After the recent E. coli O157:H7 outbreak linked to Bravo raw milk gouda cheese that sickened 38 (one with HUS), the New York Times is quickly becoming the go to newspaper for cheese lovers.
Bill Neuman wrote yet another article on cheese – “Raw Milk Cheesemakers Fret Over Possible New Rules” – after Food Safety News reported it and in follow-up to my five part series on raw milk and the “60 day rule” – Part 1, Part 2, Part 3, Part 4 and Part 5, and the continuing outbreaks, illnesses and recalls linked to raw (unpasteurized) and pasteurized dairy products in the United States.  He did note in his article from the FDA Inspection Report – Observation 2  that Bravo packaged cheese for shipment BEFORE the 60 days had run.
Mr. Neuman last year also penned – “As Cheesemaking Blooms, So Can Listeria” and “Small Cheesemaker Defies F.D.A. Over Recall” – following a Listeria recall linked to Estrella Family Creamery (See Inspection) and an E. coli O157:H7 outbreak linked to Sally Jackson Cheese (See Inspection) – both producers from the state of Washington. Here is my full series on the 60 Day Rule:
The Raw Milk Beat Goes On: A Look at the Literature and the 60-Day Raw Milk Cheese Aging Rule
Introduction
Some say raw milk cheeses are being beat-up by US regulators this year. Indeed, if there was a Food Safety Zodiac, 2010 would be the Year of the Cheese (shell eggs a close second). Whatever the underlying explanation, the number of cheese-related illnesses and recalls in 2010 appears unprecedented. While covering these events, my blog has been inundated with comments expressing outrage at FDA and state regulators for raw milk cheese “crackdowns.” The comments range from fringe screams about food Nazis and fascists to thoughtful and informative discussions about the microbiology of raw milk cheeses and implications for food safety and quality.
Tami Parr of the Pacific Northwest Cheese Association portended regulatory changes that may affect the fate of raw milk cheeses on her blog earlier last month. Interestingly, she links to a 1997 memo that recommended FDA re-examine its 60-day aging process for hard cheeses made from raw milk. No changes were made to the rule at that time, but clearly the issue of aged raw milk cheeses and food safety is not new, as shown in the timeline below.
To look at the issue closer, this paper provides an overview of the historical context and timeline of raw milk cheese regulations in the US, and examines the state-of-the-science surrounding the 60-day aging rule established by FDA.  I have broken it into 5 parts for ease of reading.  At the end of part 5, I will provide the entire paper in PDF.I welcome comments, suggestions, and additional literature from readers to add to the analysis.
Historical Perspective
Timeline of Key Studies and Regulatory Changes for Cheeses Made from Raw Milk
1941-1944: Typhoid fever epidemics are linked to cheddar cheese made from raw milk in Canada; outbreak-related Salmonella typhi strains are recovered from 30-day-old cheese, but not from 48- or 63-day-old cheese resulting in Alberta, Canada halting the sale of raw milk cheese unless ripened for at least 90 days (Marth 1969).
1946: Brucella abortus is found to survive in cheddar cheese made from raw milk for up to 6 months depending on initial inoculation level, but the authors of the study conclude that cheddar cheese is not a proven carrier of undulant fever (the human disease caused by B. abortus). D’Amico (2008a) suggests that this study, combined with the earlier data on typhoid fever illnesses not attributed to cheese cured for more than 63 days, is the likely origin of the 60-day curing period in the US. However, subsequent reports in the 1940s show extended survival of Mycobacterium tuberculosis (>100 days), Salmonella typhi (3-10 months), and hemolytic Streptococcus (>160 days) in cheddar cheese (D’Amico 2008a).
1950: FDA promulgates regulations (21 CFR Section 133) requiring that cheesemakers use pasteurized milk, or cure the cheese for no less than 60 days at a temperature greater than 35°F. According to D’Amico (2008a), there are over 30 natural cheeses that can be made legally from raw milk in the US under this rule.
1960s: Additional challenge studies show survival of pathogens including Salmonella enterica subtype Typhimurium beyond the 60 day curing period; Salmonella typhi is found to survive in stirred curd granular cheddar cheese for 150-180 days when held at refrigeration temperatures (D’Amico 2008a).
