Factors influencing the use of Maggot Debridement Therapy in the Nursing management of the Diabetic Foot

Abstract

Aims: This paper seeks to explore the factors that influence the use of maggot debridement therapy in the nursing management of the diabetic foot. It will examine literature relating to the beneficial attributes of the maggot and the advantages of its use. The paper will consider the perceptions of patients and health professionals regarding the therapy and also assess the barriers for its use and investigate the lack of credible evidential material available to professionals, which may hinder the therapy being used within the hospital environment and the community setting.

Background: Maggot debridement therapy has been used on wounds for hundreds of years but has come under intense scrutiny over the last 10 years. It is a method of debridement that uses the larvae of the common green bottle fly to remove necrotic and devitalised tissue from chronic ulcerated limb wounds. Maggots have excretions and secretions that cause various physiological changes within wounds that assist in faster debridement. The use of the therapy has other beneficial properties including its ability to disinfect, cleanse, reduce inflammation and repair difficult wounds.

Method: This dissertation took the form of a literature review and as such examined literature available between and 2010 and 2014. A systematic literature search was conducted using electronic databases including Cochrane, Cinahl, NICE, One Search, Pubmed, Wiley Online, British Nursing Index, Embase, NHS evidence and Google Scholar with inclusions in place. From these searches twenty four pieces of literature were identified and subsequently critiqued and appraised. Two themes were established from the appraisal and from these themes a synthesised document was produced.

Results: Evidence has shown that maggot debridement therapy does debride more quickly than conventional therapies. It has also been established that this debridement technique does not remove healthy tissue. However, this may be the case with surgical debridement. The review has also identified that there is substantial evidence supporting the fact that pain is a side effect of the therapy that needs to be addressed early on. Although there is generally a negative perception of maggots it has been found that with careful handling, good communication and education patients are willing to try the therapy.

Conclusions: Maggot therapy is an effective tool in the debridement of necrotic foot wounds but due to the lack of rigorous random controlled trials available, there remains a lack of evidence that supports its use. It is widely suggested that maggot debridement therapy will one day be set amongst the conventional debridement therapies and not just being used as a last resort treatment.

Introduction

maggot1This work explores the question, “Factors influencing the use of maggot debridement therapy in the nursing management of the diabetic foot?”

A chronic wound is one of a continued problem to the affected area. Chronic wounds have very different healing behaviour to acute wounds. A foot ulcer usually results from pathological processes such as vascular disease or diabetes millitus which will produce a continued and prolonged event resulting in severe tissue damage (Nigam et al 2006).

There are many different kinds of wound debridement available to persons affected by non-healing wounds and include surgical, mechanical, enzymatic, biological and autolytic debridement (Alexiadou 2012).

Maggot debridement therapy (MDT) is a mechanical/biological debridement procedure where the live maggots of the common green bottle fly (Lucilia Sericata) are placed onto a necrotic sloughy wound (Tian et al. 2013). Maggots have jaws that assist the larvae to move through the food source using mechanical debridement (Barnard 1977). It has also been established that maggots use their mandables to secrete proteolytic enzymes (Biological debridement) that devitalises tissue in a selective manner and liquefy’s the tissue enabling the larvae to digest the material. These enzymes effectively degrade extra-cellular matrix components, including laminin and fibronectin. Therefore assisting in the digestion of the necrotic wound matrix, amounting to an effective debridement therapy (Chambers 2003).

According to Opletalova et al.(2011), maggot effects on wounds have been devided into three areas including debridement, the anti-bacterial effects and the stimulation of wound healing. The debridement of the wound assists in the repair of the defective re-modelling of the extra-cellular matrix proteins and prevents the failure of re-epithelialization. The success of MDT on wounds has now been identified to be as a result of three proteolytic enzyme catagories that have been found in larval excretions (Chambers 2003). These excretions have an inhibitory effect on both gram-positive and gram-negative bacteria (Nigam et al. 2006). Other investigations have identified that the ammonia excreted by maggots has an effect of increasing the pH value of the wound, generating an inhospitable environment for bacterial growth (Pettican 2012).

