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Clinical Practice Keywords therapy/ care/ Review This article has been Wound care double-blind peer reviewed In this article... ● Evidence supporting maggot therapy in wound care ● Indications for use and how the process works ● Patient perception of the treatment

The principles of maggot therapy and its role in contemporary wound care

Key points Author Yamni Nigam is professor (anatomy and physiology), College of Human and Maggot therapy has Health Sciences, Swansea University. been available on NHS prescription Abstract Maggot therapy is becoming increasingly established as an option for the since 2004 debridement and treatment of sloughy, necrotic . Although used tentatively NT SELF- over the previous few decades, it became more widespread following its availability ASSESSMENT are on NHS prescription in 2004. Since then, the scientific and clinical evidence for the

Test your clinically effective efficacy of maggot therapy has mounted considerably, and it has been shown to be knowledge. for the debridement effective, not only for wound debridement but also in reducing the bacterial burden After reading this of sloughy, necrotic of a wound and accelerating wound healing. This article reviews current evidence, article go to chronic wounds and discusses the clinical indications for use, and the rearing and clinical application nursingtimes.net/ of maggots, as well as patient and health provider perceptions of maggot therapy. NTSAMaggots If you score 80% Secondary benefits or more, you will of maggot therapy Citation Nigam Y (2021) The principles of maggot therapy and its role in receive a certificate include reduction of contemporary wound care. Nursing Times [online]; 117: 9, 39-44. that you can use wound bacterial as revalidation evidence. load and an acceleration of ll health professionals are History of maggot therapy wound healing acutely aware of the mounting Knowledge of the improvement in the burden and cost of wound wound state as a consequence of maggot Maggots can be Amanagement. The develop- infestation dates back centuries, but docu- applied clinically ment of non-healing wounds is often an mented evidence is mainly through mili- directly to the unfortunate and inevitable consequence of tary records. It was Dr William Baer who wound or in bagged the presence of certain chronic conditions, wrote about the positive effects and out- form and are usually such as chronic obstructive pulmonary comes of unintentional maggot infesta- left on a wound for disease, cardiovascular disease and dia- tion on open battlefield wounds inflicted four days before betes. The underlying pathology of on soldiers in the First World War (Man- removal certain conditions, including diabetes, ring and Calhoun, 2011). After the war, in makes it highly probable that the resulting his role as professor of orthopaedic sur- For some patients, wounds may become necrotic, infected gery at John Hopkins School of Medicine, there may be and indolent. in the US, he initiated the use of sterile associated side- Such wounds can cause severe discom- maggots as a reputable method of wound effects of bleeding fort and distress to patients. They are often therapy. His pioneering work meant the and pain, and nurses notoriously difficult to treat and tend to use of maggot therapy began to flourish in are advised to harbour antibiotic-resistant strains of bac- the 1930s and early 1940s, and was widely monitor such teria or bacterial biofilm, which can drasti- used in hospitals in the US and Canada. patients closely cally impede healing. Effective wound By the mid-1940s, following the first debridement and a reduction in bacterial clinical use of penicillin, the industrial burden are an essential part of wound man- antibiotic era commenced in earnest; this agement and, in the search for more effec- ended the use of maggots as the steady and tive clinical management, numerous new consistent overuse of antibiotics pro- treatment modalities have gressed. Over time, several species and been introduced over the past two decades. strains of bacteria emerged that were

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Fig 1. Life cycle of the medicinal maggot, Lucilia sericata

