Section: CME Category: Wound Care

Amputation Site Soft Tissue Restoration Using Adipose Stem Cell Therapy

Debra Bourne, MD

Debra Bourne, MD discusses the augmentation of soft tissue deficits and amputations with fat grafting, its advantages and disadvantages. Dr. Bourne cites studies to support her statements.

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Goals and Objectives
  1. Understand the need for improved treatment strategies for soft tissue deficits in amputation sites
  2. Appreciate the potential role of stromal vascular fraction enriched fat grafting for the treatment of soft tissue deficits in lower extremity amputation sites
  3. Determine outcomes for patients who undergo fat grafting for the treatment of soft tissue deficits in amputation sites
  4. Understand the psychosocial and quality of life impacts of soft tissue improvements
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  • CPME (Credits: 0.75)

    PRESENT e-Learning Systems is approved by the Council on Podiatric Medical Education as a provider of continuing education in podiatric medicine. PRESENT e-Learning Systems has approved this activity for a maximum of 0.75 continuing education contact hours

    Release Date: 03/16/2018 Expiration Date: 12/31/2020

  • Author
  • Debra Bourne, MD

    Plastic Surgery Resident, University of Pittsburgh Medical Center, Department of Plastic Surgery

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    Debra Bourne has nothing to disclose.

  • Lecture Transcript
  • TAPE STARTS - [00:00]

    Male Speaker: It’s a pleasure to introduce Deborah Borne who… we’ve met through plastic surgical meetings. And she's… we are very honored to have Dr. Rubin and Dr. Kacey Marra, a lab represented by her today, which is… they are certainly one of the leaders, if not, the leader in adipose derived stem cell reconstructive option. So welcome, Deborah. Deborah is a medical… is a resident at Pittsburgh, really great, qualified resident who's going into hand surgery and has also really contributed to their research effort. So welcome, Deborah

    Deborah Borne: I'd like to thank everyone for the opportunity to present our work on treating amputation site soft tissue deficits using stem cell enriched fat grafting.

    Our main objectives are outlined here. I hope to give all of you a better understanding of the limitations of the current treatment, options for soft tissue deficits and lower extremity amputation sites and to teach a new… a novel technique using stem cell enriched fat grafting for these deficits. And hopefully by the end of the presentation, you can decide for yourselves whether you think this is a treatment option that you think should be pursued further and would be good for recommending to patients in the future.

    I would like to acknowledge the United States Department of Defense who provided the funding for this clinical trial. This is in hopes of providing better treatment for our wounded warriors. This project was done under the leadership of Dr. Peter Rubin and Kacey Marra in the University Pittsburgh Adipose Stem Cell Center. I'd also like to thank Colonel Pasquina at the Walter Reed National Military Medical Center who was instrumental in recruiting patients for this clinical trial. Sidney Coleman is a surgical consultant for the procedures performed and also developed the cannulas used for fat grafting procedures.

    Since Operation Enduring Freedom in 2001 followed by Operation Iraqi Freedom and Operation New Dawn in 2010, 1,646 United States service members have suffered from major limb amputations. Nearly 2 million people in the United States are living with limb loss and there are 185,000 amputations in the United States every year. This represents a huge burden of human suffering, economic loss, and disability.

    Due to advances in medical care and increased technology in prosthesis, 428 United States military service men who have been injured have been able to return to active duty following an amputation and 57 have been redeployed to combat situations. However, the vast majority, 74%, have not been able to return to active duty. In the civilian arena, 30% of patients who undergo traumatic amputation do not return to the workforce.

    Reasons for this are multi factorial. But even in the best circumstances with an optimal soft tissue envelope, there is significant pressure between a residual limb and a prosthesis. This can lead to chronic wound breakdown and pain. If there's inadequate soft tissue coverage over nerve endings, this can cause excruciating pain for these patients. Inadequate soft tissue can lead to poor prosthesis fit and inability for patients to do even daily activities of daily living.

    Traditional treatment options often include surgical readjustment of the soft tissue envelope. This can be done by bone shortening, which can have a mechanical disadvantage, by using local flaps which often is very limited especially in traumatic amputations where the zone of injury could be extensive, or free flaps where you can take tissue from another part of the body and replant it onto the limb. This has high donor site morbidity and it's a long complicated procedure with a long recovery period.

