Hobson [ 10 ] was one of the first investigators to systematically demonstrate proteolytic activity of L. Vistnes et al. More recent studies of larval ASE help us see just how these proteolytic enzymes fit into the context of debridement and wound healing, for we now know that they include a wide array of matrix metalloproteinases MMPs , including at least the trypsin-like and chymotrypsin-like serine proteases, an aspartyl proteinase, and an exopeptidase-like MMP, active across a wide pH range [ 12 — 14 ].
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MMPs play critical roles in all phases of tissue repair and wound healing, including hemostasis, thrombosis, inflammatory cell activation, collagen degradation, fibroblast and keratinocyte migration, and tissue remodeling. Disturbances in wound healing can occur when one group of proteases is deficient or out of balance with another.
Telford et al. At least one of these chymotrypsin-like proteases has now been produced recombinantly in Escherichia coli [ 16 ] and could soon enter clinical trials as a purified debriding enzyme. DNAse may play an important role not only in debridement but also in inhibiting microbial growth and biofilm. The wealth of case reports and case series in the literature suggests that most clinicians are impressed by the debridement efficacy of medicinal maggots. Controlled studies of maggot debridement are less common, but quite worthy of examination.
In a prospective study of spinal cord injury patients with chronic, nonhealing pressure ulcers, patients were monitored for weeks while receiving standard wound care whatever modality was prescribed by the surgically led wound care team , followed by weeks of maggot therapy [ 2 ]. Tissue quality and wound size were assessed weekly. In a cohort of 63 patients with 92 pressure ulcers, followed for at least 8 weeks while receiving either standard wound care as prescribed by the hospital's wound care team , or maggot therapy two to hour cycles per week , maggot-treated wounds were debrided four times faster than control wounds 0.
Wayman and colleagues [ 20 ] randomized 12 venous stasis leg ulcer subjects to receive either maggot debridement therapy MDT or their standard of care hydrogel. All subjects received compression dressings, except during maggot debridement. Time to debridement differed significantly between the three groups The median time to debridement was 14 days with free-range larvae, 28 days with bagged larvae, and 72 days for the control arm. Healing results will be discussed later in this review. Schematic representation of a clinical trial proposed to demonstrate the wound healing effects of maggot therapy.
After a 2-week baseline data collection AB , nonhealing wounds are randomized either to receive the surgical and medical standard of care CD , standard confinement maggot therapy dressings HI , or containment bagged maggot dressings MN for debridement. Maggot-debrided wounds would then receive either standard care for wound closure IJ; NO or maggot therapy MDT maintenance debridement, KL or PQ to evaluate the presence of maggot-stimulated wound closure. To optimize enrollment and retention, subjects randomized to standard care may cross over to maggot therapy if there has been no significant improvement after 12—24 weeks of therapy.
Most other debridement studies are not as quantitative in their data collection and assessments. Markevich and colleagues presented data from their RCT of maggot therapy for neuropathic foot wounds at the Conference of the European Association for the Study of Diabetes [ 22 ]. Although never published as a full-length, peer-reviewed research paper, this abstract is often cited because it is the only RCT of MDT in diabetic foot ulcers. Wound dimensions and quality were then monitored every 3 days for 10 days.
In a retrospective case controlled study of lower extremity wounds in nonambulatory hospice patients in whom debridement was the goal, not wound healing [ 23 ], Armstrong and colleagues concluded that MDT was an effective debridement modality. Marineau and colleagues [ 24 ] published their case series of 23 complicated diabetic foot wounds most with osteomyelitis treated with MDT.
Wounds were evaluated on days 8, 15, and 30 [ 25 ]. Wound slough was significantly less in the maggot-treated arm by day 8 The authors concluded that, compared to surgical debridement, maggot therapy was more efficient and valuable for the first 2 weeks, though additional treatments provided no debridement benefit.
This two-week limit to maggot debridement efficacy deserves comment and consideration, because it contrasts with what has been reported with free range maggots. Unfortunately, very few studies have compared free range with bagged maggots, though such a study could be a valuable mechanism for evaluating the relative importance of the maggot's physical versus chemical activity.