1987: Numerous foodborne illnesses are linked to commercial fluid raw milk including 22 deaths from Salmonella Dublin infections from 1971-1975 (Werner 1979). This prompts a Citizen’s Petition and federal judge’s ruling that orders the FDA to ban fluid raw milk and milk products from interstate commerce (21 CFR Section 1240.61). The regulations allowing cheesemakers to sell cheese made with raw milk if cured for 60 days at a temperature greater than 35°F remain in place (21 CFR Section 133).
1973-1992: CDC reviews reported outbreaks and illnesses from raw milk (Headrick 1998) and cheeses made from raw milk (Altekreuse 1998). During this time, there were 32 reported cheese-associated outbreaks and 58 deaths, but the authors conclude that “If current Food and Drug Administration sanitary requirements for cheesemaking had been met, these outbreaks would have been preventable.” They go on to say: “Curing cheeses kills most bacteria present in cheeses; however, evidence from sources other than the CDC Foodborne Disease Outbreak Surveillance System suggests that curing alone may not be a sufficient pathogen control step to eliminate Salmonella, Listeria, and E. coli O157:H7 from cheese.”
1996: Researchers at South Dakota State University publish a study showing that 60-day aging is largely ineffectual in reducing levels of E. coli O157:H7 in cheddar cheese. FDA then asks the National Advisory Committee for Microbiological Criteria for Food (NACMCF) to re-examine the literature on the efficacy of 60-day aging. In a memo to FDA, the committee states: “the sixty-day aging process for hard cheese is questionable as an effective measure in support of the public’s health.”
2002: Health officials from Alberta, Canada report an outbreak of E. coli O157:H7 hemorrhagic colitis associated with Gouda cheese made from raw milk (Honish 2005). In their paper, the authors suggest that Canada re-evaluate the federal regulations for aging of hard cheeses made from raw milk.
2004: In an interview with Food Safety Magazine, FDA officials state that they are developing a “risk profile for raw milk cheeses, which will aid in the Agency’s assessment of the requirements for processing these cheeses,” based, in part, on the report by the NACMCF and other recent research suggesting that 60-day aging may be insufficient to protect the public’s health (Sheehan 2004).
2006: Schlesser and colleagues report results from a study of E. coli O157:H7 survival in cheddar cheese made from raw milk, and confirm previous reports questioning the efficacy of 60-day aging to eliminate E. coli O157:H7 during cheese ripening.
2008: D’Amico and colleages determine that the 60-day aging requirement does not ensure safety of surface-mold-ripened soft cheeses manufactured from raw or pasteurized milk when Listeria monocytogenes is introduced as a postprocessing contaminant. The authors conclude that “the safety of cheeses of this type must be achieved through control strategies other than aging, and thus revision of current federal regulations is warranted.”
2010: According to press quotes, FDA officials are conducting a nationwide survey of cheese safety with a focus on Listeria monocytogenes contamination. Notably, this survey encompasses both raw and pasteurized cheese products from large and small cheesemakers.
In November, the CDC reports 38 illnesses from Gouda cheese made from raw milk and aged for 60 days in accordance with regulations (CDC, 2010).
A study in the December 1, 2010 issue of the Journal of Food Protection documents survival of E. coli O157:H7 in aged Gouda and stirred-curd cheddar cheese (D’Amico 2010). The authors conclude that “the 60-day aging requirement is based on decades-old research indicating that Brucella abortus is eliminated in cheddar cheese alone is insufficient to completely eliminate levels of viable E. coli O157:H7 in Gouda or stirred-curd cheddar cheese manufactured from raw milk contaminated with low levels of this pathogen.”
Definitions
Before embarking on a discussion of the 60-day curing criteria for cheeses made from raw milk, it is important to understand the definition of cheese styles and differences in regulation.  Cheese was originally developed by human societies as a method to preserve milk.  In the US, cheeses are usually made from cow’s, goat’s, sheep’s, or buffalo’s milk.  Among 72 different cheese and cheese product types defined in 21 C.F.R. Part 133, the FDA allows only a limited number of cheese types to be made with raw milk so long as the cheese is cured at a temperature of not less than 35°F for not less than 60 days. The Raw Milk Cheesemakers’ Association adds an additional criteria for low-temperature (thermised) heat treatment of raw milk cheese:  ”Cheese produced from milk that, prior to setting the curd, has not been heated above the temperature of the milk (104°F, 40°C) at the time of milking and that the cheese produced from that milk shall be aged for 60 days or longer at a temperature of not less than 35°F (2°C) in accordance with US FDA regulations.”  Table 1 summarizes cheeses and cheese types subject to the 60-day aging rule.