    A new prosthesis or better fitting of the prosthesis could be attempted but it is often unsuccessful. Patients are often resigned to a chronic local wound care and reliance on pain medication.

    Fat grafting has emerged in plastic surgery, orthopedic surgery, and multiple different domains as a successful treatment option for all over the body in treating soft tissue deficits. It is minimally evasive and has an excellent safety profile. There is almost no donor site morbidity and some patients actually consider getting liposuction to be a benefit.

    There's high patient satisfaction associated with this procedure. And skin and fat grafting not only improves volume, but it also can improve skin quality, vascularity and tissue pliability in regions that have scarring fibrosis and poor skin quality. This is seen in patients with conditions such as radiation damage.

    One of the main drawbacks of fat grafting continues to be unpredictable volume retention. And the literature of volume retention after fat grafting ranges from 20 to 80%. There's a lot of research being done to try to figure out why there's such a wide range of volume retention and to improve volume retention.

    One method is to enrich fat with the stromal vascular fraction. This is a combination of cell types including adipose derives, stem cells, [indecipherable] [04:56] stem cells, endothelial progenitor cells, pericytes, and macrophages.


    It can be derived using collagenase digestion of adipose tissue that has been harvested by liposuction and can be added back into fat to improve the volume retention and the vascularity of the region.

    Another analysis looking at SVF, stromal vascular fraction enriched fat grafting, has shown that it improves volume retention from 45% to 60% and does not increase the number of complications. Although there is money papers looking at fat grafting different regions of the body, fat grafting to the lower extremity is something that has yet to have very much research. And for amputations, there's actually no research currently out there.

    Cosmetic calf augmentation has been performed and there have been no significant complications reported. However, patients need generally two to four operations to get adequate volume.

    For atrophy in various regions of the lower extremity, fat grafting has been used with high patient satisfaction. There's only one study looking at stromal vascular fraction enriched fat grafting to the lower extremity. And in this study, there are only two patients treated with stromal vascular enriched fat grafting. They reported a rate of 25% volume retention. And the same study also had traditional fat grafting without SVF enrichment in two patients and they found a 44% volume after two treatments in those patients.

    Since there's currently no data in the literature looking at fat grafting to amputation stumps, we proposed a study to fill this void. Amputation stumps, particularly those that are traumatic in origin from blast injuries with an extensive zone of injuries, a hostile bed for fat grating. Not only is it a dependent region which is subject to edema and congestion and poor blood supply, it also is subject to significant pressure against to prosthesis or against to wheelchair. And due to scarring and fibrosis in the area because of the trauma, again, has a poor blood supply.

    Because this is a hostile environment for fat grafting, we chose to enrich the fact with stromal vascular fraction. We set out to determine safety of this procedure, the volume retention over time and the effect of this procedure on pain, disability and quality of life in these patients.

    This is a pilot cohort prospective clinical trial in which five patients were enrolled from the Walter Reed National Military Center. All patients were wounded warriors who had blast injuries to their lower extremities. All patients had amputations which had poor soft tissue coverage resulting in pain, poor prosthesis fit and limited functionality. All patients have stable amputation stumps. They had to be at least three months from the time of injury or their most recent surgery, when, in fact, most patients were actually several out from their date of injury. Exclusion criteria included diabetes, peripheral vascular disease, open wounds, infection or draining sinuses.

    This is the demographic data of the five patients who were enrolled. They were all Caucasian males from the military, all were in their mid 20s to mid 30s, none had any significant medical co-morbidities, none were smoking actively at the time of surgery. BMI was recorded at the initial operation and then was followed throughout the length of the study and there was no significant change in BMI. All patients suffered from a blast injury from IED explosions, all had bilateral amputations of the lower extremity at the transfemoral or hip disarticulation levels.

    Liposuction was performed to obtain the lipoaspirate. Liposuction was taken from either the abdomen or flanks depending on where the patients had fat deposit that could be used. The lipoaspirate was then split into half. Half was sent to the University of Pittsburgh Medical Center Hematopoietic Stem Cell Laboratory where it underwent SVF isolation. And then half was centrifuged at 3,000 RPM for three minutes and the aqueous layer was decanted by gravity and the oil layer was removed to using surgical patties leaving the fat ready for injection.

