Presurgical Maggot Debridement of Soft Tissue Wounds Is Associated with Decreased Rates of Postoperative Infection
- 1Department of Pathology, University of California, Irvine
- 2BioTherapeutics, Education, and Research Foundation, Irvine
- 3Veterans Affairs Long Beach Healthcare System, Long Beach, California
- Reprints or correspondence: Dr. Ronald A. Sherman, BioTherapeutics, Education, and Research Foundation, 36 Urey Ct., Irvine, CA 92612 (RSherman{at}BTERFoundation.org).
Abstract
Postoperative complications were assessed for all patients who received presurgical maggot debridement therapy (MDT) and for a matched group of patients who did not. Ten wounds were debrided by maggots within 1–17 days prior to surgical closure. Debridement was effective in all cases, and there were no postoperative wound infections. Six (32%) of 19 wounds not treated presurgically with MDT developed postoperative wound infections (95% CI, 10%–54%; P < .05). Presurgical MDT was effective in preparing the wound bed for surgical closure, without increased risk of postsurgical wound infection.
For decades, maggot therapy has been recognized as an effective method of wound debridement [1]. Maggots used for medicinal purposes secrete digestive enzymes that selectively dissolve necrotic tissue [2], disinfect the wound [3–5], and stimulate wound healing [6, 7].
Seventy years ago, maggot debridement therapy (MDT) was routinely used in hundreds of hospitals around the world for the treatment of bone and soft-tissue infections [8], but, by the 1950s, MDT was used only sporadically, as salvage therapy. The 21st century is witnessing a revival in the use and popularity of MDT [9–14]. However, the optimal role for MDT has not been defined, and serious questions remain concerning its safety.
To evaluate the safety and utility of maggot therapy for debridement prior to wound closure, we retrospectively evaluated all such treatments performed at our facility (Veterans Affairs Long Beach Healthcare System) between 1990 and 1995. Specifically, we intended to address claims that presurgical MDT would increase the rate of postoperative wound infections.
Methods. Between 1990 and 1995, a total of 143 patients were followed by our institution as candidates for MDT. Most patients with osteomyelitis and patients with rapidly advancing infections or patients in need of urgent debridement were not considered to be candidates; they were referred for surgical debridement. Candidates for MDT were followed every 1–2 weeks, whether they received maggot debridement or the conventional therapy prescribed by their primary wound-care team. Patients receiving MDT and candidates for MDT were selected for the present analysis if their wounds were surgically closed, grafted, or flapped. Written, informed consent was obtained prior to surgical or maggot therapy, and institutional review board approval was obtained before the present study was conducted.
MDT was administered at the hospital by use of disinfected larvae of Phaenicia (Lucilia) sericata [15, 16]. Maggot dressings were left in place for cycles of 48–72 h; 2 cycles were applied each week. With the exception of amputations, all surgical and postsurgical care was performed by the same surgical team. “Presurgical MDT” was defined as MDT applied to the wound in question within the 3 weeks prior to surgical closure.
The primary outcome measurement was the occurrence of clinically significant postoperative wound infection. Patient demographics, indications for surgery, underlying medical conditions, American Society of Anesthesiology (ASA) scores [17], type of surgery, and duration of surgery were recorded. Nonparametric data were evaluated using Pearson χ2 analyses and Fisher's exact test. Ordinal data, such as laboratory test results, were compared using independent sample Student's t tests. All P values were 2-tailed; mean values were considered to be significantly different only when the likelihood of a type I error was ⩽5%.
Results. Twenty-nine wounds in 25 patients were closed intraoperatively (table 1). Ten of these wounds received preclosure MDT. There were no significant differences in patient age, underlying medical illnesses, wound location, type of surgery, duration of surgery, or ASA scores between patients who received presurgical MDT and patients who did not. Wounds debrided presurgically with MDT tended to be older (duration, 38 weeks vs. 16 weeks), but this trend did not reach statistical significance (P = .06). The average delay between the end of presurgical MDT and the start of surgery was 5.7 days (range, 1–17 days), with a median delay of 4.5 days. The number of MDT cycles ranged from 1 to 29, with an average of 9.7 cycles and a median of 5.5 cycles.
