Bullshitometer: Is it OK to leave breastmilk out of the fridge for several hours?

Information on storing expressed breastmilk (EBM)--particularly the question of how long you could leave it outside the fridge--wasn't something I really focused on back in the days when I actually used a breastpump--probably because as a freelancer I was lucky enough to have very little need for pumping. Scrutinizing milk storage guidelines is something mums tend to do if they are away from the baby a lot, because they are trying really hard to use every last drop.

So I always treated breastmilk as highly perishable, and pumped it on the day it was to be given or occasionally froze a bit for a few days. When I accidentally left a freshly-expressed container on my desk for a few hours once, I chucked it. I wasn't too sure what the guidelines were, but breastmilk is raw milk.... right? And I certainly wouldn't drink a bottle of raw milk that had been hanging around in the fridge for days, nor would I drink a glass that had been on the counter for more than a short time. (Well, okay, I don't think I'd drink raw milk period, but that's a side issue.) 

So I was a bit surprised and wary when I started coming across information—fellow online discussion group members, backed up by Kellymom, La Leche League and all the usual sources—stating you could leave a container of EBM at room temperature for up to eight hours, and for several days in the fridge. Could this really be true? After all, we all know that a bottle of formula can't be left out at room temperature for more than a couple of hours...

What the guidelines say

I could be forgiven for being a bit suspicious of the claims of Kellymom and LLL et al in this area, since a) they’ve made a few dodgy claims in the past; and b) the evidence basis underpinning these claims seemed to be a bit, well, weak. It consisted of some studies--see Hamosh et al, Igumbor et al, here, Ajusi et al, Sosa et al, Olowe et al, and Slutzah et al for examples--which either expressed some breast milk and measured what happened to the naturally-present bacteria after several hours at various temperatures, or deliberately contaminated some EBM with specific bacteria in order to see what happened ("challenge studies"). The studies show some quite impressive results, with bacteria appearing to grow unexpectedly slowly or even dying off in the breastmilk, while no such results were seen for infant formula. Unfortunately, we are talking about a limited number of studies involving, in most cases, only a small number of samples; some of the studies are also quite old, dating back to the 1980s in some cases.

However, I concluded my suspicions may have been a little hasty after perusing Handling and storage of expressed breast milk, a set of guidelines issued by the Microbiological Safety Division of the Food Standards Agency of the United Kingdom and used by the National Institute for Health and Care Excellence (NICE)—and as such, likely (I felt) to represent a more neutral and trustworthy viewpoint on the subject. Based on its review of the evidence in existence, the guidelines state: "Many studies have looked at the growth of bacteria in EBM under different storage conditions in both tropical and temperate climates… Many of the studies in this area are relatively small and are often difficult to compare directly due to design and methodology. However, collectively they provide a reasonable body of evidence in support of the bacteriostatic behavior of EBM during several hours under ambient conditions and several days at refrigeration temperatures." Similar conclusions were reached by the Center for Disease Control (CDC) and the Academy of Breastfeeding Medicine (ABM). In other words, it looks as though Kellymom et al are basing their assertions on a handful of rather small studies because that really is pretty much all we have to go on right now, not because they are cherry picking. 

Advice on how long one can leave breastmilk at room/refrigerator temperature varies quite a bit from source to source. Around 3-8 hours at room temperature, and 3-8 days in the fridge are typical recommendations from sources such as LLL, Kellymom, Medela, Ameda and the CDC, but I have seen suggestions ranging from "up to two hours at room temperature, up to two days in the fridge," to Jack Newman's suggestions of up to 8-12 hours at room temperature and 8-11 days in the fridge.  

“Room temperature" can mean different things. Unsurprisingly, the higher the surrounding temperature the faster bacteria multiply (as the Igumbor study noted). The ABM protocol suggests EBM may be stored for up to 8 hours at lower temperatures, but only up to 3-4 hours at 27-32 degrees C, while the Hamosh study states that breast milk "should not be stored at 38 degrees C."

Surprisingly, fridge temperature can vary as much as room temperature. From the NICE guidelines: “The last comprehensive domestic refrigerator survey in the UK was carried out in 190. The mean temperature found ranged from -1 degree C to 11 degrees C over a 7-day period, and the overall mean temperature was 6.6 degrees C, with nearly 70% of fridges operating at more than 5 degrees C. Variation was found in performance between fridges and within each fridge over time. Different temperatures were also recorded in different parts of single fridges.” Other surveys cited by the guidelines tell a similar story. This matters, because assumptions that EBM is safe in the fridge for several days are based on studies that examined breast milk place in refrigerators that really had been set to the correct temperature.

As stressed by the ABM protocol, “Studies show that human milk containing fewer bacteria at the time of expression develops less bacterial growth during storage and has higher protein levels compared to milk that has an abundance of bacteria.” As shown above, the ABM suggests that the upper limit for storage (6-8 hours at coolish room temperatures) is only acceptable if the milk is "very clean." This is echoed by the NICE guidelines, which emphasize the need for "attention to hygienic preparation."

