A couple of weeks ago a study titled “Foot Bone Marrow Edema after 10-Week Transition to Minimalist Running Shoes” was published on-line by the journal Medicine and Science in Sports and Exercise. The study created a bit of a stir in the news, with the typical hyped up headlines accompanying articles on the paper. “Barefoot Running Can Cause Injuries, Too” proclaimed the New York Times. “Whoa there! Quick switch to ‘barefoot’ shoes can be bad to the bone” was the headline on Sciencedaily.com. The reality is that the results don’t say much of anything about barefoot running (the study didn’t investigate barefoot running), and may not even say anything conclusive about injury risk in minimalist shoes (I’ll explain why below).
The study was conducted by a group of researchers from Utah who set out to investigate how transitioning into Vibram Fivefingers (VFF) from more traditional shoes might affect the anatomy of the legs and feet. They split a group of 36 experienced runners into two groups – 17 continued running in their typical shoes for the next 10 weeks, and 19 made a variably gradual transition to running in Vibram Fivefingers over the same 10 week period (following transition advice that was published on the Vibram website in 2011 – this advice has since changed). The researchers took MRIs of the legs and feet of all runners both before and after the ten week period with the goal of assessing whether there might be any signs of increased injury to the tendons or bones of the VFF group relative to the non-VFF group.
The results showed no difference in soft tissue response – the the tendons of the Vibram runners were similar to those of individuals who did not make the minimalist transition after the ten week period (they looked at the Achilles tendon, dorsi-flexor, plantar-flexor, peroneal tendons, and plantar fascia). Good news for those who might be worried about injuring the plantar fascia or Achilles tendon during a transition to more minimal footwear, especially since other anecdotal reports have suggested that those tissues might be at risk (It’s worth noting that it is possible that longer term usage could still lead to soft tissue problems).
Bone was a different story. The researchers were looking for signs of bone marrow edema (fluid accumulation) on the MRI images, and scored various bones of the foot using a standard rating protocol (0-4, with 4 being a full-blown stress fracture). Below are the results for bone as reported in the paper:
“These results show a higher incidence of intense signal sub-fracture bone marrow edema as designated by an MES of 3 (stress injury) in the Vibram group (3 out of 16 subjects in the Vibram group compared to 0 out of 20 subjects in the control group)…Increased signal intensity in the feet of the Vibram group to an MES of 2 was found in 8 of the 16 participants. Including the two subjects who suffered from stress fractures, 11 of the 16 subjects in the Vibram group were classified as “injured” (at least one structure with an MES greater than or equal to 2 ) at the end of the study.”
So approximately 2/3 of the runners in the Vibram group experienced an amount of bone edema (level 2 or higher) that would classify them as suffering from a “stress reaction” or “stress injury” in at least one of the bones measured (Note: there is a discrepancy in the number of subjects listed in the control and experimental groups reported in the Abstract/Methods/Discussion vs. the Results. The former sections list 17 control/19 Vibram subjects, the latter lists 20 control/16 Vibram subjects. Not sure why.) Two of these individuals developed stress fractures – one in the calcaneus, the other in the 2nd metatarsal. All makes sense, but here’s where things get more complicated.
Suppose you don’t lift weights. Tomorrow you go to the gym and do a bunch of curls, some sets on the bench press, a few rounds of leg press, etc. What would happen to your muscles? Chances are they’d be really sore the next day. They’d likely be swollen (which is why you might think you’ve buffed up a bit on one day of lifting!). You probably have done some actual microdamage to the muscle tissue. But, is that an injury? Or, is the process of repairing this damage what will make the muscles stronger? – i.e., the damage done by lifting triggers a repair response that ultimately makes you stronger.
If you’re smart you’d let your muscles rest and recover from the initial stress, go lift again several days later, and in a slow progression of lifting over the following weeks and months your muscles get larger, and you get stronger (and you don’t get hurt). If you’re not smart and you lift again the next day, and the day after that (maybe Spring Break is coming…) you might do some real damage. The reality is the training muscles is very much about stressing them a bit so that they repair and come back bigger and stronger. But you have to be smart about it.
Bone is not unlike muscle in this way. It adapts to repeated stress in order to better withstand future application of similar stress (Google Wolff’s Law). Bones that are used get stronger, bones that are not used get frail. The textbook example I use in my Anatomy and Physiology class is to compare the thickness of bones in the racket arm of a tennis player to those of the non-racket arm. Guess which ones will be more robust?
