogens that are already prevalent In broiler poultry products produced and sold in the US. The economic rationale for these proposals is unacceptable in that it considers mainly the savings of reducing inspection and increasing line speeds in poultry slaughter and processing operations without examining costs of workplace injury and illness as well as food borne illnesses among consumers. The proposed rule contains numerous assertions that are not based on evidence, even in cases where scientific studies conducted by USDA provide important evidence. We provide these data in this comment. There is a critical need for both review of existing data and collection of new data to support the assertions in this Proposed Rule prior to finalizing any of the changes in workplace conditions in this proposed regulation.
In this comment, we have cited some of the recent relevant peer reviewed literature, including papers from our research group a Hopkins, but with an emphasis on important publications by scientists at USDA, FDA, and CDC. This highlights the need for continued intra- and inter-agency consultation and expert review prior to promulgating changes with such implications.
Food borne illness: CDC researchers have estimated the burden of food borne illness in the US from major pathogens to include 48 million cases of disease, 128,000 hospitalizations, and 3000 deaths per year (Table 1 from Scharff 2012). The economic burden of food borne illness in the US has been recently estimated to be between $51 and 77 billion per year (Scharff 2012). One of the most prevalent causes of gastroenteritis in the US is the poultry associated pathogen Camplyobacter jejuni (Table 1). Moreover, as noted by CDC, most of the burden of food borne disease outbreaks and hospitalizations is likely due to unidentified food borne pathogens (Scallan et al 2011). New and emerging food borne pathogens continue to be identified, such as methicillin resistant Staphylococcus aureus (MRSA) and Clostridium diifficile (Gould and Limbago 2010; Hanson et al 2011; Waters et al 2011).




Table 1. Burden of food borne illness, by causative pathogen, in terms of annual number of cases (Scharff 2012)

Food borne illness associated with poultry consumption also involves drug resistant pathogens because of the continued use of antimicrobial drugs at sub-therapeutic concentrations as additives to broiler poultry feeds (Angulo et al 2004; Silbergeld et al 2008). The prevalence of drug resistant pathogens in US consumer poultry products (including broiler chickens and turkeys) has been frequently reported by USDA and FDA investigators, as well as by us and other academic researchers (for example, Zhao et al 2012; Price et al 2007; Waters et al 2011; Hanson et al 2011). These draft regulations propose to significantly modify existing programs related to reducing consumer exposure to Salmonella despite compelling FDA data on the prevalence of this pathogen in poultry (Zhao et al 2006). As shown in table 1, a CDC analysis demonstrates that Salmonella infections are the leading bacterial cause of food borne disease in the US. Guo (scientist at the FSIS, USDA) and colleagues estimated the contribution of poultry consumption to the burden of human salmonellosis cases from food sources, and reported that 48% of disease cases were attributable to chicken and 17% to turkey (see figure 1 from Guo et al 2012). As indicated in this figure chicken is the leading source of salmonella infections in the food supply and the risks associated with chicken increased over the period assessed in this study.




Figure 1. Annual consumption and attributable risks of salmonellosis by food

product in the US from 1998 to 2003. Note that risks associated with poultry

increased over the period covered by these data (Guo et al 2012).

Moreover, ending testing for E coli is not appropriate, given USDA studies that demonstrates that this organism can serve as a reservoir or source of transferrable genetic determinants for antimicrobial resistance in food borne pathogens (Glenn et al 2012) well as fundamental knowledge of molecular microbiology (Staider et al 2012). Table 2 illustrates the extent of transferrable multidrug resistant cassettes isolated in E coli from poultry; some of these carry genes for as many as 10 different resistance phenotypes including resistance to the clinically important antimicrobials amoxicillin, sulfamethoxazole, streptomycin, kanamycin, trimethoprim-sulfamethoxazole, tetracycline, ciprofloxacin, cefoxitin, gentamicin, chloramphenicol, and ceftiofur (Glenn et al 2012).



Table 2. Antimicrobial resistance in E coli isolates from poultry, NARMS 2000-2007, indicating extensive multidrug resistance and detection of integrons (Glenn et al 2012).