    At the Stem Cell Laboratory, the lipoaspirate was digested using the collagenase process in order to isolate the stromal vascular fraction. Collagenase was added to dissolve the extracellular matrix and it was incubated. Then centrifugation was performed to separate out the high density stromal vascular fraction palate so that the extracellular matrix and mature adipocytes could be decanted. The stromal vascular fraction palate was then re-suspended and filtered and then washed and reconstituted. It was then packaged in a sterile container with another sterile container for transport back to the operating room.

    Prior to release and injection into the body, several parameters had to be met to ensure safety. We look at cell viability, cell yield, presence of endotoxin and Gram stain to ensure that quality measures were met and that the stromal vascular fraction was safe for re-implantation into the patient.


    Back in the operating room, the stromal vascular fraction was added back to the fat and mixed. And then the fat was was transferred into 1 milliliter syringes in order for it to be grafted. All grafting was done using small Coleman cannulas with a blunt tip and a single-hole pedestal end. Multiple different port sites were used for injecting the fat. The fat was injected in small aliquots upon withdrawal of the cannula. Areas of significant scarring or tethering were rigotomized using an 18-gauge needle.

    Fat grafting was continued until the compliance of the tissue would not allow for any further fat grafting or the desired volume was reached.

    All patients went home the same day of surgery. The time to isolate the stromal vascular fraction was approximately 106 minutes and the time for the complete operative case was 245 minutes. The mean volume injected was 126 milliliters with a range of 85 to 270 milliliters. Patients were asked to keep pressure off the site of the surgery for 68 weeks at which point they were able to return to using their prosthesis as before.

    Often, patients actually had to have their prosthesis refitted because they now had more padding over areas that recently were deficient in volume. Patients were seen at three to six days following the surgery to ensure healing and there were no complications. They're seen again at one month, three months, six months and up to two years. All patients have subjective improvement in soft tissue and skin quality.

    There were no major complications. The most common adverse event was pain and bruising at the site of the liposuction, which was to be expected. This was treated with a short course of oral pain medication and did not last more than a few days. There were no significant infections, cysts or wound healing problems.

    Volume retention was assessed using CT scan. You can see from this three-dimensional reconstruction of a CT scan, this patient has a transfemoral amputation. This is a site where the distal cut end of the femur has poor soft tissue coverage and this makes it difficult and painful for them to wear prosthesis.

    Following fat grafting, we can see an improvement in the volume of this region. A dedicated musculoskeletal radiologist read all of the CT scans. Baseline fat graft volume was determined by comparing the preoperative CT scan to one month CT scan. One month was chosen because at this time, we would expect the edema from the initial surgery to decrease. However, we would not expect significant volume resorption.

    CT scans were then measured again at three months, six months, one year and two years.

    This graph demonstrates volume retention over time. At two years, volume retention was 61%. This is similar to studies that have been at University of Pittsburgh looking at fat grafting to the craniofacial region where we found a volume retention of 63% at two years. However, the curve is different than we've seen in craniofacial fat grafting.

    In other studies, we've seen that volume tends to remain… tends to decrease initially until about six months and then it tends to plateau. In the lower extremity, we are seeing that the volume continues to decrease even up to two years.

    This is actually similar to some research that has been done by Dr. Jeffrey Kassinove who is a plastic surgery physician at University of Pittsburgh and his wife, Beth Kassinove, who is a podiatrist. They have been working together to do fat grafting to metatarsal heads for patients who have pain in their feet. And they found that at two years, the volume of the fat graft actually goes back to baseline but the thickness of the dermis has improved in two years, and that remains. And also relief of symptoms remains at two years. So maybe the fat grafting to areas that are dependent and that have significant pressure actually act differently than areas in other regions of the body.

    A portion of the fat was sent to the lab and was analyzed by flow cytometry. Cells were stained for their cell markers using monoclonal antibodies and then suspended in a fluid and passed in a stream for analysis. This allowed us to determine what our cellular composition was. It also allows us to determine cell viability using DAPI exclusion.