Most, though not all, laboratory studies comparing free range versus contained maggots have suggested that maggots in direct contact with the wound are more effective, at least for debridement, than maggots separated from the wound by their containment dressings [ 9 , 26 ]. To date, only one clinical study was designed to compare the difference between these two methods of maggot therapy.
Maggot debridement therapy: the current perspectives
In this prospective clinical trial, Steenvoorde and colleagues [ 27 ] enrolled 64 patients with 69 chronic, necrotic wounds. Patients were treated with either free range or contained maggot debridement therapy, depending on maggot availability and clinician preference. The investigators monitored 8 specific outcome measures: 1 complete healing without any other intervention; 2 complete healing by secondary intervention e.
Dumville et al. As pointed out, this study was not powered to detect significant differences between these two groups, so it is not possible to determine whether or not the twofold difference in debridement time is real. The natural habitat of L. Therefore, it should be no surprise that this maggot would be well-protected from infection. Early on, scientists believed that ingestion was the primary method by which the maggots cleared the wounds of infection [ 8 , 28 ], and subsequent researchers demonstrated that highly effective killing does indeed occur in the gut [ 29 , 30 ].
Greenberg hypothesized that antimicrobial compounds might be produced in the gut by symbiotic microbes such as Proteus mirabilis , and, in , Erdmann and Khalil identified and isolated two antibacterial substances phenylacetic acid and phenylacetaldehyde from the P. They also pointed to the antimicrobial activity of ammonia-containing byproducts of the maggots' digestion of tissue proteins and the resulting alkalinized wound bed [ 1 , 34 , 35 ]. With advanced molecular and biochemical methods now at our disposal, many researchers over the past two decades have focused their attention on isolating antimicrobial proteins and other biochemicals produced by L.
Often, the isolated molecules were more active against gram positive bacteria than gram negatives, but sometimes this was merely a matter of dose and potency [ 42 ]. Antimicrobial activity has been seen even against highly antibiotic-resistant bacteria [ 40 , 43 ] and against the protozoan Leishmania parasite [ 44 , 45 ].
Kawabata et al. Even more antimicrobial molecules are likely to be discovered in the coming years. Numerous antimicrobial molecules have already been isolated in other blow flies, including the antibacterial peptide diptericin from Phormia terraenovae [ 50 ] and the antiviral alloferons from Calliphora vicina [ 51 ], the latter of which has already been commercialized.
Maggots also fight bacteria in their more resistant form: biofilm. Antibiofilm activity is valuable because biofilm is highly resistant to the penetration and successful activity of the human immune system and antibiotics. Biofilm is a particularly difficult problem in chronic wounds. One of the most powerful tools we have against biofilm is physically eroding it i. Many therapists prescribe brushing to rid a wound of biofilm.
It is reasonable to assume that the maggots are helping to rid a wound of biofilm simply by crawling over it with their rough bodies. What was particularly surprising, though, was the discovery that maggot ASE is capable of dissolving biofilm and inhibiting the growth of new biofilm [ 53 — 55 ]. This has been shown at least for Staphylococcus aureus and Pseudomonas aeruginosa biofilm. There should be no more doubt that maggots secrete and excrete potent antimicrobial compounds.
But what is the evidence that maggots bring about clinically relevant disinfection? Numerous case reports have purported wound disinfection following maggot therapy, but controlled clinical evidence of maggot-induced antimicrobial activity has been sparse, until recently. In a prospective clinical trial of maggot therapy for chronic leg ulcers, Contreras-Ruiz and colleagues [ 56 ] randomized 19 subjects to either maggot therapy or conventional debridement and compression therapy and found that maggot-treated wounds had significantly reduced bacterial counts compared to control wounds.
The maggot-treated group displayed more anxiety and wound odor during treatment, but no greater pain or other adverse events.
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In Tantawi et al. In an observational study by Bowling and colleagues [ 58 ], 13 sequentially enrolled stable diabetic patients with MRSA-colonized ulcers, not already receiving MRSA-specific antibiotics, were debrided with maggot therapy.