Worker health and safety: Current conditions, including line speeds, in slaughter/processing plants, are associated with a considerable burden of chronic and acute injury and disability. It is generally agreed that these injuries as well as chronic musculoskeletal diseases and disorders are under reported by the poultry slaughter and processing industry (as reviewed by a 1990 study sponsored by the National Broiler Council (Ortiz and Jacobs 1990)). With these caveats, the following data sources are highly relevant for evaluating the current burden of disease and disability related to work in this industry. A study of poultry processing workers in North Carolina, conducted in 2009-2010, reported that medically diagnosed carpal tunnel syndrome (CPT) was 2.5% more likely than in other manual workers, a highly significant finding (p<0.0001) (Cartwright et al 2012). Moreover, workers on the line were the most likely to be diagnosed with CPT as compared to workers in other jobs in these poultry plants. A 2007 study of women employed in poultry processing in North Carolina observed a 2.4-fold increase in rates of musculoskeletal disorders compared to similar persons not employed in poultry processing (Lipscomb 2007). These findings are similar to a larger study conducted in Sweden in which workers involved in deboning processes had the highest rates of diagnosed CPT (Frost et al 1999). Line speed has been also associated with increased reports of dysmenorrhea in female workers, an indication of work-associated stress. In a study of women working in a French processing plant, workers who reporting working on the line, who were restricted from frequent movement due to line speed, and experienced difficulty keeping up with the line at greater risk of dysmenorrhea compared (Messing 1993).
We are conducting an analysis of industry reports submitted from 2004 to 2008 to OSHA on injuries and infections in poultry processing plants in the US (OSHA 300 reports). These data confirm that occupations in poultry slaughter/processing plants continue to have elevated rates of injuries as compared to the US private industry workforce (BLS 2010). As shown in Table 3, industry-reported injury rates ranged from 4.8 to 14.3 per 100 workers. These high rates are also consistent with an earlier study of four poultry processing plants sponsored by the National Broiler Council (1990). Our study is the first to examine associations between reported injuries and infections in poultry processing workers. As shown in Figure 2, most lacerations and infections were reported by workers in the live hang and cut support jobs, work areas with lines. This is an example of failure to examine and evaluate the evidence from existing studies on a critical topic that will be influenced by this proposed regulation if finalized.

Table 3. Reported injuries (lacerations) and infections among poultry workers reported by nine poultry processing plants to OSHA from 2004 to 2008. Data extracted from OSHA300 reports.




Figure 2. Distribution of industry-reported lacerations and infections by departments in poultry processing plants extracted from OSHA 300reports.


Inter-relatedness of worker and food safety. The issues of worker safety and food safety are intertwined and should be considered in mutual context. That is, allowing changes that impact on worker safety -- such as permitting large increases in line speeds in poultry slaughter and processing -- will also impact food safety. Equally, changing rules that impact on food safety – such as reducing inspections and testing – will increase worker health risks. As noted above, both musculoskeletal injury and acute physical injury rates are highest in those areas of work within poultry processing where line work dominates, demonstrating the importance of understanding line speed as a risk factor for injury. Increasing line speed also increases the likelihood of pathogen contamination in consumer poultry products at two stages, at the first stage (from kill to chill), increased line speed will decrease the available time for visual inspection and the already incomplete process of carcass sanitization through chilling or a brief chlorine or other chemical immersion; and most importantly at the second state by increasing contamination and exposure or workers during product deboning, cutting, and other operations in the processing plant (which is discussed in more detail in the next paragraph). With regard to the first stage, an empirical study by USDA on different immersion chilling methods reported overall reductions in prevalence of Salmonella contamination of carcasses (Berrang et al 2009). However, complete pathogen control has never been achieved. A more recent and comprehensive review and meta-analysis of interventions to reduce Salmonella in processing plants was recently published (Bucher et al 2012). This review drew on studies of intervention trials conducted in the US and other countries. The authors concluded that variations in results precluded detection of significant reductions in contamination by chilling with or without chlorination. They further noted that as the disinfection bath is used, it accumulates pathogens and other contaminants such that over a relatively short period of time no net reduction in carcass contamination is accomplished.
However, the most important aspect of this issue is the complete failure of the Proposed Rule (and in fact HACCP guidelines as well as industry practice) to evaluate pathogen contamination after the chill/rehang step. This is demonstrated in Figure 3 (from Northcutt and Russell 2010). Because of this, we have no information related to worker risks of exposure to pathogens after the chill/rehang step, and in fact we have no data on food borne contamination from this step. The standard methods for assessing contamination control in processing plants rely on measurements taken pre and post chill, sometimes including rehang, but prior to all the cutting, deboning, and other activities that involve workers on the line.  These are the activities that employ the bulk of the workforce in slaughter/processing plants. Thus the data reviewed above are not informative on the impact of line speed changes in terms of worker health safety during the major part of their activities in slaughter/processing nor is it fully informative as to food safety. Given the present conditions of work and lack of pathogen control during the work day, it is clear that even if reductions in pathogen prevalence are achieved between killing and chilling the carcass, there is ample opportunity for contamination (which is never fully controlled, as admitted in USDA’s own studies; see above) to persist and spread through these later stages of processing into consumer products. At present there is relatively little published data on pathogen contamination throughout the processing cycle. A study conducted by the French food safety authority concluded that cross contamination increased over the work day at poultry slaughter plants due to contamination of equipment, work surfaces, and process water Hue et al 2010).