A difference between bone and muscle is that bone adaptation in response to stress can take longer. Bone regularly undergoes a process called remodeling. When we apply stress to bones they develop microdamage – think of this as small cracks that appear in the bone. However, just like the damage we do to our muscles, this is not necessarily a bad thing or an “injury” in the traditional sense of the word. Your body has little cells called osteoclasts and osteoblasts that travel around chewing up damaged bone and replacing it with fresh, new bone. This process is the basis for remodeling – making bones stronger in response to applied stress.
The thing with bone is that this process takes time, and bones can get weaker before they get stronger since damaged bone needs to be removed before it can be replaced. If you add a new stress too quickly, microdamage can add up faster than the body can repair it and this can cause the bone to break – this is what we call a stress fracture. What do you do when this happens? Put on a boot, take 6-8 weeks off, and let the osteoclasts and osteoblasts do their thing. They’re pretty effective little buggers, and in a few months you’re right back out there on the road or trail.
So what does all of this have to do with the study we’ve been looking at here? Well, edema in bone is a sign of remodeling. In the authors own words:
“An MES of 1 could very well be the product of the physiologic phenomenon of osseous remodeling due to stress which is essential to the normal development and maintenance of bone(2).With appropriate application of stress, the remodeling process results in a stronger bone structure – which is visible on the MRI by low levels of bone marrow edema.”
Edema measurements might simply correlate to the intensity of the remodeling process. A little bit of edema is indicative of bony repair that will lead to stronger bones. A lot of edema might indicate that the bone has really been damaged and is working really hard to repair itself before something really bad happens. The categorizations applied to the different levels of edema observed are simply a way to try and classify what is in actuality a continuous scale from normal remodeling to injury. Where you cross the line from one to the other seems rather uncertain for reasons I’ll describe below.
Research on Bone Marrow Edema
Rapid transitions have a tendency to stress the body. A transition can come in the form of a new or altered form of training as in our lifting example above, or it could be something as seemingly benign as running in a new pair of shoes. The transition exposes the body to a new condition, and this can stress the body in some way.
For beginning runners, simply taking those first few running steps is a stress (we all can recall how those first few weeks as a runner felt – it hurt!). For more experienced runners, adding speedwork is a stress. Adding mileage to a long run each week is a stress. Yet, we commonly employ these training methods to stimulate a training response that will ultimately make us better runners. Similarly, switching to any kind of shoe with different properties than you are used to will be a stress.
When we stress the body in a new and different way, tissues respond. For bone, one possible response is marrow edema in the feet and legs associated with a remodeling response. But here’s the key point – this bone marrow edema may not be symptomatic or progress to an actual injury. It may actually serve to make the bone stronger. Quite a different conclusion than that made by many articles that have covered the Vibram study. Here is some of the evidence I’ve found to support this:
1. The authors of the Vibram study point out that studies have shown that bone marrow edema can occur in the feet of new runners after only one week of running. Add a new stress, and the bones respond. See Trappeniers et al., 2003.
2. Schweitzer and White, 1996 placed a longitudinal metatarsal arch pad under the lateral side of one foot of subjects and had them wear it continuously for two weeks. Bone marrow edema was found in the foot/leg on the pad side in 10 out of 12 subjects. Only one subject showed signs of edema in the non-pad side. The femur and tibia even showed signs of edema in a few of the subjects. Two subjects showed a level of edema typically indicative of a stress fracture. None of the subjects were symptomatic (i.e., no pain) upon pad removal or after 1-week or 1-month follow-ups. Three subjects were followed up with again after another two weeks with the pad removed. Two showed no signs of edema, one showed reduced edema. The authors concluded that “altered biomechanics” such as via altered weightbearing should be added as an additional cause of bone marrow edema, with emphasis that it may not be of clinical significance (not indicative of symptomatic injury).
3. Lazzarini et al., 1997 imaged the feet of 20 collegiate runners immediately after the end of their cross-country season and 12 non-runners. 16 of the 20 runners exhibited bone marrow edema, only 2-4 of the 12 non-runners exhibited edema (there were two MRI readers hence the range). Runners exhibited edema in an average of 3.4 separate bones. None of the subjects who exhibited edema were symptomatic.
