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According to the USDA cooking chicken at 145ºF (63ºC) for 13 minutes (i.e. maintaining an internal temperature of 145ºF for that long) will bring about a "7 log10 relative reduction of salmonella".

A recent question made me wonder whether this can be considered safe for sous-vide applications where it takes 4+ hours to reach 140ºF since the FDA recommendation (which only applies to commercial kitchens) is that once food enters the 41-135ºF zone (5-57ºC), it should be "cooked and served" within 4 hours. The USDA rules for home cooks are much stricter recommending that food should not remain in the 40-140ºF (4-60ºC) zone for more than two hours.

I always imagined that food left in this, so called, danger-zone for too long has given bacteria time to multiply and produce enough toxins in the food for it to become dangerous.

Another idea occurred to me, that after four hours the bacteria count has risen enough that a significant number of bacteria will be present even after a 7 log10 reduction.

Frankly my first guess still seems most likely to me, but really I just don't know. If my second idea is correct, then it would presumably still be safe to eat meat left in the danger zone for 4+ hours, as long as it holds an internal temperature of 140ºF+ for some time longer than the USDA time-temperature tables otherwise suggest.

Can anyone say which, if any, of my guesses is correct? I think this is equivalent to asking whether there exists a type of bacteria that can produce a dangerous amount of toxins in food within four hours at temperatures between 40ºF and 140ºF.

Update: In earlier revisions of this question, I attributed the 4 hour rule to the USDA which caused an amount of confusion. As the text now states, the 4 hour rule is set by the FDA in their Retail Model Food Code and pertains only to cooking in commercial establishments. While I did find that the USDA guidance for school food authorities also has a 4 hour recommendation, this is no doubt because school kitchens can be placed on an equal footing with commercial kitchens.

There has also been some discussion regarding whether the USDA's 2 hour rule encompasses cooking time, or pertains only to time spent in the danger-zone during storage or preparation prior to cooking. For anyone interested in the details, please read the comments on this question and those on @Athanasius' answer.

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The USDA paper you link to shows INTERNAL TEMP and HOLD TIME AT TEMP not cooking temp and cooking time. From the paper: "The stated temperature is the minimum that must be achieved and maintained in all parts of each piece of meat for a least the stated time." Maybe I'm being pedantic in your case, but it's a critically important difference for anyone who might not realize. –  mghicks Dec 1 '12 at 15:41
    
Yep, I'll update to clarify. –  Chris Steinbach Dec 1 '12 at 21:06
    
I won't put this as an answer because I am not willing to do a bunch of research to get supporting links, but NO. By holding the temperature specifically in the hazardous zone, you are intentionally creating a breeding ground for pathogens. This is what incubators are for in labs! Cooking is not sterilization, even if the food was previously cooked to a higher temperature, and home conditions are not clean rooms. –  SAJ14SAJ Dec 1 '12 at 21:22
    
The recommendation is 2 hours, not 4 hours. What I don't understand is why you assume that it will take 4 hours for food to reach 140° F, given that sous-vide is all about efficiency and precise temperature control. Sous-vide equipment will hold the temperature at 140° F for long enough to kill as many bacteria as the USDA recommendation of 10 seconds at 165° F. I'd be very surprised if it takes more than 1 hour to reach the programmed temperature. –  Aaronut Dec 2 '12 at 14:26
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Perhaps I'm not reading this right, but it seems that the "2 hour rule" has nothing to do with cooking. It is the maximum recommended time for food to be left out at room temperature before cooking (e.g., the time food sits in your cart at the grocery store and in your car before going back in the refrigerator) or after cooking (before refrigerating leftovers). I believe this "2-hour rule" may also be referenced in the school children document regarding transport times (p. 10). Is there a document that clearly references 2 hours in regard to cooking time? –  Athanasius Jan 9 '13 at 20:36

3 Answers 3

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This article may be a good starting place for some advice. They consider a lot of the common microbes, not just Salmonella. Assuming you get somewhere close to the 140F range for an extended period of time, you'll kill off most things. Other things might only survive in spore form, so you might be okay eating the food while it's hot.

But care should be taken if you wanted to cool the food and heat at a later time, since a lot of spores means that they could become active again and multiply significantly if left in the so-called "danger zone" for very long. Also, note that during the initial cooking, lots of bacteria will be competing, and the really bad stuff may not have a chance to grow much. But after most are killed at higher temperatures, any cooling phase of the food will allow remaining spores to reactivate in an environment where they don't have to compete as much and thus often grow faster. In many cases, it can sometimes be more dangerous to let cooked food sit at room temperature than to take a long initial time to cook.