Figure 3. Schematic diagram of poultry slaughter and processing. The red box (added) indicates the processes not covered by current methods of assessing pathogen control. Schematic from Northcutt and Russell, University of Georgia College of Agriculture Department of Poultry Science http://www.caes.uga.edu/applications/publications/files/pdf/B%201155_4.PDF


In fact, USDA knows that there is extensive (re)contamination of poultry products before they are sealed at the processing plant because of the high prevalence of pathogen contamination in consumer products reported in published studies by US FDA and academic researchers (including ourselves) There is also evidence for worker exposure to pathogens on poultry products after the chiller, as evident in our study of



coincident risks of lacerations and infections in poultry workers (figure 2). Infections were highly associated with lacerations caused by contact with the product (e.g., poultry bones) rather than with tools or equipment, indicating the role of contaminated poultry meat and carcasses in infectious diseases among workers.
More fundamentally, the current USDA HACCP strategy for testing pathogen control at the pre/post chill stages gives the lie to USDA’s vaunted HACCP program of protecting consumers “from farm to fork.” Conditions in food animal production at the farm level are increasing these risks, rather than reducing them (Silbergeld 2008), which leaves the processing plant as the main point of infection control. As discussed above, there is no assessment that covers the entire processing cycle. This concept of HACCP does not protect workers or consumers who are exposed after the chill stage and it provides no insight to support the assumption of this Proposed Rule that line speed increases will not affect either worker or food safety.
Because the processing plant remains a key part of USDA's vaunted HACCP program to protect the American public -- workers and consumers – from exposure to and infections by pathogens in the food supply, current conditions demand increased vigilance rather than pandering to a miscalculation of benefits and costs. The appropriate response to current conditions of worker injury and food safety is to increase, rather than to decrease, requirements related to both and to avoid changes that will increase risks of injury to workers and the prevalence of food borne pathogens in the consumer food supply.
I recommend withdrawal of these proposed regulations as unsupported by empirical data and likely to increase risks of workplace and consumer harms. Given the many shortcomings in this proposal, I urge withdrawal. USDA should not propose changes in the operations of poultry slaughter/processing plants without adequate data review and research to fill critical data gaps that support proposed changes. The available data, briefly reviewed in this comment, does not support the changes proposed in this Proposed Rule. In addition, USDA should undertake a thorough and competent analysis of the economic burden on workers and consumers and not just industry and government inspection resources . I urge USDA to commit to regulatory reform that enhances worker and food safety:


  • USDA should enhance processing plant inspection and improve workplace conditions. Conditions in US poultry processing are such that the USDA, in concert with its sister agencies, should be taking steps in the opposite direction from these proposals. Rates of injury and infection among meat and poultry processing are the highest in any US workforce, and they are not decreasing, according to data provided by industry to OSHA.




  • USDA should maintain and increase targeted monitoring of major food borne pathogens, such as Campylobacter and Salmonella, and additionally add emerging good borne pathogens quickly in order to prevent disease in workers and consumers. USDA must react to recent information on emergence of new pathogens in the food supply in order to prevent disease; this system should be responsive to new surveillance data on the food supply as well as clinical/epidemiological studies of exposures in humans, both works and consumers. USDA should sponsor research and quickly update its methods to enhance rapid and real time detection of pathogens throughout the processing cycle.




  • USDA should work with FDA in accomplishing the policy goal of restricting use of antimicrobial drugs in food animal feeds. The prevalence of highly pathogenic bacteria, also largely drug resistant, in the food supply is very high as demonstrated in recent studies by FDA, USDA, and academic research groups such as ours. .Strong temporal associations between resistance phenotypes in E coli isolates from food animals and humans have been reported by FDA researchers (Tadesse et al 2012) While primary authority for this issue lies with FDA, USDA can support this initiative by funding research on production methods that do not incorporate these agents into feeds. USDA can also assist FDA in monitoring drug use in the food production industry.




  • USDA should take immediate steps to revise guidance related to HACCP in poultry processing plants. The present implementation does not cover the whole slaughter/processing system and provides no information relevant to reducing exposures of workers and consumers to pathogens. Analyses based on current HACCP data are misleading in terms of worker and food safety risks. HACCP-based systems must be expanded to assess pathogen contamination during the stages of cut up, deboning, and further processing to provide full information on worker and consumer health risks.




  • USDA should address inadequacies of existing programs related to food safety. USDA needs to review the actual efficacy of its current requirements for tracking information on packaging. In our recent study of meat and poultry products in Baltimore food outlets, none of the packages we purchased contained such information. This failure probably contributes to the finding by CDC that nearly 70% of food borne disease outbreaks are never fully identified as to pathogen or source.