Table 1
Characteristics of 29 wounds that were closed surgically, with or without presurgical maggot debridement therapy (MDT), as well as characteristics of and laboratory findings for the 25 patients who had the wounds.
None of the 10 wounds treated presurgically with MDT became infected (table 2). Six (32%) of the 19 wounds not treated presurgically with MDT developed postoperative infections (95% CI, 10%–54%; P < .05), with subsequent dehiscence. Even after the exclusion of amputations (given that amputation sites were distant from the wound beds on which debridements were performed, and given that none of the 5 amputations were complicated by clinical wound infections), the rate of postoperative wound infection in the absence of antecedent MDT was still higher (38%; 95% CI, 13%–62%), compared with a 0% rate of postoperative wound infection for wounds presurgically debrided with medical-grade maggots (P = .05).
Table 2
Analysis of data for patients with wounds that were or were not treated with presurgical maggot debridement therapy (MDT).
Presurgical MDT was the only single factor associated with the absence of postoperative wound infections. Neither ASA scores nor duration of surgery, nor the combination of these 2 factors, adequately predicted the development of postsurgical infections. The mean duration of surgery for dehisced, infected wounds was 168 min; the mean duration of surgery for wounds that were not dehisced was 167 min. Correlation of outcomes with wound cultures and antimicrobial therapies was not possible because most of that data, which was >10 years old, was destroyed or lost.
Three patients in the control group had received MDT at 21–95 days prior to surgery, and, therefore, they were not considered to have received presurgical MDT. The rate of infection for these patients was similar to that for the other patients in the control group: 1 patient, who received a split-thickness skin graft 21 days after finishing MDT, developed a postoperative wound infection; the other 2 patients, who had limbs amputated 21 and 95 days following the cessation of MDT, respectively, had no postoperative infections. Although these findings are similar to the overall postoperative infection rate for the control group, this subgroup is too small for us to draw any statistically valid comparisons with the control group or with the presurgical MDT group.
The most common adverse event associated with maggot debridement was pain at the wound site, beginning when the larvae reached ∼30 h of age. Pain was reported by 2 (17%) of the 12 patients who were treated with maggots, both of whom had earlier experienced wound pain with sharp debridement and dressing changes. Pain caused by MDT was controlled with analgesics; when pain was not adequately controlled, the maggot dressings were removed early, and the pain ceased immediately.
Discussion. During the early years of MDT, the use of “nonsterile” (nondisinfected) larvae was associated with at least 1 case of erysipelas [18] and 2 cases of tetanus [1]. Although there is no proof that the maggots were the cause of these wound infections, it was decided >70 years ago that maggots used for medicinal purposes should be disinfected. Disinfection of larvae used for medicinal purposes has been the standard practice ever since. A recent cluster of cases of bacteremia associated with the use of contaminated larvae emphasizes the importance of this standard [19].
Some health care providers and administrators express concern that disinfected fly larvae may introduce or worsen existing wound infections. The present study explored the probability of MDT-associated wound infections by examining the frequency of postoperative wound infections among patients receiving MDT. At our institution, wounds debrided preoperatively by maggots were less likely to develop postoperative wound infections than were wounds closed without presurgical MDT (P = .02). Amputation sites would not be expected to develop postoperative wound infections as a result of ulcer colonization, and there were slightly more amputations performed in the group that was treated with MDT (not statistically significant). However, when amputations were excluded from analysis, still there remained a significant decrease in the rate of postoperative wound infections seen among subjects who were treated with MDT. Univariate and multivariate analyses failed to demonstrate that any factors were significantly associated with postoperative wound infections, except the lack of presurgical MDT. Postoperative wound infections were not even associated with ASA scores or with duration of surgery, which are both known to be risk factors for postoperative wound infections [20, 21].