    These are our results, 62% of the cells were adipose derived stem cells. They were CD34 positive. 15% were endothelial cells as marked by CD31 positivity and 6% were pericytes as marked as CD146 positivity.

    Patients who had a higher percentage of adipose derived stem cells had a trend towards improved volume retention. This is not surprising since adipose derived stem cells are instrumental in maintaining the volume of fat at volume fat grafting. Not only are adipose derived stem cells able to differentiate into mature adipocytes, they can also act as adipose progenitor cells. Furthermore, they can promote neoangiogenesis by secreting factors such as VEGF and by differentiating into endothelial cells.


    Patients who had higher cell viability had a trend or actually had a significant correlation with improved volume retention. This again is not surprising.

    Higher cell viability would be expected to correlate with greater volume retention as more cells would be allowed to survive and to divide.

    Additionally, patients who had higher cell viability after liposuction and processing will be expected of healthier cells. They might be better able to withstand the transient ischemia that they would undergo after being grafted into a new site.

    We also looked at psychosocial outcomes, general health, and general wellbeing with the SF 36. We looked at multiple different domains.

    The physical health domain at baseline was moderate to good at 75%. There was a dip at three months but it came back to baseline at six months and surpassed baseline at one year and two years with score of 87%. Energy was in the moderate range at 50% at baseline. It increased slightly at three and six months, came down to baseline at one year and then went to a high 64% at two years.

    Physical functioning was quite low at baseline at only 9. It increased up to one year to a high of 40 and at two years was 18 which is significantly higher than their baseline. General health fluctuated in the moderate range around 60. Social functioning again fluctuated around 80% in the good range. And emotional role functioning was in the good to excellent range with a baseline of 75 and then at two years of a hundred.

    All of these domains did not have any statistically significant change but many of them were higher at two years and they were baseline and these results are encouraging. With a larger sample size, we may be able to find a statistically significant difference and I think that these results are very encouraging.

    Depression was assessed using the Beck Depression Inventory. Anything less than 12 or 13 is considered subclinical. Patients never had a mean inventory school above eight and there was no significant signs of depression throughout the study.

    I think this represents some of the most exciting and encouraging data that we have to present. The pain scores are measured using the 10 point visual analog scale. Ten representing excruciating pain and zero representing no pain at all.

    There was a decrease in the average pain score from 4.5 at baseline to zero at two years. Although statistical significance was not reached, this is very encouraging and I think with a greater number of patients, we might find some really exciting significant results.

    Disability indexes were assessed. The functional mobility assessment is used when assessing a patient's ability to use an assistive device. Generally, when fitting the prosthesis, you want to see a score of at least 48, the highest possible score is 60. Unfortunately, none of the patients reached the score of 48.

    At baseline, the score was 45 and at 40, it was 43 at two years. There was no significant increase or improvement.

    The lower extremity functional scale is an assessment of a patient's ability to perform activities of daily living. It ranges from 0% to 100% with 0% being severe disability. Again, unfortunately, the score has really remained quite low at 25% at baseline and 23% at two years.

    I think our lack of improvement in these scores is two-fold; first of all, as we talked before, this is a small sample size, but also all these patients had high bilateral amputations and had significant disability. And I think these disability indexes were not really able to pick up on differences in this particular patient population.

    Let's talk about some of the individual patients who were treated. This is a 25 year old man with a left hip disarticulation and a right transfemoral amputation following an IED explosion.

    We can see the purple is the area we plan on doing the fat grafting. He also has some areas of fat in his abdomen that we used for liposuction. And then the area that's marked with the red, blue, and green is the area we plan to do the fat grafting.

    This is an area that when he sits on his wheelchair is subject to a lot of pressure and he has chronic wound breakdown and pain in this region. Here's a close up, we can see a little bit better.

    So here are his results. Preoperatively, we can see that he has areas of ulceration and a little bit of scabbing where he's healing. He has chronic wound breakdown at this area and it's causing him pain and frustration because he's chronically having to put dressings in this region.