Reports relating to the properties of maggots are numerous, highlighting their abilities to debride, cleanse, disinfect, and repair stubborn non-healing wounds where conventional therapies have failed. It has been noted for centuries that maggots have the ability to prevent infection and promote healing in wounds. The battlefield surgeon of Napoleon noted that soldiers had returned to the field hospital with healing maggot-infested wounds sustained during battle. It was believed that the maggots had not only prevented infection but had accelerated the healing process (Nigam et al. 2006). During World War 1 orthopedic surgeon William Baer had witnessed for himself the attributes of maggot infested wounds and as a result subsequently pioneered the first systematic application of clinical maggots on a non-healing wound. Baers’ entire work on maggot therapy was published posthumously in 1931(Sherman 2009). The use of MDT became widespread during the 1930’s, however with the availability of antibiotics and the ability to mass produce penicillin, despite MDT’s success, by the mid 1940’s it had all but disappeared from use (Nigam et al. 2006).

More recently and as a result of bacterial resistance to antibiotics, MDT was revisited as a medical procedure to assist in the treatment of non-healing wounds that were resistant to antibiotics or when patients were unable to tolerate anesthesia (Merilyn & Russel 2004).

Method

image012The paper was to take the form of a systematic literature review with the aim of identifying the most relevant and recently published material on the subject of a predetermined academic question. In order to do this 10 electronic databases including: Cinahl, One Search, Cochrane, Pubmed, Wiley online, British Nursing Index, Google Scholar, NICE, NHS Evidence and Embase were searched to identify the relevant literature for the review. There were 23 key word and search terms used within the search parameters and also included a detailed inclusion and exclusion criteria formed part of the overall methodology. Of the literature identified as potential sources of information, 24 papers were formally critiqued and reviewed to form the basis of this document.

Influencing Factors

Qualities that make MDT a successful tool in wound debridement

The research has identified the following authors who give a variety of findings related to this topic and this chapter will discuss these from Tian et al.(2013); Hall (2010); Menon (2012); Jones et al. (2011); Cazander et al. (2013); Pritchard (2013).

Recently, efficacy of MDT has been examined in great depth. Tian et al. (2013) conducted a meta-analysis involving four studies Markevich et al. (2000); Sherman (2003); Paul et al. (2009); Armstrong et al. (2005). Comparisons were drawn between MDT and conventional therapy using three hundred and fifty six patients. Three of the studies Markevich et al. (2000); Sherman (2003); Paul et al. (2009) were in relation to MDT and diabetic foot ulcers (DFUs). The fourth Armstrong et al. (2005) was in relation to maggot therapy in lower extremity “hospice” wound care. Of the four trials selected, Markevich et al. (2000) was a random controlled trial (RCT) and the other three were case control studies, Sherman (2003) being retrospective and Paul et al. (2009), being prospective in nature. The evidential strength provided by a prospective study is more reliable than that of other non-experimental designs because the investigator is able to determine the incidence of an issue and its possible causes (LoBiondo-Wood & Haber 2002).

The outcome measures of the analysis were the healing rate of DFU’s defined as full re-epithelialisation, time of healing, incidence of infection and rate of amputation.

The results of the meta-analysis conducted by Tian et al. (2013) suggesed that the MDT group were significantly superior than the control group in most areas. Comparison of healing rate was twenty seven percent for MDT and nineteen precent for controls. However, within the prospective case control study itself the results relating to the comparison of healing rates were fifty six percent for MDT and sixty two percent for the controls. This suggests a significant difference between the single study Paul et al. (2009) and the four study meta-analysis results identified by Tian et al. (2013).

Further examination revealed that the case control study in question had defined the concept of complete healing differently from the other trials which may have produced the error when collating the outcomes. Amputation rates were fifteen percent in the MDT group compared to thirty six percent in the control group. Regarding comparison of incidence of infection, MDT group was sixty five precent and the control group was eighty percent. Two of the four studies, Sherman (2003) and Armstrong et al. (2005) examined comparisons of time to heal and both studies showed that MDT was on average of three and a half days faster to heal than the conventional group. Tian’s et al. (2013) conclusions suggest that MDT may be more effective in increasing healing rate and anti-biotic free days and decreasing the rate of amputation and time of healing compared with control inteventions. However, due to the insufficencey of high quality evidence of relevant literature regarding the effectiveness of MDT the finding of this meta-analysis are not definitive.