Anyhow, the spores are not your concern for a long initial cooking time if you're planning to eat the food right away. In that case, you need to worry about things that will generate persistent toxins. The linked article mentions a couple: C. perfringens and S. aureus.

As the article points out, Clostridium perfringens will be killed in slow cooking by the time you reach 140F. However, they don't seem to explicitly mention the enterotoxin produced by C. perfringens. That toxin can be inactivated by further heating up to 165F, but that may not be desirable for all foods. (That may be the reason why they don't mention the toxin -- they are assuming the turkey and stuffing will be at a minimum of 165F by the end of the roast.) In any case, the article implies that you'd need to cook for roughly 10 hours to produce enough to be dangerous for "normal" C. perfringens. (For the special quick-growing type mentioned in their source, it would grow twice as fast.)

Staphylococcus aureus, on the other hand, clearly would take a long time to grow. They estimate even in ideal conditions, it would take about 15 hours to produce enough toxin to worry about. Also, in raw food, they state that S. aureus typically does not grow much, since it doesn't do well competing against other spoilage microbes (e.g., Salmonella) that grow better but won't produce the same levels of persistent toxins.

For some reason, Bacillus cereus doesn't get a mention in this article (it's more common on grains but small amounts are usually found in meats too), and I think it's a potential concern with some foods. My guess is that again B. cereus usually doesn't compete well against things like Salmonella and Campylobacter. Looking up typical growth rates, it may not be an issue unless you had a high concentration to begin with.

As with other microbes (e.g., C. perfringens, C. botulinum) the more typical cause of food poisoning with B. cereus is the spores that survive after cooking. When food is held for a long time in the "danger zone" (e.g., in buffets below 140F, at room temperature before refrigeration), these bacteria have a chance to revive from their spore form and produce persistent toxins. The particular problem with B. cereus is that normal heating below boiling will not destroy that toxin, making even normal reheated foods a potential danger.

I only mention the spore issue because a higher population of these bacteria (grown during longer cooking) will produce more spores, which can potentially make cooling food down and reheating more dangerous. These bacteria typically don't grow fast when in the presence of things like Salmonella, but in the more sterile growth medium post-cooking, they can really get going. If you slow-cook for a long time, be really sure to handle leftovers properly.

But getting back to the main issue: what if you just plan to eat the food right after slow-cooking? In that case, I think the original article I linked above implies that you're almost certainly safe even if you take up to 10 hours or so with the food between 50F and 130F. Since most of the bacteria that produce persistent toxins don't grow well when competing against things like Salmonella, you're probably safe for even longer. As they point out at the end of the article, food kept even as high as 55-60F will generally "spoil safe," partly due to competition among spoiling agents. However, as you get into the range around 100F in cooking, you hit ideal growth temperatures for some of the more nasty stuff.

Personally, after I researched this stuff a while back, I'm willing to extend the limit to about 10 hours between 50F and 130F for my own cooking, as long as the food is ultimately held above 130F for a significant amount of time. So, slow-roasting a chicken or turkey at 250F should be fine, and even 200F may be okay. With such a slow heating process, though, I'd generally want the final temperature of the food to get to about 165F at a minimum -- to further reduce bacteria count and destroy some toxins. If I intended a lower final temperature (e.g., 140F), I would tend to use a cooking method that gets the food up above 130F more quickly. (Sous vide should do the trick in most cases.)

But I'd really start to get concerned when you go much beyond 10 hours in the "danger zone." Chances are that you might even be okay taking 12-24 hours to get up to temperature in many foods, but it could be very risky for some foods/ingredients. And then, the food must hit a higher temperature standard (at least 165F), which will destroy some potential toxins. Go much more than a day in your cooking in the "danger zone," and you could even be growing significant amounts of botulism toxin, so your safe temp would have to go even higher to destroy that toxin. Also, by that point, you may be growing all sorts of nasty stuff.

Whatever you do, don't follow the advice of self-proclaimed experts like the authors of Modernist Cuisine, who want to throw out all of the USDA regulations and rebuild a theory of food safety from scratch, apparently based on the authors' reading of only a couple papers on Salmonella death curves. Salmonella death curves may be a good guideline for normal cooking methods and sous vide, but with extended slow cooking that allows a long time below 130F, you can grow all sorts of stuff that leaves behind persistent toxins.

In sum, I think the 4 hour "danger zone" thing is a rough guideline with a built-in safety margin (for people who leave the meat in the car for 45 minutes, etc.). With proper food handling otherwise, in most cases, you should be able to push it to 8 or 10 hours with little chance of harm. But the longer you go, the more potential hazards. Do it at your own risk.