Cheese and Cheese Products in the US (adapted from The American Cheese Society) Application of the 60-Day Aging Rule
Fresh cheeses: 60-day aging rule not allowed. Italian style mascarpone and ricotta, chevre, feta, cream cheese, quark and cottage cheese, queso freso and other Mexican-style fresh cheeses.
Soft-ripened cheeses: 60-day rule allowed. Brie and camembert styles, triple crèmes.
Semi-soft cheeses: 60-day aging rule allowed. Blue cheeses, colby, fontina styles, havarti and Monterey Jack, washed rind cheeses. Firm/hard cheeses: 60-day aging rule allowed. Gouda styles, most cheddars, dry jack, Swiss (Emmenthaler) styles, Gruyere styles, many “tomme” styles and Parmesan styles.
Blue cheeses: 60-day aging rule allowed. French (roquefort), Italian (gorgonzola) and Danish blue styles. 
Pasta Filata cheeses: 60-day aging rule not allowed. Italian style Mozzarella, Provolone, and Scamorza.
Natural or washed rind cheeses: 60-day aging rule allowed. French Tomme de Savoie and Mimolette, as well as the English Stilton (also a blue), and Lancashire cheeses (natural); Epoisses, Livarot and Taleggio (washed).  Processed cheeses: 60-day aging rule not applicable. American Cheese, processed cheese spreads, and “cheese flavored” spreads. Regulation of Raw Milk Cheeses in Other Countries
Canada regulates cheeses made from raw milk similar to the US, except for Quebec where raw milk cheeses can be manufactured without 60-day aging if strict rules for milk quality and veterinary inspections of cattle herds are followed.  In 1996, following an outbreak of E. coli O157:H7 linked to cured Gouda cheese, Health Canada proposed a ban on all raw milk cheeses, but the initiative was defeated by industry and consumer groups (Honish 2005).
The European Union has no aging rule, but their requirements for hygiene during milking, storing, and collection of milk for cheesemaking are likely much stricter than in the US.  Additionally, requirements for both animal health and worker/personnel health help ensure safe raw milk cheese production.  Cheeses made from raw milk in Europe must be labeled “Made with Raw Milk.”
The regulation of raw milk cheeses in Australia and New Zealand has been an area of intense controversy in recent years.  Australia bans all domestic raw milk cheeses, but allows importation of certain cheeses–Roquefort, Gruyere, Sbrinz, Emmental–from Europe and Switzerland provided they are aged 90 days and meeting European safety standards (Standard 4.2.4A).  Domestic cheeses must be “thermised” by using a low temperature heat treatment followed by aging for 90-days.
Epidemiology
The epidemiology of cheese-related outbreaks has changed in the US since the 60-day aging rule was established in 1950.  The studies conducted in the 1940s that presumably  provided the basis for the rule were based on diseases such as Typhoid fever, an infection transmitted by human carriers.  Today, most of the cheese-linked illnesses are due to zoonotic enteric pathogens carried by ruminants including Campylobacter, E. coli O157:H7, Listeria monocytogenes, and Salmonella.  L. monocytogenes is also a ubiquitous inhabitant of the dairy environment.
Dairy-related Outbreaks Attributed to Raw Milk Cheese  
Internationally, dairy-related outbreaks are relatively uncommon in developed countries, but an estimated 11.8 percent are attributed to cheeses made from raw milk (FSANZ 2006).  Foodborne disease outbreaks have been reported in all countries that allow raw milk cheese including France where raw milk cheeses are popular (Desenclos 1996; Desenclos 1996; DeValk 2000; Dominguez 2009; Haeghebaert 2003; Ostyn 2010).  The most recent published review in the US examined reported cheese-related outbreaks and illnesses from 1973 – 1992 (Altekruse 1998).  Fresh Mexican-style cheeses (for example, queso fresco) were the most frequently implicated vehicle and caused 56 of the 58 deaths described in the review; the other 2 deaths were linked to improper pasteurization of Mozzarella cheese. 