Complementary Medicine | Maggot Therapy
Semiquantitative cultures were taken at baseline and before each cycle of MDT. The mean duration of MDT was less than 3 weeks one treatment per week , and the authors noted that this was far less than the duration of conventional antibiotic treatment for MRSA. When reviewing their patients, Steenvoorde and Jukema [ 59 ] also found decreased colony counts of gram positive organisms following maggot therapy, but they found increased counts of gram negatives.
Their results may have resulted from the decreased competition by gram positive microbes. The study authors speculated that higher doses may be necessary for effective gram negative killing. Armstrong et al. As described earlier in this review, this study revealed significantly fewer days of antibiotics compared to controls, over a 6-month observation period, indicating that the patients were cleared of their infection faster and remained infection free longer.
Not all clinical studies of maggot-induced disinfection have demonstrated such positive results. But then, as the authors pointed out, there were so few patients with MRSA that the study was not adequately powered to see any likely difference. What's more, looking for significant population differences in colonizing bacteria may not truly be an appropriate endpoint if we are really more concerned with clinical infections. Evidence of maggot-induced tissue growth or wound healing now comes from both laboratory and clinical studies and also suggests both mechanical and biochemical pathways.
Among the early theories about maggot-induced wound healing were that the simple removal of debris and microbial killing [ 28 ] or the action of crawling over the clean wound bed [ 60 ] might be enough to stimulate wound healing. We now know that both of these hypotheses likely contribute to wound healing: physical and electrical stimulation of healthy cells can induce the release of host growth factors, and any meaningful reduction in debris and biofilm or microbial population likely decreases inflammation and promotes wound healing.
Some investigators believed that the alkalinity of maggot-treated wounds, along with the isolated allantoin and urea-containing compounds, was responsible for wound healing [ 61 ]. In fact, today, allantoin and urea are components of many cosmetics. With recent advances in cellular biology and chemistry, we now know that maggot ASE stimulates the proliferation of fibroblasts [ 62 ] and endothelial tissue unpublished data , increases angiogenesis [ 63 ], and enhances fibroblast migration over model wound surfaces [ 64 — 66 ].
Biopsies of maggot-treated wounds reveal profound angiogenesis [ 67 ]. Using remittance spectroscopy to evaluate patients before and after maggot therapy, Wollina and colleagues [ 68 ] found that vascular perfusion and tissue oxygenation surrounding the wound actually increased following maggot therapy. Zhang and colleagues [ 69 ] are currently seeing evidence that maggot extracts may even stimulate the growth of neural tissue.
Early clinical reports of maggot-induced wound healing were merely case studies or series; but beginning in the 's, controlled comparative trials of maggot therapy began to appear. These were small, due to a lack of funding and support; but they showed the promising results needed to propel maggot therapy into the scientific limelight and justified larger and more definitive studies. In a prospective study of spinal cord injury patients with chronic, nonhealing pressure ulcers, patients were followed for weeks while receiving standard wound care whatever modality was prescribed by the surgically led wound care team , followed by weeks of maggot therapy [ 2 ].
Tissue quality and wound size were assessed and photographed weekly. Debridement of necrotic tissue was achieved in just 10 days with maggot therapy. A cohort of 63 patients with 92 pressure ulcers was prospectively followed for at least 8 weeks while receiving either standard wound care as prescribed by the hospital's wound care team or maggot therapy two to hour cycles per week [ 18 ].
In patients with bilateral wounds, only one was treated with maggot therapy, and patients were allowed to select that one. Nevertheless, 4- and 8-week healing rates were significantly better for maggot-treated wounds than control wounds, as was the weekly decrease in surface area and the rate of granulation tissue growth over the base of the wound see Table 2.
The wound healing rate, based on studies by Gilman [ 69 ] and Margolis et al. Study details provided in text. The wound healing rate, based on studies by Gilman [ 70 ] and Margolis et al. Four and eight-week healing rates have repeatedly been shown to be accurate surrogates for wound healing in general, although they have not been accepted as substitutes for complete wound closure in clinical trials. But most patients were not followed more than 10 weeks, and this difference was not statistically significant.