4. Bergman et al., 2004 took MRIs of the lower leg of 21 college runners (Stanford University) after their 8-week pre-season training program (men were running 50-70 miles per week, females 40-60 miles per week). Nine of the 21 runners had visible edema in at least one tibia, and 6 of these had edema classified as level 2 or 3 (using the same grading scheme as in the Vibram study). Interestingly, none of the runners with tibial edema were symptomatic in the 8 weeks of running leading up to the MRI, and none of them developed symptoms or signs of tibial stress injury in the year following the study. This demonstrates that a runner could have grade 2 or 3 bone edema and not be symptomatic or develop a clinically significant injury.
Putting all of this together it seems clear that when we stress our bones in a new or unusual way (e.g., starting running, running big miles, changing the positioning of our feet), edema is a pretty normal response, and probably a sign of bony remodeling that will ultimately make the bone stronger. And, the edema that occurs may or may not be clinically significant, even when it reaches levels that would be graded as a “stress reaction” or a “stress injury” using standard classification procedures. This is where I take issue with the Vibram study – it’s not clear to me that grade 2 bone marrow edema really constitutes an “injury.” Based on the Bergman study, even a runner with a score of 3 (classified as a “stress injury”) might also be asymptomatic and not go on to develop a stress fracture.
Each increasing grade of bone marrow edema is just a step along the continuum of the remodeling response, and in the Vibram study only 2 of the 16 VFF runners were actually classified as suffering a stress fracture. The rest? We don’t know how things would have turned out had the study continued. Maybe the edema would have died down in each and all would be normal after another 10 weeks (i.e., remodeling would have done its job and the bones became stronger and more robust). Maybe we would have seen a bunch more fractures had the study continued. Hard to say. What we can say is that switching to Vibrams did seem to trigger edema, and thus likely bone remodeling. This could make the bones weaker for a time and justifies a slow and careful transition. But, ultimately it’s not entirely out of the question that a headline for this study could have been “Vibram Fivefingers Stimulate Bone Remodeling and Adaptation.” Far from causing injury, they might actually make some of the foot bones stronger in the long run.
My biggest problem with this study is that it compares change to no change. It compares a novel condition to which a group of subjects are not adapted to a familiar condition that involves no change to what is normal. Thus, we have no way of knowing specifically if Vibram Fivefingers are particularly dangerous, if minimal shoes as a category are dangerous, or if the simple act of changing shoe type (to any type) might be dangerous. Is it the shoe, or is it the change?
The study would have been much stronger had they added a control of having a group of runners switch to a new shoe that is similar to the one they were used to, or perhaps something only slightly more or less cushioned than what they typically wear (motion control or a racing flat perhaps). If a lateral foot pad can cause edema in non-runner in just a few weeks, it’s quite possible that any footwear change can cause bone marrow edema in a runner when the shoe is unfamiliar. Thus, another headline could simply have been “Adapting to New Footwear Causes Bone Marrow Edema.” Maybe it has nothing to do with the fact that the shoe was minimal.
The above is similar to why drug studies use placebos. Placebos allow researchers to know whether an effect is due to some property of the drug being administered, or whether it is a property of the patient knowing they are getting a pill. The Vibram study needs a control to allow us to determine if bone marrow edema is caused by a footwear change, or whether it is specifically linked to a minimal shoe, or even more specifically to the Vibram Fivefingers.
Despite all of my concerns expressed here, I do believe that an ultraminimal shoe like the Vibram Fivefingers stresses the foot in new and different ways, and that the added stress to the foot can be quite high for someone used to more cushioned footwear. I absolutely believe that pushing a transition too hard in these shoes can lead to bony injury since I know people who have broken their feet running in them. I myself rarely ever run in them anymore because they make my forefoot ache (VFFs are the only shoe that does this to me, I think it has to do with the toe pockets). That being said, I also have two very good friends who have broken metatarsals in the past few years who never run in ultraminimal shoes like the VFFs. Broken foot bones happen to runners regardless of what they put on their feet, and we still have little conclusive data on whether stress fracture rates are higher in one type of shoe than any other.
The true value of this study is that it reminds us that any shoe change should involve some amount of caution, and it gives us something to point to as backup when we make that claim. The more different the shoe is from what you are used to (i.e., the bigger the change), the more care you likely need to take in transition. Running in a shoe like the Vibram Fivefingers will stress the feet and legs of someone used to running in a cushioned shoe, and if you push the transition too hard and too fast you’re potentially asking for trouble.