    Following surgery, his skin quality is significantly better and he has much better padding in this region. And even up to two years, we can see that the difference is maintained. His pain score at baseline was 2 and at two years, it was 0. He was able to sit in his wheelchair much more comfortably. This patient is the patient that we saw at the CT scan of earlier. He's a 32 year old gentleman with bilateral above knee amputations.


    Again, you can see here that he does not have very good soft tissue padding over the distal cut end of his femur. He has some skin changes here along the scar and he has a pain level of 7 when using his prosthesis because of the pressure against the femur.

    You can see our operative markings. This blue line here along the scar represents where we planned to do some rigotomizing with an 18 gauge needle. And then post operatively, this is only at four days so he's still significant swollen, but you can see the improvement we have in volume.

    And even at 12 months, he has significant improvement in volume around his bone compared to preoperatively and he has improvement in the skin changes that we saw preoperatively. His pain level went from a 7 preoperatively, to 0 at two years.

    And he was able to use his prosthesis, his stubbies, as he calls them, without pain at two years for activities of daily living.

    This is a 25-year old man with bilateral hip disarticulations. Here we can see -- this is his left ischial tuberosity and he has chronic wound breakdown in this area. You can see just a little area right there of ulceration but that entire region breaks down often for him because of the pressure between his ischial tuberosity and his wheelchair.

    And you can see when you pinch his skin preoperatively, that it's very thin coverage over top of that ischium.

    So post operatively, we see a huge improvement. He has much better skin quality. When you pinch it, there's a lot of tissue there padding that bony prominence, and this was very helpful for the patient.

    This is a 30-year old man who again had bilateral above knee amputations. He also had injuries to both of his upper extremities from the same IED blast. And here, this skin graft is tethered to the muscle underneath and every time he moves his muscles, it pulls on this tethered skin graft causing irritation, pain, and it makes this prosthesis fit difficult.

    He underwent fat grafting with some improvement to his lower extremity but what really made a difference for him, this is his upper extremity so his left upper extremity here, you can see and not only does he have a distal amputation of his ring and small fingers but he has this skin graft that's very thin and it's tethered all along the base of his thumb, the thenar eminence, hypothenar eminence. It makes it difficult for him to push his wheelchair and it makes it difficult for him to grasp objects.

    You can see here how thin the skin is, and that it's tethered to the tissue underneath. So at the same time is his lower extremity fat grafting, we put 18 ccs of fat in this region as well. And he was extremely happy post operatively. he was able to hold a Starbucks coffee cup, which he couldn’t do before with that hand, which is a huge, for him, quality of life issue. He was also able to move his wheelchair without pain. And the pain in his hand went from a six to zero.

    So in conclusion, stromal vascular fraction-enriched fat grafting is a promising treatment for traumatic amputations. This is the first study to look at this population with this treatment and we think that the results here are really very exciting. Volume retention can be expected to be about 60% at two years. Inherent factors within the patient’s cell biology, including adipose-derived stem cell percent and cell viability will impact volume retention. We did not find any significant change in disability indexes but we did find a trend towards improvement in pain and in quality of life.

    We are now undergoing a follow-up study looking at 30 patients with lower extremity amputations. They are currently in enrollment and they’re being randomized to either getting stromal vascular fraction-enriched fat grafting or non-enriched fat grafting to their lower extremity. We are very excited about this study and look forward to presenting the results hopefully in the next year or so.

    These are references. And then just a quick plug for the International Federation of Adipose Therapeutics and Science meeting that’s going to be occurring in Miami Beach at the end of November, I would encourage all of you to go. There’s going to be some really exciting research looking at adipose-derived stem cells and all of the potential implications and we would love to have your abstracts presented there. The deadline for submitting the abstracts is June 7. Thank you.

    Male Speaker: It’s really great. That’s great work. It’s a little unfair for them to ask for so many disability and functional scores for only five patients, but from a plastic surgical perspective, it makes a lot of sense. Other people showing profound changes in the skin of radiation, patients who get fat injections. So my question is, what are you guys doing in the lab to look at the tissue effects of adipose tissue?