Bacterial Pathogens That Can Survive in Cheeses Aged for 60 Days
Brucella spa.: incubation 1-2 months or longer; duration, may relapse for years; signs and symptoms, fever, headache, joint pain, depression, weight loss. Can cause abortions in dairy animals.
Campylobacter: incubation, 2-5 days; duration, 2-7 days, some patients develop paralytic syndrome as a long-term complication; symptoms, diarrhea (sometimes bloody), cramps, fever, nausea, vomiting, muscle aches. Found in healthy dairy animals.
E. coli O157 and other pathogenic E. coli: incubation, 2-8 days; duration, 5-8 days, some patients develop kidney disease or other long-term complications; symptoms, diarrhea (often bloody), cramps, sometimes low-grade fever. Found in healthy dairy animals.
Listeria monocytogenes: incubation, 3-70 days (average 3 weeks); duration, variable depending on susceptibility, death rate in patients with meningitis as high as 80 percent, septicemia as high as 50 percent; symptoms, septicemia, meningitis, intra-uterine infections in pregnant women with spontaneous abortions and stillbirths. Found in healthy dairy animals and the dairy processing environment
Mycobacterium bovis: incubation, 4-12 weeks to positive tuberculin test, 1-2 years for systemic infection; duration, years, may persist lifetime as latent infection; symptoms, pulmonary and extra-pulmonary disease. Systemic illness in cattle, transmitted through milk and aerosols.
Salmonella enteric: incubation, 6 – 48 hours; duration, 2-8 days, some patients develop long-term complications including arthritic disease;  symptoms, diarrhea, nausea, vomiting, cramps fever. Some strains cause illness in dairy animals.
Salmonella typhi: incubation, 8-14 days; duration, variable, case fatality of 10-20 percent without antibiotic treatment; symptoms, fever, cramps, diarrhea, anorexia. Human carriers.
Staphylococcus enterotoxin: incubation, 2-4 hours; duration,1-3 days; symptoms , vomiting, nausea, cramping. Animal and human carriers; toxin produced following growth in a food.
The problem with fresh, soft cheeses is ongoing and most often associated with use of inadequately pasteurized milk and cross-contamination in the processing environment (CDC 2000; CDC 2001; CDC 2008; CDC 2009; Cody 1999; MacDonald 2005; Villar 1999).  Listeria monocytogenes and Salmonella are pathogens most often found in fresh Mexican-style soft cheeses as reviewed previously (Marler, 2009).  Over the last decade, there have been only two deaths from cheese made with raw milk; both occurred in 2003, and were due to consumption of contaminated fresh (un-aged) queso fresco Mexican-style cheese (CDC OutbreakNet).
In contrast, outbreaks and illnesses linked to 60-day aged cheese are relatively rare despite microbiological evidence of pathogen survival in these cheeses (Altekruse 1998; D’Amico 2008b; D’Amico 2010; Donnelly 1990; Jaros 2008; Reitsma 12996; Schlesser 2006).  Researchers from the University of Vermont have speculated that the relative paucity of outbreaks and illnesses associated with 60-day aged cheese may be due to 1) a low contamination level in milk used for cheesemaking or 2) alterations in virulence of pathogens within the cheese matrix (D’Amico 2010).
However, there are notable exceptions including E. coli O157:H7 outbreaks linked to cured Gouda cheese in Canada in 2002 (Honish 2005) and the US in 2010 (CDC 2010).  In the latter, at least 38 cases have been linked to consumption of Gouda cheese made with raw milk and presumably aged for 60 days in accordance with FDA regulations.  The CDC summarized findings from the ongoing investigation in a November 24, 2010 report.