Hall (2013) conducted a review of current literature to establish whether using MDT for the removal of devitalised and infected tissue in chronic wounds is a valuable tool in healing. This review identified four themes that were relevant in confirming the effectiveness of MDT, Debridement, Infection, Granulation and Cost Effectiveness. Systematic electronic searches were conducted for all themes mentioned above. From these searches a total of twelve studies were identified and discussed within the review. It was concluded by Hall (2013) that the review of the relevant literature identified that MDT was both an effective and efficient tool in the reduction of time to complete debridement of chronic wounds, when compared with conventional therapies. However, there is little significant difference regarding the time for wounds to heal, which is in conflict with the evidence of Tian et al. (2013). Some conventional therapies are more pedestrain at fully debriding a wound bed of devitilised tissue.

There is evidence to suggest that MDT does have the ability to supress and eradicate infection and may stimulate the re-granulation of vitilised tissue. Unfortunately, the trials within this review had some evidence of limitation, including very small sample groups and non-randomised selection of participants which may influence bias within the study.

Menon (2012) conducted a literature review of methods of MDT and patients experiences. An electronic database literature search was conducted and common themes were identified, namely, debridement, antimicrobial effects and psychological issues. Menon (2012) further discussed and compared the appropriate methods of application of both free range and confined maggots. The review identified that both application methods debride with similar efficiency. Menon (2012) further reviewed on the issue of both applications of MDT when compared to that of hydrogel. It was established that time to ulcer healing was not significantly different between the two groups which is a direct contradiction to the findings of Tian et al. (2013) but does corroberate the results of the review conducted by Hall (2013). However, it can be confirmed that Hall (2013); Tian et al. (2013); Menon (2012) concurs the MDT was considerably more efficient at time to full debridement than the conventional therapy. It was also stated in the review by Menon (2012) that MDT produces secretions that inhibits the bacterial load of wounds that are susceptible to infection. In doing so they are helping to eliminate meticillan resistant staphylococcus aureus (MRSA) and other antibiotic resistant bacteria. Larval secretions change the pH value within the wound making it more alkaline. This in turn makes the wound an inhospitable environment for various bacteria. MDT also disrupts and destroys the formation of colonies of bacteria, namely biofilms. Menon (2012) concludes that if used appropriately, MDT can be an in-expensive, efficient and effective debridement tool. Its properties of accelerated debridement and anti-bacterial action have been witnessed in both acute and chronic wounds alike, especially in diabetic foot ulcers. MDT has few side effects and is generally well received by patients, however, evidence suggest that some individuals, dependent on their co-morbidity, may experience pain as a side effect and this should be managed from the offset with appropriate analgesia.

Jones (2011) produced a literature review examining maggots and their role in wound care. A comprehensive search for appropriate material identified seven articles suitable for viewing. The Critical Appraisal Skills Programme (CASP) critiquing tool was used on the collated literature where four themes were subsequently established:- Infection control and Promotion of healing will be discussed in this chapter. The “Yuck” factor will be discussed in a later chapter. Cost effectiveness will not be discussed in this paper.

It was confirmed by Jones (2011) that MDT was a driving force behind the reduction of bacteria in ulcerated wounds, therefore, being responsible for the prevention of infections. Further to this, it has the added benefit of reducing malodorous wounds and reducing pain. The reduction of pain by the use of MDT may be at odds with the comments made in the review by (Menon 2012). Jones (2011) discussed the promotion of healing. It was stated MDT did accelerate necrotic tissue debridement from chronic wounds which in turn promoted rapid granulation when compared with conventional therapies. These comments were similar in nature to those of Tian et al. (2013); Menon (2012); Hall (2013).

Cazander et al. (2013) conducted a litratrure review that examined the multiple actions of the Lucilia Sericata larvae in hard to heal wounds and discusses the molecules contained within the maggot secretions that accelerate wound healing and reduce chronic inflammation and inhibit bacterial infection. His review accepts that MDT has a proven value as a debridement tool along with other benefits that have been widely reported in clinical trials, inluding anti-infection, immunomodulation, angiogenesis, tissue remodelling and regeneration.