Raw (breast) milk

Breastmilk has a number of interesting compounds which either kill bacteria ("bactericidal") or stop them from multiplying ("bacteriostatic"), including secretory IgA, leukocytes, lactoferrin, lysozyme, lactoperoxide and lactobacillus bifidus growth factor. These appear to work to suppress the growth of bacteria in EBM; they don’t exist in formula, which is why a formula bottle can’t stay out of the fridge for too long. The way breastmilk can kill bacteria or stop them in their tracks is fascinating but much too complex to cover here; see "Further reading" for more information. 

It's important to bear in mind that thawed frozen milk has less bacteria-inhibiting power depending on how long it was frozen, because some of these compounds are significantly affected by the freezing process. This is even truer for pasteurized milk.

Many of these compounds also exist in raw (=unpasteurized) cow’s milk—and I'll be frank, part of the reason why I was initially skeptical of the idea that it was okay to leave EBM hanging around for hours at room temperature was because I would never dream of doing the same thing with raw cow's milk, even if I did choose to drink such stuff. I am assuming that this difference has to do with the cleanliness of the collection conditions, something stressed by the NICE and ABM guidelines. Women have—quite rightly—fought for the right not to be sent to toilet cubicles to pump their milk, whereas if you’re a cow, the world is your toilet because cows crap everywhere (including during milking) and cow manure splatters. Even the cleanest milking barn isn’t an setting where I would feel comfortable pumping milk for my child. 

Bullshitometer verdict

Is it okay to leave breastmilk at room temperature for several hours (or in the fridge for several days)? My answer is that, thanks to a number of useful bacteriostatic and microbicidal compounds found in EBM, the correct answer is probably a cautious “yes.” Turns out I probably could have used that forgotten container that I poured down the sink.

Some caveats. Firstly, “a few hours” means just that—not 8-12 hours as a few sources like Jack Newman have claimed. Given that Newman gives no evidence basis for such generous time periods and none of the studies that I have seen support them, I am going to go ahead and discount them (along with Newman's other helpful suggestion that we should just avoid the need for expressing in the first place by bringing our babies with us absolutely everywhere, including the cinema.... erm, no thanks, Jack). The ABM’s suggestions of “[*Room temperature] 3–4 hours optimal, 6–8 hours acceptable under very clean conditions; [*Fridge] 72 hours optimal, 5–8 days under very clean conditions,” seem more reasonable and accord with the (admittedly rather limited) studies that have been performed.

Secondly, "room temperature" really means something not much higher than 30 degrees C; if mothers are planning to be out and about all day in hot weather, a cooler pack with ice sounds like a good plan.

The "store in the fridge for several days" thing requires a little caution too, simply because in the real world people's fridges are frequently nowhere near as cold as they should be. If mothers want to leave EBM in the fridge for several days, they would be wise to think about the age of their equipment, maintain the fridge properly, use a fridge thermometer and store EBM at the back of the fridge, not in the door (which is significantly less cold).

Finally, as discussed in the ABM protocol, the storeability of breastmilk depends a lot on how cleanly it is expressed. Over the past few years there has been a big increase in computer and cellphone usage at work and leisure, with many mothers fitting pumping sessions in between typing sessions--and keyboards are notorious for being covered in germs. Very careful handwashing would appear to be called for if we want to store breastmilk as long as permitted by the studies that have been cited. And for a number of reasons, exclusively-pumping mothers are a lot commoner than they used to be. So we also need consider ways to ensure that women have safe and clean places to pump not just in workplaces but also in shopping centers, stations and so on.

Finally: just a plea for more and better research on EBM storage and microbial safety! These experiments are surely not particularly complicated to undertake, and with more mothers expressing milk than ever before, there is clearly a need for more information. Really good, evidence-based guidelines would improve safety, increase mothers' confidence and perhaps encourage the acceptability of EBM among daycare nurseries that are currently reluctant to handle the stuff. 

Further reading

Handling and storage of expressed breast milk (NICE)

Good basic guidelines. It includes an interesting table allowing you to compare the time limits recommended for different storage conditions by all sorts of different sources, from UNICEF to the UK Association for Milk Banking.

ABM Clinical Protocol #8: Human Milk Storage Information for Home Use for Full-Term Infants (Original Protocol March 2004; Revision #1 March 2010)
A more detailed guide, including discussion of appropriate container type and issues such as thawing and refreezing.

Antimicrobial Activity of Breastmilk Against Common Pediatric Pathogens
Esperanza F. Rivera, M.D. and Ricarchito B. Manera, M.D.
A bit old, but this is a nice readable overview of EBM's bacteria-zapping properties.

Antimicrobial Factors in Milk
Illini DairyNET (the Online Resource for the Dairy Industry)
This one looks at cow's milk, and is an interesting comparison.

Effect of storage and heat on antimicrobial proteins in human milk.
T J Evans, H C Ryley, L M Neale, J A Dodge, and V M Lewarne
More detailed information on the extent to which freezing/heating EBM can alter its bactericidal/bacteriostatic powers.