The reason for this reduced infection rate is not clear, but it may be related to the maggots' ability to disinfect wounds. Blow fly larvae kill bacteria in their guts [4, 22, 23], and their digestive secretions, elaborated into the wound bed, also are antibacterial [24–26]. However, because the antimicrobial peptides that have been characterized thus far are very short-lived, perhaps the decreased postoperative infection rate was not due to the perioperative presence of maggot-secreted antimicrobials but, rather, to the preoperative antimicrobial action that eliminated some critical number or species of organisms that had not yet repopulated prior to the time of surgery.
Another factor that may have contributed to the lower postoperative infection rate is the capability of the maggot to stimulate healing. Epithelial growth factors [6] and cytokines [27] have been identified in blow fly maggot secretions, and tissue oxygenation is measurably increased during MDT [28].
Methodologic problems are unlikely to be responsible for the decreased infection rate seen for the wounds treated with MDT. The operative and postoperative staff and care provided were similar both for wounds treated with MDT and for wounds not treated with MDT. The infection rate in the control group was consistent with historical rates at our hospital.
Risks and benefits are best quantified by conducting prospective clinical trials. Unfortunately, only 2 prospective clinical trials of MDT have been completed [29, 30], and they were too small to allow assessment of uncommon risks, such as the occurrence of postoperative wound infections. Until large clinical trials can be performed, the present retrospective analysis can, at least, reassure us that the risk of postoperative wound infection among patients treated with MDT is very low, if not lower than that seen among patients with wounds not treated with MDT. Of course, even disinfected maggots will pick up microorganisms in the wound bed and spread them about the wound, possibly introducing them into the bloodstream during debridement. Therefore, seriously infected wounds may need peri-MDT “prophylactic” antibiotic coverage to prevent bacteremia or cellulitis [31].
Acknowledgments
Financial support. The costs of maggot debridement were supported by grants from the Spinal Cord Research Foundation of the Paralyzed Veterans of America, the California Paralyzed Veterans of America, and the Andrus Foundation of the American Association of Retired Persons.
Conflict of interest. R.A.S.'s laboratory provides medical-grade maggots to physicians and surgeons in North America for a nominal fee; that fee is waived (underwritten by donations) for patients without insurance or ability to pay. R.A.S. sits on the Board of Directors of the BioTherapeutics, Education, and Research (BTER) Foundation, a not-for-profit charity that develops educational programs involving maggot and other biotherapies and that also raises money to cover the costs of treatment for uninsured patients. None of the patients in the present study were treated using BTER Foundation funds. In addition, R.A.S. is on the speakers' bureau for Abbott, Boehringer Ingelheim Pharmaceuticals, GlaxoSmithKline, and Gilead, none of which are likely to benefit from the publication of the present study. K.J.S.: No conflict.
- Received February 13, 2004.
- Accepted May 11, 2004.
- © 2004 by the Infectious Diseases Society of America
References
This Article
- AbstractFree
- » Full Text (HTML)Free
- Full Text (PDF)Free
Classifications
Services
Citing Articles
Google Scholar
PubMed
Related Content
Share
- Email this article
-
CiteULike
Connotea
Delicious
Facebook
Google+
Mendeley
Twitter
Published on behalf of
IDSA Members: For your free access to this journal, log in via the IDSA members area.
The Journal
Impact Factor: 8.186
5-Yr impact factor: 7.898
For The Media
For Authors
- Services for authors
- Self-archiving Policy
- IDSA Conflict of Interest policy
- Instructions for Authors
- ICMJE Form
- Submit Now!
Open access options for authors visit Oxford Open
This journal enables compliance with the NIH Public Access Policy
Corporate Services
Alerting Services
Related IDSA Publications