In addition, maggot secretions contain two different molecules that are able to prevent bacterial biofilm formation and breakdown existing colonies of bacteria as previously discussed and corroberated by Menon (2012). With regard to wound healing, secretions also enchance the production of growth factors by monocytes and macrophages within the wound. Maggots secrete various enzymes that consume devitalised tissue and it may be the case that these enzymes also destroy various host molucles within the wound. It has been suggested by Cazender et al. (2013) that the larvae may produce anti-bacterial molecules enabling them to survive in a heavily contaminated bacterial environment who compete with the larvae for their nutritional source. There is potential that by reducing the bacterial load, maggots may well control the process of decay and therefore protecting themselves from harmful bacteria. Cazander et al. (2013) is of the opinion that the combined actions of molecules within maggot secretions are responsible for the beneficial effects of MDT.

Pritchard (2013) argued that larval therapy should be a primary and secondary treatment in wound healing. The debridement of the wound conducted by the primary application and the secondary applictation targeted at the debrided wound on a cellular level that promotes healing. Pritchard (2013) states there is evidence that molecules secreted by maggots can have a role in promoting tissue regeneration and accelerating wound healing. this idea is shared by the review of Cazander et al. (2013). Pritchard (2013) explains that maggot secretions play an intrinsic role in various physiological actions including perfusion; reduction in inflammation; anti-bacterial effect; promoting cell signalling; fibroblast motogenesis, and angiogenesis. Maggot secretions have been shown to promote fibrinolysis therefore interacting with and influencing perfusion. Secretions are believed to interact directly with aspects of the inflammatory response, modulating its performance to aid and contribte to wound healing. They destroy and prevent the formation of biofilms that cause infection. Maggot secretions in low doses have been shown to induce changes in cell morphology which stimulate fibroblasts into the wound . In conclusion Pritchard (2013) states that the growth promoting activities of maggots and their secretions has been demonstrated effectviely, and the investigations conducted within the subject strongly indicates that maggots are capable of much more that just wound debridement. The reapplication of MDT onto a debrided wound will not only assist in the healing process but also closure of the wound.

This theme has shown to some degree that maggots and their secretions have several primary and secondary benefits that supports the argument that MDT is a very useful tool in the management of ulcerated wounds.

Factors that present barriers for the use of MDT

The research has identified authors who have findings relating to this topic, namely Mudge et al. (2014); Davydov (2010); McCaughan et al. (2013); Menon (2012); Jones et al. (2011); and Gilead et al. (2012).

Mudge et al. (2014) conducted a randomized controlled, open, observer blind, parallel group study relating to a trial of larval therapy for the debridement of leg ulcers. The study compared the clinical effectiveness of a larval therapy dressing with a standard debridement treatment, namely Hydrogel. According to the BNF (2014) hydrogel dressings are recommended for dry sloughy wounds and donate liquid to the wound enabling autolytic debridement of the necrotic tissue to take place. The dressings are best avoided in cases of infection of heavily exuding wounds. The study aim was to identify the time of debridement of venous leg ulcers and mixed arterial leg ulcers. Sixty four patients completed the full study. There were thirty two patients in each group of which thirty one patients of the larval group and eleven patients in the hydrogel group fully completed the study. Mudge et al. (2014) explained that previous research conducted by Dumville et al. (2009) intimated that pain associated with larval therapy should be anticipated. For this reason throughout the trial participants experience of pain was monitored during each treatment visit. It was subsequently identified that the larval therapy group experienced ulcer related pain or discomfort on a more regular basis than that of the hydrogel group. More participants withdrew from the study as a result of pain than for any other reason. The review of Davydov (2012) corroborates the findings of Mudge et al. (2014) and further adding that pain is indeed a common side effect of larval therapy and develops within two or three days from commencement of treatment and according to the findings within Sharman (2002); Sharman (2003); Courtenay (2000) between four percent and thirty three percent of patients experienced pain that ranged between mild to severe in intensity. McCaughan et al. (2013) in her qualitative study identifies a small qualitative study by Kitching (2004), who’s findings within his own study suggested that patients experienced a reduction in the level of pain experienced when using larval therapy. It can be seen that this statement directly conflicts with those of Davydov (2012); Mudge et al. (2014); McCaughan et al. (2013).