slowly becoming more and more resistant For clinical use, disinfected eggs hatch ● Disinfection (reducing bacterial to almost any antibiotic therapy. We now under sterile conditions. Upon emerging, infection and biofilm burden); face a global public-health crisis, with a and just prior to being packaged for ● Helping to accelerate wound healing. worldwide rise in patients with antibiotic- delivery, hungry first-stage (L1) larvae are Advances in our understanding of resistant wound infections (Alfadli et al, fed once on a high-protein cereal-based maggot therapy and its treatment stem 2018). Consequently, maggot therapy is diet, so they can survive for up to 24 hours from clinical reports and the results of lab- being revisited and advocated for debride- in transit. Once placed on a wound, the oratory investigations in these three areas. ment, disinfection and the ultimate larvae can feed and grow to their final third healing of necrotic tissue. stage (L3); they usually remain on the Wound debridement Currently, there are several specialist wound for four days before being removed. The primary goal of maggot therapy is to laboratories worldwide that are licensed to Used larvae are treated as infectious clin- carry out the process of wound debride- aseptically produce clinical-grade mag- ical waste. ment. The ability of L sericata larvae to gots. ‘Medicinal maggots’ can be ordered If a wound is assessed as suitable for achieve speedy and effective debridement through these companies and supplied treatment with maggots, the therapy can is attributed to their highly necrophagous directly to hospitals and clinical centres progress under clinical guidance. Suitable nature (ability to rapidly consume and for the treatment of all sorts of wounds, wounds include any type of chronic wound ingest dead tissue). including leg ulcers, pressure ulcers, and that has moist slough or necrotic tissue on diabetic and necrotic ulcers, as well as its floor (Naik and Harding, 2017). The Clinical evidence base infected surgical wounds, burns and application of maggots requires appropri- The efficacy of maggot therapy in wound trauma injuries. ately trained clinicians to place a number debridement is proven. Since its resur- of tiny larvae onto a wound, either as free- gence in the US and UK in the 1990s, clin- What is maggot therapy? range or bagged maggots. ical studies have assessed the success of Maggot therapy, also known as larval Over the next few days, the larvae not larval therapy compared with conven- therapy, is one option available for treating only clear away the dead, sloughy or tional treatment methods for debriding chronic, infected, necrotic and sloughy necrotic tissue in the wound, but also chronic wounds (Dumville et al, 2009a; wounds. The maggots used are special eliminate infection. Once the larvae are Opletalová et al, 2012). clinical-grade, aseptically reared larvae of removed, the wound is reassessed for fur- Sun et al’s (2014) systematic review of the common greenbottle (Lucilia seri- ther therapy. Maggots are now thought to clinical studies from 2000-2014 incorpo- cata). Fig 1 outlines the life cycle of this benefit wounds in three ways: rated 12 comparative studies, including six

FRANCES THORNTON, SWANSEA UNIVERSITY SWANSEA THORNTON, FRANCES medicinal maggot. ● Debridement (getting rid of dead tissue); randomised controlled trials. Based on an