    Male Speaker: Because the volume retention you got at 60% is great. You can see this with your own two eyes how much that makes a difference around those pressure points for the prosthetics. But it really does seem to have changed the quality of the scar as well. Is there any thoughts about the mechanism for that or are you taking biopsies and looking before and after in future studies?

    Deborah Borne: That’s a great suggestion. We aren’t doing that but I think that’s something we potentially want to do moving forward. And I think the mechanism probably has to do with improving the vascular supply. I think that the stem cells help with neoangiogenesis and a lot of the problem is due to poor vasculature. And also, as I mentioned before, the dermal thickness in the fat grafting over metatarsal heads improves with fat grafting, so that may also be something we might want to look at. And they’ve been using ultrasound to look at that so that might be something we want to do moving forward.

    Male Speaker: It’s a really impressive observation about the thickening of the dermis over metatarsal heads. That’s great work. Thank you.

    Male Speaker: Thank you for that presentation. It’s an interesting twist on really an old procedure that was done back in the early ‘90s even, not this way. But I have a couple questions. Is there actual engraftment of this tissue or do you think the positive effect you’re saying are really due to the paracrine effect of the ASCs and the recruitment of VEGF, other vascular inducing factors that are regenerating the tissue? That’s number one.

    And number two, these are all healthy young warriors for the otologist grafts. What do you think is going to happen if we take it in a diabetic patient covering an amputation site and a diabetic patient who has plenty of fat but is 55 years old, renal failure, and certain other comorbidities that we see.

    Deborah Borne: Great questionS. To your first question, I think that it’s a combination. Some of the fat mature adipocytes, some of them do survive and some of the adipose derived stem cells do differentiate into mature adipocytes. But I think the paracrine effects also are really instrumental in improving sort of the whole milieu of the area. Of course, we didn’t look specifically at that or take biopsies but that’s what I suspect is happening.

    And then as far as what’s going to happen if we start treating patients with a lot of comorbidities like diabetes, peripheral vascular disease, things like that, I think that we’re going to see that the volume retention is not as high. But the benefit of this procedure compared to other procedures, flaps and things like that, is that it is minimally invasive and quite safe. So I think that we’re not going to hurt these patients by doing this but they may need more procedures to get the same result because I suspect that the retention is not going to be as high.

    Male Speaker: Do you think… and I’ll leave the microphone in a second. If I’m not mistaken, you had a long operating time for this where people are really subjected to three hours or four hours in the OR. And with that said, can this be done as an outpatient or at least in separate sessions? I presume the most intensive session really would be the harvesting of the adipose tissue, then you could spin it down. Isn’t there a way that you might be able to do that like as an outpatient to do the injections like we often do with other clinical procedures?

    Deborah Borne: Sure. So these were longer procedures because, first of all, there is 100 minutes for the SVF isolation, although you can sort of use that time to process your other fat. But I think this can be done faster.

    Because those are clinical trial, we wanted to sort of do everything perfectly and pay really close attention to detail. I don’t think there was sort of in an impetus to do things quickly but I’ve certainly been in cases like cosmetic fat grafting cases where we’ve gone much faster. And if you’re not having to isolate the stromal vascular fraction, if you’re just doing unenriched fat grafting, I think you can still have a significant improvement in volume and faster than that.

    And although these studies, like you said, were done in the operating room, fat grafting can be done in the clinic if it’s a small volume and small area under local anesthesia. And we do do that for other indications. So I think that’s a possibility.

    Male Speaker: Thank you.

    Male Speaker: Hi. Could you please elaborate on the age related effect you think occur with adipose MSCs? The age window of your patients were quite similar, right?

    Deborah Borne: Yeah.

    Male Speaker: But do you think as they age, if you were to submit them to similar procedures, could you please elaborate what you think would be the effect?


    Deborah Borne: I mean, a lot of studies have been done looking at facial aging and doing fat grafting for improving facial volume since we all lose volume on our faces over time. And those patients are much older, and they tend to have pretty good volume retention. But that’s a different population because you’re looking at a non-scarred area and you’re looking at a face which is vascularized quite well.

    So those patients do do well. They do have good volume retention. But I couldn’t say in this population, in this region, if that would necessarily correlate. I think we would really have to do studies looking at those patients specifically.

    TAPE ENDS - [30:35]