Microbiology
Johnson (2001) reviewed the microbiology of cheese products and noted the complexity of the subject because of the great diversity in cheese manufacturing and ripening protocols, as well as composition of the different cheese types.  The 60-day aging rule is based on the theory that pathogens, if present, will die off to levels below the infectious dose during the aging process. However, the effectiveness of this system depends on the initial microbiological quality of the milk and other ingredients used, and the hygienic practices used during cheese processing (Donnelly 1990). No amount of curing or aging or even pasteurization will compensate for poor quality milk or lack of hygiene during manufacturing and storage. The intrinsic properties of the cheesemaking process that affect pathogen survival and growth include:
• pH• moisture• salt content• acidity• temperature• humidity• redox potential• cheese microbial flora including starter culture (microbial community)
Individually and in combination, these factors can have significant impacts on whether a foodborne pathogen survives or grows in cheese during curing. The effectiveness of these natural processes is ultimately dependent on the initial contamination level of the cheese. A high inoculum of a pathogen, especially one with a low infectious dose, will overwhelm these control systems. The soft and semi-soft surface-mold-ripened cheeses are at the greatest risk of contamination due to their higher pH and moisture content (D’Amico 2008a).
The presence of pathogens in milk used for production of raw milk cheeses represents a risk for consumers.  Oliver (2009) reviewed the literature on pathogen prevalence in US bulk tank milk and found these levels.
• Campylobacter: 2 – 9.2 percent • E. coli O157:H7: 0 – 0.75 percent • Listeria monocytogenes: 2.8 – 7.0 percent • Salmonella spp: 0 – 11 percent • Shiga-toxin E. coli: 2.4 – 3.96 percent • Yersinia enterocolitica: 1.2 – 6.1 percent
D’Amico (2008b and 2010) surveyed milk used to produce small-scale farmstead cheese in Vermont and found an overall low level of contamination, but documented variations from farm-to-farm indicating that some operations practice strict hygienic controls while other need improvement in their food safety practices.
Experimental studies of the behavior of pathogens in aged cheese show mixed results (Bachmann 1995; Back 1993; D’Amico 2008a; D’Amico 2008b; D’Amico 2010; Govaris 2002; Marth 1969; Reitsma 1996; Schlesser 2006).  The studies are difficult to compare because of different experimental methods, and variations in how the cheese was manufactured for the experiments.  For example, Reitsma (1996) found viable E. coli O157:H7 in cheddar cheese at 158 days, but used pasteurized milk in their comparisons.  Schlesser (2006) inoculated cheddar cheese with a 5-strain E. coli O157:H7 cocktail and demonstrated an inadequate reduction at 60 days (1 log) and 120 days (2 logs); in contrast, heat treating the milk resulted in a 5-log reduction.  D’Amico (2010) examined the behavior of E. coli O157:H7 in aged Gouda and stirred-cured cheddar cheeses manufactured from raw milk and was able to recover viable cells for more than 270 days in both cheese types using selective enrichment.
Listeria monocytogenes can be a pervasive problem in the dairy processing environment.  There is evidence that L. monocytogenes can survive aging in both pasteurized and surface-mold-ripened cheeses if the pathogen is introduced post-processing (D’Amico 2008b). These findings underscore the importance of hygienic practices at cheesemaking facilities regardless of pasteurization status. D’Amico (2008a) provides a more comprehensive review of experimental studies using different pathogens and cheese types.
Producing Cheese Safely
Unlike fluid raw milk producers who have been the subject of intense conflict with regulators for many years, artisanal and specialty cheesemakers that use raw milk have maintained a relatively good relationship with state and FDA regulators in the US. According to their website, the American Cheese Society (ACS) shares resources to help producers adequately prepare for audits and inspections and work collaboratively with state regulators and the FDA.  The recent increase in FDA inspections and Listeria testing of soft cheeses and cheesemaking facilities has no doubt caused tensions between cheesemakers and regulators. The New York Times reports that FDA inspectors visited 102 facilities beginning in April 2010, including both large and small cheesemakers. They found Listeria in the facilities of 24 cheesemakers and more than half were small, artisan-scale operations.
While these findings are a cause for concern and have resulted in at least one major recall, fortunately, cheesemaking associations such as the ACS have an infrastructure to address food safety. For example, the ACS advises their members to:
• take part in ongoing food safety education• follow a HACCP plan• regularly conduct their own product and environment testing• maintain accurate and up-to-date records• seek third party certification• build relationships with local regulators
Conclusions
Artisanal raw milk cheeses are distributed around the world and revered by fans for their unique sensory characteristics, as well as the art and tradition of making these cheeses.   Cheeses, especially fresh and soft or semi-soft styles, are susceptible to contamination with pathogens such as Campylobacter, E. coli O157:H7, Listeria monocytogenes, and Salmonella.  Countries where raw milk cheeses are popular take different approaches in their regulations.  Experimental and epidemiological evidence suggests that the 60-day aging rule used in the US and Canada is not a fail-safe approach to cheese safety, which has prompted the FDA to re-evaluate the efficacy of the rule and conduct a national survey of cheesemaking facilities. 