(Please note that although I have a lot of scientific training, I'm not a microbiologist, so there may be things I'm overlooking here.)

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I can't imagine anyone is going to better this answer, and if they do, well that's worth rewarding another bounty. I looked through the Modernist Cuisine reviews on amazon immediately after reading this and came across your review which is also well worth reading. –  Chris Steinbach Jan 7 '13 at 20:47
    
What about Aaronuts food-safety tag wiki, I'm confused why is this post OK? Do not get this wrong, I think this post is correct, I'm just asking why it is OK to post it, or is this a meta question? –  Stefan Jan 9 '13 at 7:39
    
If it would be appropriate, I'm more than happy to add further disclaimers. I already said "Do it at your own risk." I personally would not recommend these practices in a restaurant setting, although the paper I cited at the beginning is actually written by a major food scientist proposing recommendations for professional food service, including the possibility of a 8-10 hour roast turkey. –  Athanasius Jan 9 '13 at 15:35
    
@Stefan See the comments Athanasius posted under the question. The 2 (or 4) hour recommendation has nonsensical consequences if understood as being applicable to cooking time. I think this ought to answer Aaronut's concerns. –  Chris Steinbach Jan 9 '13 at 21:23
    
@Chris - Again, I could be reading these things wrong, but I do think the USDA somewhere has a 4-hour recommendation for most foods to get to 140F (unlike the 2-hour rule that has been referenced, which is clearly referring to storage temperatures, not cooking). On the other hand, you have things like the USDA's smoking recommendations, where you can use cooking temperatures between 225 and 300F, and "Cooking time depends on many factors... It can take anywhere from 4 to 8 hours to smoke meat or poultry." –  Athanasius Jan 9 '13 at 21:44

First of all, for most food the issue is only for the outside of the food, the inside does not have e.g. salmonella (exception is e.g. minced meats) So if you have a piece of meat that really requires 4 hours to reach 60ºC in the inside, the outside will still reach 60ºC after a few minutes, the rest of the steak (the inside) does not have any salmonella that can reproduce, so there is no problem. (remember the USDA is trying to make rules that is fool proof, not correct) Also you cannot see the danger zone as one constant range such that at 4ºC salmonella starts to reproduce and at 60ºC they stop. Salmonella reproduces at its maximum speed somewhere at 40ºC, at 50ºC the reproduction rate have been reduced to something similar to 5ºC, which is the same as a bad fridge, meat can be stored for many days in a fridge. At 51-52ºC salmonella dies faster than it reproduces. (I can get references to this from Modernist Cuisine, but it is at home, I'm writing this from memory, I might be off on a few degrees, but the principle is correct).

Update

The toxin you talk about is only dangerous when you heat and then cool the food below 60ºC, if you eat directly they are not an issue since the bacteria is already killed as I described above, see the section below from Baldwin or read the wikipedia page section.

If you’re not going to eat all your food immediately, then you need to know that some bacteria are able to make spores. Spores themselves will not make you sick, but they can become active bacteria that could. Cooking to kill active bacteria like Listeria, Salmonella, and E. coli will leave these spores unharmed. If you keep your food hot, then the spores will not become active bacteria. But when you cool your food, the spores can become active bacteria: if you cool your food too slowly or store it for too long, then these active bacteria can multiply and make you sick. To keep these spores from becoming active bacteria, you must quickly cool your food – still sealed in its pouch – in ice water that is at least half ice until it’s cold all the way through.

So to answer what I think is your question, it is safe to cook as low as 55ºC for very big pieces of meat in an oven.

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Beef is actually one of the few meats where the "surface bacteria only" rule applies; chicken and pork both need to be cooked all the way through for proper food safety. It's also not true that bacterial toxins are only left after heating and then cooling; they're left at any temperature at which bacteria are allowed to grow for a sufficient period of time. "Warm" temperature is the ideal condition, and that can either be during the cool-down or the warm-up, depending on how long either one takes. –  Aaronut Dec 4 '12 at 1:51
    
@Aaronut That you need to cook pork all through is not true any more), see cdc.gov/parasites/trichinellosis/epi.html , from 2008 to 2010 about 20 cases of trichinellosis where reported in the US per year, most due to consumption of wild meat. Also I do not think curing kills Trichinella? In Europe e.g. Param Ham is eaten daily without people getting sick of it, not sure if it is legal in the US yet? I tried to say that the toxins(spores) are not dangerous when eaten directly, and only after they have been cooled they will produce new dangerous bacteria which is dangerous. –  Stefan Dec 4 '12 at 6:22
    