McCaughan et al. (2013) is a qualitative study regarding patients’ perceptions and experiences of venous leg ulcers and their attitudes towards larval therapy. Eighteen patients took part in the study twelve men and six women. Five people in the study were treated with larval therapy. McCaughan et al. (2013) comments that two of the five patients treated with larval therapy experienced severe pain and were withdrawn from the study. Menon (2012) in her literature review reiterates the comments made by all the above authors that there was significantly more pain in groups of patients that had undergone larval therapy as opposed to Hydrogel therapy. Gilead et al. (2012) adds that the conclusions of a review they conducted of their experiences of treating four hundred and thirty five patients with a combined number of seven hundred and twenty three wounds over a period of thirteen years, revealed that although eighty two point one percent of wounds fully debrided, there was a significant increase in the level of pain and discomfort reported by thirty eight percent of the patients. This agrees with the comments made by Menon (2012); McCaughan et al. (2013); Mudge et al.(2014); Davydov (2010).

Jones et al. (2012) discusses the “Yuck” factor, which for the purpose of this dissertation has been interpreted as the clients distaste or mental aversion to the whole concept. Jones et al. (2011) draws on the phenomenological study of Kitching (2004) whereby six patients were monitored over a twelve week period. The initial pre-conceived feelings of the group regarding maggot therapy were feelings of disgust and not wanting to have the maggots crawling around in their wound. However, following a period of education and subsequent therapy five out of six of patients were subsequently un-phased by the thought of maggot therapy and that their wounds had improved somewhat. According to Jones et al. (2011) further studies from Steenvorde (2005); Courtenay (1999) established that providing all patient issues are addressed through appropriate, up to date, honest and accurate information regarding the therapy and its perceived outcomes, concerns regarding this issue can be eliminated. Encouraging practitioners and patients alike to accept and work with the therapy will go a long way in dealing with the barriers and issues associated with maggot debridement therapy. When these problems arise nurses are best placed to promote and influence patient choice with good quality transparent communication.

Davydov (2014) commented that some patients may feel repulsed by the idea of live organisms within their wounds which may lead to a refusal to have this therapy administered. McCaughan et al. (2013) identified that participants in their study believed that the feelings of squeamishness in relation to maggots would be short lived if they witnessed an improvement in the wound. It was also acknowledged that patients had built their own knowledge database regarding the treatments and abilities of MDT.

The evidence clearly shows there are some issues regarding the use of maggot debridement therapy and this chapter has highlighted a couple of the most prominent issues. These issues are easily resolved by planning for pain and having full, honest, open discussions with patients regarding the treatment prior to its application (Jones et al. 2011).

Discussion

Chronic wounds are notoriously difficult the treat especially in patients with failing health. Evidentially, conventional debridement therapies have been shown to work, however, research suggests that MDT is more effective and efficient at debriding chronic ulcerated leg wounds (Sun et al. 2014).

Diabetic patients generally suffer peripheral vascular changes and as a result of poor perfusion tend to suffer with severe septic lower limb wounds (Pettican 2012). Surgical debridement and other debridement techniques can be used where appropriate. However, with surgical debridement there is the potential of removing healthy tissue alongside devitalized matter (Pettican 2012). Maggots on the other hand have been shown not to damage healthy tissue but remove devitalised necrotic matter leaving healthy tissue and granulating wound bed material undamaged (Pettican 2012).

The evidence has suggested that MDT offers the clinician a debridement tool that has a faster time of healing, fewer amputations, fewer incidence of infection therefore a higher rate of antibiotic free days (Tian et al.2013). Maggots have shown an ability to remove sloughy, devitalised tissue from the wound bed more quickly than other conventional therapies including hydrogel (Menon 2012). It has been established that excretions and secretions from maggots contain proteoltyic enzymes which devitalise selective tissue effectively degrading extracelular matrix components and digesting the matter in a liquid form (Pettican 2012). Maggots have also been shown to inhibit the bacterial load within the wound and also altering the pH value of the wound creating an inhospitable atmosphere for bacteria such as MRSA to survive. Maggots disruprt, destroy and prevent the formation of biofilms or bacterial colonies associated with wounds, Therefore, preventing and eradicating infection (Jones 2011). There have been suggestions that MDT has further microbiolical properties including anti-imflamatory abilities and immunomodulation, angiogeneis, tissue remodelling and regeneration (Cazander et al. 2013).