Nursing Times [online] September 2021 / Vol 117 Issue 9 40 www.nursingtimes.net Copyright EMAP Publishing 2021 This article is not for distribution except for journal club use Clinical Practice For more articles on tissue viability, go to Review nursingtimes.net/tissue-viability analysis of these 12 studies, the authors secretions being caused by a complex mix also received maggot therapy. A swab cul- concluded that larval therapy was more of enzymes. ture was collected before and after each effective and more efficient in the debride- maggot application and analysed for the ment of chronic ulcers compared with Bacterial burden presence of Staphylococcus aureus and Pseu- conventional treatments (Sun et al, 2014). While debridement is often the primary domonas aeruginosa. In the maggot treat- As an example, one randomised controlled aim in the clinical use of maggot therapy, ment group, cases of S aureus infection trial compared the clinical effectiveness of evidence is accumulating that the therapy reduced after 48 hours of treatment, with a a larval therapy dressing with a standard contributes to other aspects of wound further reduction after a second applica- debridement technique (hydrogel) on treatment (Pritchard and Nigam, 2013). In tion of larvae. Cases of P aeruginosa reduced venous or mixed arterial/venous leg ulcers. particular, larvae have been shown to have too, but only after a second maggot treat- The analysis revealed that 96.9% of ulcers a significant antibacterial effect on the ment. In the control group, which had no were debrided in the larvae arm compared wound surface, not only by the removal of maggot therapy, no reduction in cases of with only 34.4% from the hydrogel arm infected tissue, but also through the anti- either S aureus or P aeruginosa was observed (Mudge et al, 2014). microbial action of their secretions (Vala- (Malekian et al, 2019). Sun et al (2014) also noted other benefits chová et al, 2013; Bexfield et al, 2008). The formation of bacterial biofilm on a of associated larval therapy that had been wound can also pose a serious problem to identified in the studies – namely, a wound healing. Biofilms are widely recog- quicker healing rate of chronic wounds 96.9% nised to be highly resistant to antibiotics QUICK Ulcers reported in one (Sherman et al, 2003), a longer antibiotic- FACT study as debrided using and host immunity. Maggots, however, free time period and decreased amputa- maggot therapy have been shown to be able to tackle bac- tion risk (Armstrong et al, 2005). In addi- teria in this more-resistant form, and var- tion, an increasing number of reports ious studies have determined the positive show maggot therapy success from con- The explanation for the observed anti- effect of maggot secretions, both on the trolled, retrospective studies and clinical microbial activity of maggot secretions is ability of bacteria to form biofilm commu- case studies (Sherman, 2014). that it would be vital for any organism nities and as an agent to disrupt existing inhabiting a heavily contaminated envi- bacterial biofilms (Harris et al, 2013). Scientific evidence base ronment. In their natural environment, Wound debridement is the best understood blowfly larvae are exposed to decaying car- Maggot therapy and wound aspect of maggot therapy. It is now known rion and masses of heavily contaminated healing that maggots produce a combination of materials so need to be able to survive this. For years, anecdotal reports from wound proteolytic and other digestive enzymes With regards to chronic wounds, bacte- clinicians have suggested wounds treated that are released externally in their secre- rial infection can both compromise and with maggots had better outcomes and tions and get distributed over the wound as delay wound healing (Roy et al, 2020). Pro- healed faster compared with those not the maggot crawls around (Thomas et al, gression of healing is said to be dependent treated with maggots. It is only recently, 2002). Maggot movement over the surface on both bacterial count and the microbial however, that these healing effects have tissue facilitates the penetration of these species present, so managing the bacterial been scientifically and clinically investi- enzymes into the necrotic tissue, causing it levels of the wound site is vital for healing gated. There is now growing evidence sup- to break down and liquefy into a nutrient- (Negut et al, 2018). Recently, there has been porting maggot-induced acceleration of rich fluid that the larvae subsequently particular interest in understanding and healing. This includes the ability of mag- ingest. Two key enzymes, trypsin and chy- identifying the therapeutic antimicrobial gots to: motrypsin, have been identified as being properties of maggot secretions, the main ● Promote (growth of new produced by medicinal maggots (Cham- drive for this being the use of larvae as a blood vessels); bers et al, 2003), with studies suggesting source of novel antibiotics and anti-infec- ● Improve oxygen perfusion to wound that key to their effectiveness is the ability tives (Pöppel et al, 2015). sites; of these enzymes to withstand endogenous Most of the compelling discoveries on ● Enhance the migration of vital cells wound inhibitors that would normally the nature of the therapeutic antimicro- (fibroblasts) to the wound bed (Nigam degrade and destroy other enzymes (Tel- bial effects have come from scientific labo- and Morgan, 2016). ford et al, 2011 ). ratory findings using externalised maggot A recent review of clinical studies from Larval chymotrypsin has been shown to secretions. Several studies – for example, 2000-2015 by Siribumrungwong et al (2018) effectively degrade macromolecules pre- those by Jaklic et al (2008) and Daeschlein compared time to heal in five separate sent in venous leg slough and large et al (2007) – have served to reaffirm the studies; the authors reported that time to molecules, such as fibrin and fibrinogen, notion that maggot secretions are effective heal for maggot-treated wounds was that, if left on the wound, could act as key in destroying a broad range of gram- shorter (3.1 weeks) than conventionally substrate sites for the accumulation and positive and gram-negative bacteria. treated wounds. attachment of wound bacterial biofilm Clinical evidence from a recent ran- (Pritchard and Brown, 2015). More recently, domised controlled trial of 50 patients Indications and clinical use a maggot enzyme known as ‘Jonahm’ was with diabetic foot ulcers by Malekian et al Currently, maggot therapy is a treatment found to be active in digesting certain (2019) also supports this theory. Patients of last resort, usually used only when other extracellular matrix components normally were randomly selected for two groups: a conventional therapies fail or when non- present in the chronic wound environ- control group treated conventionally with surgical debridement is being considered. ment (Pöppel et al, 2016). This points surgical debridement, antibiotic therapy The National Institute of Health and Care towards the debridement effect of larval and offloading; and a treatment group that Excellence (2014) suggests considering

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maggot therapy in chronic pressure ulcers Fig 2. Application of free-range maggots onto a wound if debridement is needed, but sharp debridement is contraindicated. Maggots have been available on NHS prescription since 2004. In the US, they are classed as medical devices, making them the first live organism marketed in the US for medical purposes, with treatment being reimburs- able by medical insurers. Most moist wounds that possess a degree of devitalised, sloughy tissue are suitable for maggot therapy, but published reports have shown successful outcomes when using it for other clinical manifesta- tions (Borst et al, 2014) and conditions including haematomas (Rafter, 2012).