@Aaronut, ran out of space. For chicken, it is still true that Salmonella does not 'live' inside chicken meat, it does live inside the intestines, the beak and the claws, but not inside the e.g. breast meat. Same as for cows, I'm sure you have E. coli or something else not so nice, inside a cows intestine. –  Stefan Dec 4 '12 at 6:29
    
Trichinella has become increasingly rare but what is your point? That's not the only bacteria living on/in meat. You've got campylobacter, listeria, C.perfringens, S.aureus, B.cereus, the list goes on and on; chicken and pork really do need to be cooked through, they cannot be eaten rare, at least not if you bought them from a supermarket as opposed to slaughtering them personally. No amount of rhetoric will change that. Additionally, while spores are not necessarily dangerous, toxins are extremely dangerous (in fact, they are the danger). –  Aaronut Dec 5 '12 at 0:16
    
What I was trying to say is that >4h cooking is OK since the surface area will not be in the 'danger' zone that long. Modernist Cuisine states that they cannot see any reason to need to cook pork any way different than beef. This is against most current advice, but this is what they say, I tend to trust that book, it feels like they back up their claims more than most other sources. I understand that you do not want to go against decades of belief, that is OK. –  Stefan Dec 5 '12 at 9:20

Yes. You can safely sous vide meat for more than four hours. However, it's pretty dependent on the temperature, size, and type of meat that you're cooking if it will work or if you'd even want to.

When cooking sous vide, you're either pasteurizing or not pasteurizing your meat. If you pasteurize the meat, then the 4 hour limit wouldn't really matter. It's pasteurized and you're ok. Douglas Baldwin covers the times for pasteurization online. You can definitely pasteurize food within your 140F / 60C range (i.e. 70mm of chicken will take 7hrs to pasteurize at 134.5F / 57C). For poultry, you need a minimum temp of 57C for pasteurization. For red meat, you need a minimum temp of 131F / 55C.

If you are not pasteurizing your food, then it's important to stay below the 4 hour time frame you've discussed. You should also be careful storing your food prior to cooking, sourcing it properly, and not serving it to immune compromised people.

Douglas Baldwin talks about this pretty extensively in the food safety portion of his primer. Here's an excerpt:

You were probably taught that there’s a “danger zone” between 40°F and 140°F (4.4°C and 60°C). These temperatures aren’t quite right: it’s well known that food pathogens can only multiply between 29.7°F (-1.3°C) and 126.1°F (52.3°C), while spoilage bacteria begin multiplying at 23°F (-5°C) (Snyder, 2006; Juneja et al., 1999; FDA, 2011). Moreover, contrary to popular belief, food pathogens and toxins cannot be seen, smelt, or tasted.

So why were you taught that food pathogens stop multiplying at 40°F (4.4°C) and grow all the way up to 140°F (60°C)? Because it takes days for food pathogens to grow to a dangerous level at 40°F (4.4°C) (FDA, 2011) and it takes many hours for food to be made safe at just above 126.1°F (52.3°C) – compared with only about 12 minutes (for meat) and 35 minutes (for poultry) to be made safe when the coldest part is 140°F (60°C) (FSIS, 2005; FDA, 2009, 3-401.11.B.2). Indeed, the food pathogens that can multiply down to 29.7°F (-1.3°C) – Yersinia enterocolitica and Listeria monocytogenes – can only multiply about once per day at 40°F (4.4°C) and so you can hold food below 40°F (4.4°C) for five to seven days (FDA, 2011). At 126.1°F (52.3°C), when the common food pathogen Clostridium perfringens stops multiplying, it takes a very long time to reduce the food pathogens we’re worried about – namely the Salmonella species, Listeria monocytogenes, and the pathogenic strains of Escherichia coli – to a safe level; in a 130°F (54.4°C) water bath (the lowest temperature I recommend for cooking sous vide) it’ll take you about 2½ hours to reduce E. coli to a safe level in a 1 inch (25 mm) thick hamburger patty and holding a hamburger patty at 130°F (54.4°C) for 2½ hours is inconceivable with traditional cooking methods – which is why the “danger zone” conceived for traditional cooking methods doesn’t start at 130°F (54.4°C). [Note that Johnson et al. (1983) reported that Bacillus cereus could multiply at 131°F/55°C, but no one else has demonstrated growth at this temperature and so Clostridium perfringens is used instead.]

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Thanks for a great answer. I'm still concerned that enough toxins could be produced during cooking that it wouldn't help that the food is eventually free of dangerous microbes. Bacillus cereus, for example, produces heat tolerant enterotoxins during growth. –  Chris Steinbach Dec 3 '12 at 22:35

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