This review has illustrated that the use of MDT has many beneficial effects and advantages over conventional therapies on the debridement of diabetic chronic ulcerated wounds. Where there is a need for speedy debridement or where a patient cannot undergo surgical debridement (Sun et al. 2014). MDT should be considered by health care professionals as a primary tool in the treatment of chronic infected wounds within the hospital environment or community setting rather than an after thought or a last resort (Pettican 2012). However, there are issues that must be considered and addressed when using MDT. It has been identified by several authors including Mudge et al. (2014); Dumville et al. (2009); Davydov (2012); Sharman (2002); Sharman (2003); Courtaney (2000); Menon (2012); Gilead (2012) that ulcer ralated pain is a side effect of MDT treatment and that it can be between mild to severe in nature. The onset of pain is normally within the first two or three days and can affect between four percent and thirty three percent of patients. Only one author Kitching (2004) claimed that the majority of the patients in his study had a reduction in pain. Patients have been known to withdraw from studies as a result of associated pain.

Pettican (2012) makes the connection between pain and the alteration of the pH balance within the wound caused by maggot secretions and excretions and believes for MDT to succeed pain management is critical. Within this study there is overwhelming evidence to suggests pain is an overriding factor that should be monitored during treatment and having analgesia available from the outset may ensure that the therapy is tolerated by patients who would remain pain free. Should the issue of pain not be addressed early on in the process, pain may present itself as a barrier for the use of MDT.

The aversion to maggots is not uncommon, Jones et al. (2012); Kitching (2004) Steenvorde (2005); Courtenay (1999) all highlight issues concerning the distaste and aversion both patients and clinicians have regarding MDT. Interestingly, it has been established that the majority of persons who were given appropriate and transparent education regarding the therapy tolerated it well. Educating clinicians and patients alike in the treatment and its application is essential for the fears and feeling of repulsion to be eradicated.

From the study of McCaughan et al. (2013) it can be seen that patients with chronic leg ulcers were willing to try alternative therapies in order to rid them of their wounds as their quality of life had been blighted by this condition. Feelings of squeamishness were soon forgotten on visualising the improvement within the wound. McCaughan et al. (2013) How the treatment was presented to the patients was also a factor as to whether the treatment would be accepted by the patient.

One of the most discussed topics was the lack of research findings regarding the credibility of the use of MDT. Most authors within the review make comment regarding that fact that research for the use of this therapy is simply at this time not strong enough. The reasons for this lack of rigorous evidence has been identified as a lack of random controlled trials on the subject, poor description controls, non-blinded assessment outcomes, poor description of control and inadequate sample sizes (Gottrup 2012) and (Tian et al. 2013).

For MDT to be taken seriously, a more intensive evidential programme needs to be undertaken. It can be seen that very few random control trials have been carried out on the efficacy of MDT. Jones et al. (2011) identifies more healthcare professionals than ever before are reliant on evidence based practice when making clinical decisions regarding treatment. As a result of this, it is felt that more indepth research relating to MDT must take place in order to encourage and support the use of this debridement tool. Random controlled trials are the essence of research and offer the strongest evidential platform from which to stand when trying to prove the strengths or weaknessess of a particular subject (Ellis 2010). RCT’s explore the relationship between two variables therefore creating an RCT for the efficacy for MDT is going to be difficult to prepare because of the nature of MDT designing prospective randomised and placebo-controlled trials may prove difficult (Davydov 2011).

Conclusions

This work has examined what factors influence the use of maggot MDT in the nursing management of diabetic foot ulcers. It has established through detailed examination of current available literature that MDT could be a valuable tool in the treatment of necrotic wounds despite there being very few credible random controlled trials relating to its efficacy and use.

Obstacles such as the lack of strong evidential literature, associated pain and the feelings of revulsion and disgust have been highlighted within the paper and are believed to be elements within the subject that may have hindered the success and use of this therapy within the medical profession.

However, with detailed, specific, in-depth random controlled trials and thorough meta-analysis investigations of the current literature, well directed education for clinicians and patients alike and honest, transparent communication with clients, MDT may in time secure itself amongst the existing debridement tools that assist in the nursing management of diabetic foot ulcers within the hospital environment or community setting.

Vincent H Curtis, Adult Nursing, BSc (Hons) Nursing student

References

Alexiadou, K. & J. Doupis. 2012. Management of diabetic Foot Ulcers. Diabetes Therapy, pp. 3:4, 1-15.

Armstrong, D., P. Salas and B. Short. 2005. Maggot therapy in lower extremity hospice wound care, fewer amputations and antibiotic free days. Journal of American Podiatry , pp. 95: 254-257.

Armstrong. D., V. Kanda and L.A. Lavery. 2013. Mind the Gap: Disparity between research funding and cost of care for diabetic foot ulcers. Diabetes Care, pp. 1815-1817.