Rearing of clinical-grade maggots Even though the efficacy of larval therapy is well established, its widespread adop- tion is limited by several issues, including practical problems associated with the use of living organisms. These include a short “Recently, there has been Bleeding shelf life, the need for an advanced logistic particular interest in Maggot therapy should be used cautiously network to allow for express delivery, and and under close supervision near exposed training to ensure that maggot dressings understanding and blood vessels, organs or wounds in body are applied and maintained correctly. identifying the therapeutic cavities. As maggots are also known to While clinical grade maggot-rearing facili- antimicrobial properties produce an anticoagulant (Van der Plas et ties have been established all over the al, 2014), bleeding complications have world, in the UK there is only one company of maggot secretions” been encountered, so observation of the specialising in the sterile production of therapy is required, particularly for medicinal maggots. Based in South Wales, The bag containing the maggots patients who are on anticoagulant therapy it is the sole provider of larvae to the UK (BioBag) is placed easily on the wound. or have bleeding tendencies. and several other countries in Europe. Some netting is placed over the bag and taped to an adhesive on the wound edges. Pain Application and management Wet gauze and a light bandage are wrapped The skin around a wound may be sensitive Maggot therapy is undertaken under clin- over the net. Maggot bags come in varying to motion, pressure and the liquefied ical control and direction. Currently, there sizes to match different wound sizes. The necrotic drainage associated with maggot are two methods of larval application: free larvae remain sealed inside the bag secretions. The use of protective creams range (Fig 2) and bagged (Fig 3). throughout the whole treatment period. It can prevent this last from making contact is the necrophagous nature of larvae that with healthy periwound skin. The sensa- Free-range maggots has enabled the development of the maggot tion of maggot movement becomes more Free-range maggots are applied directly bag; as maggots have no teeth, they release apparent after 24 hours of therapy, due to onto the wound. They arrive in a sterile digestive enzymes through the netting, the increased larval size (Jordan et al, 2018). tube and, with the help of a small pod of turning the dead and devitalised tissue into The associated side-effect of pain is sterile saline, can be gently poured directly a sort of ‘soup’ they can then ingest. reported in approximately 5-30% of onto the wound. The wound is then well BioBags or free-range larvae remain on patients and ranges from localised tissue sealed with a breathable dressing. Essen- the wound for three to seven days per discomfort to significant pain, although tially the maggots are free to roam within application. During this time, the tiny L1 most of these patients report baseline pain the confines of the wound bed and are able larvae become larger L3 larvae (Fig 3b), and before maggot therapy administration to reach all corners of the enclosed wound any maggot dressings should then be (Jordan et al, 2018). Most complaints of space. The use of free-range larvae domi- removed and treated as contaminated pain can be treated with analgesics and nated clinical use for decades, before the waste. The number of fresh maggot some clinicians suggest that pre-emptive development of the maggot bag. therapy applications required for com- analgesia may be helpful, particularly plete wound debridement depends on the when treating patients with a known pre- Bagged maggots type of wound, but usually ranges from disposition for pain exacerbations. Bagged maggots became available in the UK one to three treatments. in 2002. Larvae are enclosed between two Perception of maggots layers of thin polyvinyl netting; a small cube Adverse effects Anecdotal reports suggest the potential of spacer material is inserted to prevent bag There may be side-effects of maggot benefits of maggot therapy are overshad- collapse, and the bag edges are heat sealed therapy in some patients, including owed by the ‘yuck factor’ (an inherently

ALAMY (Fig 3a) ready to be sent out for delivery. bleeding and pain. negative, cultural dislike of maggots). A

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Fig 3. Sealed maggot BioBag 2009b). For patients with a chronic wound, the offer of maggot therapy is often their final hope, but Steenvoorde et al (2005) found a high number of patients are sub- ject to adverse social interactions while undertaking it. This consisted mainly of other people finding the idea of maggot therapy “eerie”. The authors suggested: ● Public acceptance is important to reduce worry and keep patients’ adverse feelings to a minimum; ● There is a need to decrease the general prejudice towards maggot therapy. To help with this, in 2016 at Swansea University, we set up a worldwide public engagement campaign, Love a Maggot! (loveamaggot.com), which addresses the perception of the general public towards maggot therapy.

Cost The cost of an initial maggot treatment will vary depending on how many maggots 3a. BioBag pre-application are needed or the size of the BioBag required. The smallest maggot bag costs approximately £250.00, and this is a cru- cial factor when considering whether to embark on this therapy or not. However, reports suggest that using maggots is, in fact, a very cost-effective wound treatment (Bennett et al, 2013; Wayman et al, 2000).