There are at least four potential outcomes that may result from FDA’s recent actions:  1) a ban on all cheeses made from raw milk, 2) an extension of the 60-day aging period to 90-days or longer depending on evidence from the literature, 3) adoption of a European-type approach with intense regulation of animal health and hygiene during processing, but no aging rule, or 4) no change in the 60-day aging rule in the US.  While the future of the 60-day aging rule for cheeses made from raw milk in the US remains to be determined, the openness of cheesemakers to working with state and federal regulatory agencies will hopefully foster a science-based approach to cheese safety that both protects the public’s health and preserves the unique characteristics and tradition of artisanal cheeses.
APPENDIX
Outbreaks, illnesses and recalls linked to cheeses made from raw (unpasteurized) and pasteurized milk, United States, 2010 (through November 2010): February 2010, Washington, Listeria monocytogenes, 5 ill, queso fresco cheese, pasteurized milk used to make the cheese, FDA February 2010, Washington, Listeria monocytogenes, 0 ill, various raw milk cheeses. 60-day aged raw milk cheeses from Montesano plant, FDA March 2010, Washington, Listeria monocytogenes, 0 ill, Tomme raw milk cheese. Expanded recall of 60-day aged raw milk cheeses from Montesano plant, FDA April 2010, Washington, Listeria monocytogenes, queso fresco cheese. Pasteurized milk used to make the cheese; recall with no illnesses reported, FDA May 2010, Nevada, Campylobacter, 1 ill, illegal Mexican-style cheese. Type of milk used to make the cheese unknown, Washoe County
May 2010, Minnesota, Shiga toxin-producing E. coli, 0 ill, raw milk cheese. Non-O157 found in dairy’s cheese during raw milk outbreak investigation, MDA/MDH June 2010, Delaware, Brucella and Listeria monocytogenes, 2 ill, raw dairy products including cheese. Two separate incidents, DE DHHS July 2010, Pennsylvania, Staphylococcus aureus, raw milk hard cheddar cheese, 60-day aged cheese, recall with no illnesses reported, PDA July 2010, New York, Listeria monocytogenes, queso fresco cheese, pasteurized milk used to make the cheese, recall with no illnesses reported, NY AGMKT August 2010, Rhode Island, Listeria monocytogenes, queso fresco cheese, pasteurized milk used to make the cheese, recall with no illnesses reported, RI DOH Aguust 2010, Misssouri, multiple Listeria monocytogenes and Staphylococcus aureus, raw milk cheese, 60-day aged raw milk cheese from plant in Missouri, recall with no illnesses reported, MO AG
September 2010, Washington, Listeria monocytogenes, 0 ill, raw milk cheeses, expanded recall of 60-day aged raw milk cheeses from Montesano plant, FDA
October 2010; Washington, Listeria monocytogenes; 0 ill; raw milk cheeses expanded recall of 60-day aged raw milk cheeses from Montesano plant, US AG
November 2010, AZ, CA, CO, NM, NV; E. coli O157:H7 and Listeria monocytogenes, 38 ill, raw Gouda cheese, other cheeses, 60-day aged Gouda, E. coli outbreak linked to Costco “Cheese Road Show;” recall expanded to all company cheeses on 11/17/10,  no Listeria illnesses reported, CDC November 2010, Colorado; E. coli O157:H7, gorgonzola cheese, cheese imported from Italy, made from pasteurized milk, no illnesses reported, FDA
November 2010, Washingotn, Listeria monocytogenes, fresh (queso and ricotta) Mexican-style cheeses, made from pasteurized milk, no illnesses reported (previous recall from same plant in April 2010),  FDA
Here is the full article by PDF – “The Raw Milk Beat Goes On: A Look at the Literature and the 60-Day Raw Milk Cheese Aging Rule”
References
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