Barnard, D. R. 1977. Skeletal muscular mechanisms of the larva of Lucilia Sericata in relation to feeding habit. Pan-Pac Entomology, pp. 53, 223-229.

Blueman, B. 2012. the use of larval therapy to reduce the bacterial load in chronic wounds. Journal of Wound care, pp. vol 21, no 5.

British National Formulary, 2013/14. BNF 66 September 2013 – March 2014. London: BMJ.

Cazander,G., D.Pritchard., Y.Nigam., W.Jung., and P.H. Nibbering. 2013. Multiple Actions of Lucilia Sericata lavae in Hard to Heal Wounds. Bioessays 35, pp. 1083-1092.

Chambers, S., S.Woodrow. and A.P. Brown. 2003. Degredation of extracallular matrix componenets by defined proteinases from the green bottle larva Lucilia Sericata used for the clinical debridement of non healing wounds. British Journal of Dermatology , pp. 148, 14-23.

Courtenay, M. 1999. The use of larval therapy in wound management in the UK. Journal of Wound care, pp. 8: 177-180.

Courtenay, M., J.Church. & T. Ryan. 2000. Larval therapy in wound management. J R Soc Med , pp. 93(2) 72-74.

Cutliffe, J. and M. Ward. 2007. Critiquing nursing research ( second edition). London: Quay books.

Davydov, L. 2011. Maggot Therapy in wound management in modern era and a review of Published Literature. Journal of Pharmacy practice, pp. 24(1) 89-93.

Driver, V. and P. Blume. 2014. Evaluation of wound care and health carem use costs in patients with diabetic foot ulcers treated with negative pressure wound therapy versus advanced moist wound therapy. Journal of the American Podiatric Medical Association, pp. Vol 104 , No 2, pages 147-153.

Dumville, J.C., G. Worthy, and J Bland. 2009. Larval Therapy for Leg Ulcers (VenUS II) randomised controlled Trial. British Mdeical Journal , p. 338; b773.

Ellis, P. 2010. Understanding Research for Student Nurses. Exeter: Learning Matters.

Gilead, M. I. 2012. the use of maggot debridement therapy in the treatment of chronic wounds in hospitalised and ambulatory patients. Journal of Wound care, pp. vol 21, no 2.

Gottrup, F. and B. Jorgensen. 2011. Maggot Debridement, An alternative method of debridement. Open Access of the Journal of plastic Surgery, pp. 290-302.

Hall, 2010. a review of maggot debridement therapy to treat chronic wounds. British Journal of nursing, pp. Vol 19, no15.

Jones, G., J Green. and K. Lillie. 2011. March. Maggots and their role in wound care. Wound care, p. S 24.

Kitching, M. 2004. Patients perceptions and experiences of larval therapy. Journal of wound care, pp. 13: 25-29.

Lo-Biondo-Wood, G and J. Haber 2002. Nursing research, methods, critical appraisal and utilization. St Louis: Mosby.

Margolin, L. and P. Gialanella. 2010. Assessment of the anti-microbial properties of maggots. international Wound Journal, pp. 7: 202-204.

Markevich, Y.O.,J. Mcleod-Roberts. & Melloy, E., 2000. Maggot therapy for diabetic neuropathic foot wounds. Diabetlogia, p. 43 (supp 1)A 15.

McCaughan, D., N. Cullum. and J. Dumville. 2013. Patients perceptions and experiences of venous leg ulceration and their attitudes to larval therapy, an in depth qualitative study. Journal of Health Expectations, pp. 1-15 .

Menon, J. 2012. Maggot Therapy. British Nursing JournaL, pp. vol 21, No 5.

Merilyn, G. and R. Russel. 2004. Fly Larvae for Wound Management, A maggot Makeover. Institute of Clinical Pathology and Medical Research, pp. Vol 15, no 11-12, Pages 218-219.

Mudge, E., P. Price., N Walkley. and K. G Harding. 2014. A randomised controlled trial of larval therapyfor the debridement of leg ulcers: results of a multi center randomised controlled open observer blind parellel group study. wound healing society, pp. 43-51.

Nigam, Y., Alison, B., Steven, T. & Norman Arthur, R., 2006. Maggot Therapy: The Science and Implication of CAM. Part 1- History andbacterial resistance. Open Access Publication – eCAM, pp. 3 (2) 223-227.