Clinician acceptance Anxiety about the use of maggots is also common among health providers (Jones et al, 2011; Dumville et al, 2009b). In the UK, wound care is predominantly nurse led. Sherman (2009) showed that health pro- fessionals and administrators are much more likely to be repulsed by the thought of maggot dressings than the patient with the chronic wound. We conducted a UK survey through Nursing Times that suggested not all nurses are keen on maggot therapy (Stephenson, 3b. Maggot bag after three days’ application 2017). A paper on the study of which the survey was a part is still in submission, but the results showed that wound specialist study undertaken by Nigam et al (in press), Influential factors for this negativity nurses rated maggot therapy highly, and surveyed and evaluated public perceptions included: were less squeamish and felt less revulsion and understanding, along with the accept- ● A lack of information and under- than non-wound specialist nurses. This ance, of maggot therapy. This revealed standing about the therapy; suggests a need for better education and some worries and fears, with only 36% of ● Associated fears about maggots. training for all nurses as, if general team/ survey participants agreeing that they ward nurses are unwilling to help and sup- would accept maggot therapy as a first Patient views port the ongoing therapy, it may inhibit choice for a hypothetical painful wound; Some patients may express anxiety when the ability of specialist nurses to offer this this proportion did, however, increase maggot therapy is suggested and applied, treatment to patients who might benefit with wound severity. but patients are generally considered very from it. The most predominant concerns about accepting, as they have often suffered with maggot therapy were: a non-healing stagnant wound for many The future of maggot therapy ● Sensation; months or years and are quite desperate During the last decade, thousands of

3A COURTESY BIOMONDE, 3B COURTESY JULIE EVANS, SWANSEA BAY UNIVERSITY HEALTH BOARD HEALTH UNIVERSITY BAY SWANSEA JULIE EVANS, 3B COURTESY BIOMONDE, 3A COURTESY ● A feeling of disgust. for some improvement (Dumville et al, patients all over the world have had their

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Box 1. Negut I et al (2018) Treatment strategies for Clinical case study infected wounds. Molecules; 23: 9, 2392. Nigam Y et al (in press) An exploration of public A 58-year-old woman, who was fit and well but had a medical history of diabetes and perceptions and attitudes towards maggot high blood pressure, presented to the emergency department with acute abdominal therapy. Journal of Wound Care. pain and was diagnosed with a colon abscess. She was admitted in January for com- Nigam Y, Morgan C (2016) Does maggot therapy puted tomography image-guided drainage, which failed several times and, in February, promote wound healing? The clinical and cellular evidence. Journal of the European Academy of underwent surgical drainage through a midline incision. Two days after surgery, the Dermatology and Venereology; 30: 5, 776–782. wound dehisced (burst open), so tension sutures were placed intraoperatively and Opletalová K et al (2012) Maggot therapy for then removed three weeks later. Unfortunately, the wound dehisced again shortly after- wound debridement: a randomized multicenter trial. Archives of Dermatology; 148: 4, 432-438. wards and the patient was referred to the tissue viability service. Sharp debridement Pöppel A-K et al (2016) A Jonah-like chymotrypsin was contraindicated due to sutures being visible. from the therapeutic maggot Lucilia sericata plays The wound was thick, with tenacious slough and the tissue viability nurse chose to a role in wound debridement and coagulation. Biochemistry and Molecular Biology; 70: treat with maggot therapy to avoid the need for invasive surgery. The wound was 138–147. treated with one BB300 BioBag dressing, with three applications of larval therapy used Pöppel A-K et al (2015) Antimicrobial peptides over 14 days. The patient was aware that the larvae were present on her wound but did expressed in medicinal maggots of the blow fly Lucilia sericata show combinatorial activity against not experience any issues from pain or discomfort. bacteria. Antimicrobial Agents and Chemotherapy; After three rounds of treatment, the wound bed was left with 100% granulation 59: 5, 2508–2514. tissue. The wound had progressed from complete slough coverage to healthy granula- Pritchard DI, Brown AP (2015) Degradation of MSCRAMM target macromolecules in VLU slough tion tissue and wound margin contraction. Following the successful debridement of by Lucilia sericata chymotrypsin 1 (ISP) persists in the wound, negative pressure wound therapy was started to maintain the momentum the presence of tissue gelatinase activity. of wound progression and promote wound closure. International Wound Journal; 12: 4, 414-421. In April the patient was discharged. The wound continued to close and was well Pritchard DI, Nigam Y (2013) Maximising the secondary beneficial effects of larval debridement healed by the end of October. therapy. Journal of Wound Care; 22: 11, 610–616. Rafter L (2012) Debridement of a traumatic haematoma using larval therapy. Wounds UK; 8: 1, 81–88. wounds successfully treated with mag- Chambers L et al (2003) Degradation of extracellular Roy S et al (2020) Staphylococcus aureus biofilm gots, as illustrated in the case study (Box 1). matrix components by defined proteinases from the infection compromises wound healing by causing Maggot therapy is recognised by many cli- greenbottle larva Lucilia sericata used for the clinical deficiencies in collagen. Annals debridement of non-healing wounds. British Journal of Surgery; 271: 6, 1174-1185. nicians as an important treatment in its of Dermatology; 148:1, 14–23. 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