  • Funding of increased worker and food safety: In order to fund a more vigorous and reliable system of food and worker safety, we suggest adoption of the system put in place by US FDA for reviewing new drug applications: USDA could collect license fees from all slaughter/processing plants, pro-rated to production levels, to fund an adequate and transparent system of outside inspection and monitoring.


References cited
Angulo, F. J., V. N. Around, et al. (2004). Evidence of an association between use of

anti-microbial agents in food animals and anti-microbial resistance among bacteria

isolated from humans and the human health consequences of such resistance. J Vet

Med B Infect Dis Vet Public Health 51(8-9): 374-9.


Bering ME et al . Prevalence, serotype, and antimicrobial resistance of Salmonella on broiler carcasses post pick and post chill in 20 US processing plants. J Food Prot 72, 1610-1615.
Bucher O et al. A systematic review-meta-analysis of chilling interventions and a meta-regression of various processing interventions for Salmonella contamination of chicken. Prep Veteran Med 103: 1, 2012.
Bureau of Labor Statistics. Injuries, Illnesses, and Fatalities, 2010 data release. http://www.bls.gov/iif/oshwc/osh/os/ostb2813.pdf

Cartwright M et al. The prevalence of carpal tunnel syndrome in Latino poultry processing workers and other Latino manual workers. JOEM 54: 198, 2012.


Frost P et al. Occurrence of carpal tunnel syndrome among slaughterhouse workers. Scand J Work Environ Health 24: 285, 1998.
Glenn LM, Englen MD, et al. Analysis of antimicrobial resistance genes detected in

multiple-drug-resistant E coli isolates from boiler chicken carcasses. Microb Drug

Resist, epub doi:10.1089/mdr.2011.0224, 2012.
Gould LH and Limbago B. Clostridium diifficile in food and domestic animals: a new

food borne pathogen? Clin Infect Dis 51: 577, 2010.


Guo C et al. Application of Bayesian techniques to model the burden of human salmonellosis to US food commodities at the point of processing. Foodborne Pathogen Dis 8: 5092011

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Hanson, B. M., A. E. Dressler, et al. (2011). "Prevalence of Staphylococcus aureus and



methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa." J Infect

Public Health 4(4): 169-74.


Hue O et al. Prevalence of and risk factors for Campylobacter spp. contamination of broiler chicken carcasses at the slaughterhouse. Food Microbiol 27: 992, 2010.
Lipscomb, H J. Musculoskeletal symptoms among poultry processing workers and a community comparison group: Black women in low-wage jobs in the rural South". Amir J Induct Med 50 (5), 327, 2007.
Messing, K. Factors associated with dysmenorrhea among workers in French poultry slaughterhouses and canneries. JOEM 35 (5), 493, 1993.
Nauta M et al. A poultry processing model for quantitative microbiological risk assessment. Risk Anal 25 85, 2005.
Northcutt JK and Russell SM. General guidelines for implementation of HACCP in a poultry processing plant. University of Georgia College of Agriculture Department of Poultry Science http://www.caes.uga.edu/applications/publications/files/pdf/B%201155_4.PDF
Ortiz DJ and Jacobs DE. A safety and health assessment of two chicken processing

plants, Atlanta: Georgia Institute of Technology, 1990.



http://www.oshainfo.gatech.edu/nbc-rpt.pdf
Scallan E, et al. Food borne illness acquired in the United States – unspecified agents Emerg Inf Dis 17: 16, 2011.
Scharff RL. Economic burden from health losses due to food borne illness in the United States. J Food Prot 75: 123, 2012.
Silbergeld, E. K., J. Graham, et al. (2008). Industrial food animal production,

antimicrobial resistance, and human health. Annu Rev Public Health 29: 151-69.


Staider T et al. Integron involvement in environmental spread of antibiotic resistance.

Front Microbiol 3: 119, 2012.


Tadesse DA et al. Antimicrobial drug resistance in E coli from humans and food animals, United States, 1950-2002, Emerg Inf Dis 18: 71, 2012.
Waters, A. E., T. Contente-Cuomo, et al. (2011). Multidrug-Resistant Staphylococcus

aureus in US Meat and Poultry. Clin Infect Dis 52(10): 1227-30.


Zhao, S., K. Blickenstaff, et al. (2012). A Comparison of the Prevalence and

Antimicrobial Resistance of Escherichia coli from Different Retail Meats in the United

States: 2002-2008. Appl Environ Microbiol.78: 1701-1707
Zhao, S., P. F. McDermott, et al. (2006). Antimicrobial resistance and genetic

relatedness among Salmonella from retail foods of animal origin: NARMS retail meat

surveillance. Foodborne Pathog Dis 3(1): 106-17.

Appendix: Silbergeld resume.



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