Nigam, Y., A. Bexfield., S. Thomas., and N. Ratcliffe. 2004. Detection and partial characterisationof two antibacterial factorsfor the excretions of medical maggots Licilia Sercata and their activity against methicillin-resistant staphylococcus aureus MRSA. Microbes Infect, pp. 6: 297-304.

Opletalova, K., X. Blaizot., B. Mourgeon., Y. Chene., C. Creveuil., P. Combemale., A.L Laplaud., I. Sohyer-Lebreuilly. and A. Dompmartin. 2011. Maggot therapy for wound debridement a randomized multi-center trial. Arch dermatol, pp. Vol 148 no 4, 2012 April.

Paul, A.G., N.W. Ahmad., H.L Lee., A. M. Ariff., M Saranum., A.S. Naiker. and Z. Osman. 2009. Maggot debridement therapy with Licilia Cuprina: a comparison with conventional debridement in diabetic foot ulcers. International Wound Journal, p. Vol 6: no 1.

Pettican, A. and C. Baptista. 2012. Maggot debridement therapy and its role in Chronic wound management. Singapore nursing journal, pp. Vol 39, no 1, Jan to March.

Polit, D.F. and C.Tatano-Beck. 2010. Essentials of nursing research, appraising evidence for nursing practice. Philadelphia: Wolters Kluwer/lippincott Williams and Wilkins.

Pritchard, N. and Y. Nigam. 2013. Maximising the secondary beneficial effects of larval therapy. Journal of Wound Care, p. Vol 22 no11.

Sherman, R. 2002. Maggot versus conservative debridement therapy for the treatment of pressure ulcers. Wound repair and regeneeration, pp. 10: 208-214.

Sherman, R. 2003. Maggot therapy for threating diabetic foot ulcers unrespobsive to conventional therapy. Diabetes Care, pp. 26: 446-451.

Sherman, R. 2009. Maggot Therapy Takes Us Back to the Future of Wound Care: New and Improved Maggot Therapy for the 21st Century. Journal of Diabetes Science and Technology, pp. Volume 3, Issue 2, 336-344.

Sherman, R. & K.Shimoda. 2004. Pre-surgical maggot debridement of soft tissue wounds is associated with decreased rates of post operative infection. Clinical Infection Dif, pp. 39: 2067-70.

Sherman, R., Wyle, F. and M. Vulpe. 1995. Maggot Debridement therapy for treating pressure ulcers in spinal cord injury patients. Journal of Spinal Cord Medicine, pp. 18: 71-4.

Singh, N., D. G. Armastrong. and B.A. Lipsky. 2005. Preventing Foot Ulcers in Patients with Diabetes. American Medical Association, pp. Vol 293, no 2.

Steenvoorde, P., T. Budding, and J. Oskam. 2005. determining pain levels in patients treated with maggot debridement therapy. Journal of wound care, pp. 14(10) 485-488.

Sun, X., K. Jaing., J. Chen., L. Wu., H. Lu., A. Wang. and J. Wang. 2014. A systematic review of maggot debridement therapy for Chronically infected wounds and ulcers. International journal of infectious diseases.

The National Diabetes Information Service, 2013. What is the cost of the diabetes service?. [Online]
Available at: http://www.yhpho.org.uk/resource/view.aspx?RID=137555
[Accessed 11th June 2014].

Tian, X., X.M. Liang., G.M. Song., Y. Zhao. and X.L. Yang. 2013. Maggot debridement therapy for the treatment of diabetic foot ulcers a meta analysis. Journal of Wound care, pp. vo l22, no 9..

Wayman, J., V. Nirojogi., A.walker., A. Sowinski. and M.A. Walker. 2000. The cost effectiveness of larval therapy in venous ulcers. Tissue viability, pp. 10: 91-94.

Wilasrusmee, C., M. Marjareonrungrung., S. Eamkong., J. Attia., N. Popram., S. Jirasisrithum. and A. Thakkinstain. 2013. Maggot therapy for chronic ulcer: a retrospective cohort and mata-analysis. Asian Journal of Surgery.

Zarchi, J. and G.B.E. Jemec. 2012. the efficacy of maggot debridement therapy a review of comparative trials. International Wound Journal, pp. 469-477, no9.