In another cohort of 18 diabetic subjects with 20 nonhealing neuropathic and neuroischemic foot ulcers, six wounds were treated with conventional therapy, six with maggot therapy, and eight with conventional therapy first and then maggot therapy [ 19 ].
As in the pressure ulcer patients, 4- and 8-week healing rates were significantly better for maggot-treated wounds than control wounds, as was the weekly change in surface area and the rate of granulation tissue growth over the base of the wound Table 2. Repeated measures ANOVA indicated that treatment rendered was the only factor associated with these differences. In this study population, the probability of healing may have had more do to with the patients' underlying circulatory compromise, malnutrition, and poor physiologic health than with the treatments rendered.
Many in the wound care community looked with excitement at the study by Dumville et al.
This RCT demonstrated significantly faster debridement in the maggot therapy arms as already discussed , but did not demonstrate any significantly faster healing in those subjects. Several reasons may explain this, including the simple fact that the maggots may not expedite healing in any clinically meaningful way.
Alternatively, as the authors pointed out, their study may have been too small to demonstrate the difference, given that there were less than subjects in each of 3 arms. In this study, maggot therapy was stopped as soon as wounds were debrided treatment day number 15, on average, for the free range maggot therapy group and was never administered to those patients again, even if their wounds deteriorated over the subsequent 7 months that it took, on average, to heal [ 73 ].
Indeed, maggot-associated wound healing and antimicrobial activity is likely short-lived after the maggots are removed. Many clinicians intuitively feel that faster debridement brings faster wound healing. After all, the wound cannot heal if infected, necrotic tissue and debris are occupying the center of the wound. Yet, it has been difficult to find any large RCT that demonstrates this to be true [ 75 ]. Perhaps the problem has been that chronic wounds often reacquire infection or biofilm; and additional tissue may die, requiring redebridement.
If this paradigm is correct, it would explain why maggot therapy continued beyond the point of gross debridement has been associated with faster wound healing [ 2 , 18 , 19 , 22 ]. It may be true that no one single method of maintenance debridement is faster than another. But maggot therapy is one of the few highly effective methods of debridement which can safely and inexpensively be continued throughout the healing process, which may explain why it remains one of the methods of maintenance debridement best associated with faster wound healing.
Maggot secretions have recently been found to affect the activity of these cells in ways that decrease inflammation. While this can be thought of as a subset of actions which promote wound healing, they are separated out for the purpose of this discussion because these actions may also play important roles in disinfection, if not also debridement. Exposing unstimulated human neutrophils to crude L. But when opsonized zymosan stimulated neutrophils were exposed to high concentrations of the salivary gland extract, superoxide generation and MPO release were significantly reduced. The researchers concluded that medicinal maggots might aid in wound healing by decreasing the generation of proinflammatory factors in this way, while still maintaining normal phagocytosis or apoptosis.
Their findings of elevated cAMP and suppressed proinflammatory responses without a measurable decrease in antimicrobial activity led the authors to conclude that the larval secretions were moving the monocytes and neutrophils forward from the proinflammatory phase and into the angiogenic phase of wound healing [ 81 ]. Cazander and colleagues [ 82 ] recently discovered that maggot ASE reduced complement activation in healthy and immune-activated postoperative human sera by as much as From clinical and laboratory studies to date, it is clear that maggot therapy contributes significantly to wound care, both physically and biochemically.
Figure 2 represents our current understanding of the mechanisms by which maggot therapy affects wound healing.
This schema is a work-in-progress, intended to be modified as additional research adds to our understanding of the maggot-wound interaction. Schematic drawing of proven and postulated mechanisms by which medicinal maggots promote wound healing. Many questions remain about wound healing, in general, and maggot therapy in particular. Several of these questions might be answered by a single well-designed clinical study. This review was undertaken to help design the next study or at least offer an initial proposal for what that study might look like.
Evidence of maggots' debridement efficacy is irrefutable. The results of maggot therapy have been impressive in treating diabetic foot ulcers, slow-healing wounds resulting from circulatory problems, and pressure sores in bed-bound patients: over a majority of these wounds - many of them in existence for years - heal without pain or side effects. In addition to detailed descriptions of the clinical problems for which maggots can be used, there are case studies and questions and answers from medical practice.
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