The use of maggot debridement therapy in 41 equids

Transcription

1 bs_bs_banner The use of maggot debridement therapy in 41 equids O. M. LEPAGE*, A. DOUMBIA #, M. F. PERRON-LEPAGE and M. GANGL Université de Lyon, Lyon, France VetAgro Sup, Veterinary Campus of Lyon, Equine Department, Marcy l Etoile, France Theizé, France # SPANA Rue 77, Badalabougou, Bamako, Mali. Equine Veterinary Journal ISSN DOI: /j x *Correspondence olivier.lepage@vetagro-sup.fr; Received: ; Accepted: Presented in part at the World Veterinary Congress, Cape Town, South Africa, October Summary Reasons for performing study: Maggot debridement therapy is a long-established tool to promote wound healing. Objectives: To describe and assess the results of this technique in equids with various lesions. Methods: Retrospective analysis performed on cases in which, depending on clinical case, type, size and location of the wound, maggots were applied either in direct or indirect contact with the wound. Results: Treated cases (n = 41) included horses with foot pathology (n = 9), laceration of the limbs (n = 15), other soft tissue abscesses or wounds (n = 6), fistulous withers (n = 5), other musculoskeletal infection (n = 2) and dehiscence of the linea alba (n = 4). In 5 cases, a second maggot application was necessary to reach the desired level of wound healing. In 38 cases a favourable outcome was reached in less than one week. In one individual with a sequestrum, healing was uneventful after its removal. In 2 other horses, squamous cell carcinoma and melanoma were involved in chronic infected wounds and complete healing was not achieved because of recurrence of underlying tumours. Some discomfort was recorded in 7 individuals between 24 and 72 h of treatment. Conclusions: Maggot debridement therapy can be recommended in equids for debridement and enhanced healing and its potent antibacterial action. Maggot debridement therapy is not recommended on wounds invaded with a tumour and if bone sequestration is suspected. Potential relevance: Maggot debridement therapy can be an integral part of modern wound care in equids. Keywords: horse; donkey; maggot; biotherapy; wound dehiscence; debridement therapy Introduction Maggots have been used for the treatment of wounds for centuries [1] and are now part of the therapeutic options used by human and veterinary surgeons. Maggot debridement therapy, for human [2] and veterinary medical purposes [3,4], uses freshly emerged, germ-free larvae of the common green bottle fly Lucilia sericata. The action of maggots on wound healing is attributed to a debridement effect, through the production of potent proteolytic enzymes [5], an antiseptic effect [6], a direct effect on cytokine and cell proliferation involved in wound healing [7] and breakdown of biofilm formation [8,9]. During the dissolution of fibrin and necrotic tissue, maggots also destroy and digest bacteria [6]. With regards to the prevalence of antibiotic resistance, the action of maggots against methicillin-resistant Staphylococcus aureus (MRSA), multidrug-resistant Pseudomonas aeruginosa or Escherichia coli is of particular interest [10]. Maggots can be applied to a wound in a direct or an indirect contact technique. With the direct contact technique, free range maggots (Larve E) a are applied directly onto the surface of the wound. Once the maggots are placed, a nylon retention net is fixed to restrict the maggots to the area of the wound. With the indirect contact technique, maggots are deposited on the surface of the wound within a biobag. The indirect contact method has practical and aesthetic advantages when maggot debridement therapy is used in man [11]. Maggot debridement therapy has been used in horses as an alternative approach to the management of septic navicular bursitis, complicated laminitis [3,12], infected abscess with pedal bone osteomyelitis, other hoof diseases [1] and supraspinous bursitis [4]. This study describes the clinical outcome of 41 equids treated with maggot debridement therapy with various lesions. Materials and methods Medical records of equids that had one or multiple treatments with maggot debridement therapy between March 2007 and March 2011, at either the Equine Clinic from the Veterinary Campus of Lyon (France) or at SPANA Veterinary Centre of Bamako (Mali), were reviewed. The data selected from the medical records included history, clinical signs, technique of applying maggot debridement therapy and response to therapy, based on clinical description and photographs. Animals were presented with wounds of 2 days to more than 8 weeks duration. Before ordering the maggots, the size of the wound was estimated. In human medicine it is recommended that 5 10 maggots are placed on each square centimetre surface of a wound [11]. In all horses with wounds deeper than 2 cm, the surface area was multiplied by the depth of the wound in centimetres. The number obtained was then multiplied by 5 in order to obtain the total number of maggots required for a specific lesion. The maggots were ordered from the same company (ZooBiotic) a and received the following day, except during weekends. Upon arrival at the clinic, maggots were removed from the delivery bag as soon as possible and stored at 8 10 C if not used immediately. Maggots were applied in a direct a or an indirect a contact technique. In the first technique, maggots were applied directly onto the wound (Fig 1). In the indirect contact technique, a closed polyester net with absorbent hydrophilic polyurethane foam (LarveE BioFOAM T ) a (Fig 2), was deposited on top, or into, the wound. With both methods, the wound was prepared with a light surgical debridement in order to remove debris, dry necrotic tissue and allow for adequate drainage from the lowest point of the wound. If a foot was involved, hoof wall resection was performed to allow better access to the lesion or to facilitate drainage. All other local treatments were discontinued before the maggots were applied to the wound and systemic antimicrobial therapy was discontinued the day maggot debridement therapy commenced. The only exception was the use of regional limb perfusion with gentamicin in selected cases of septic podotrochlear bursitis. Neither occlusive dressings nor film were applied as these can be lethal to the larvae [13]. If necessary, strips of hydrocolloid dressing or zinc paste were applied on the surrounding healthy skin to delineate the wound. In all cases a nylon retention net or an elastic cohesive retention bandage (Easifix cohesive) b was placed on top of the wound to confine the maggots to the area of the wound. Depending on the anatomy, bandages were specifically adapted for each individual. Three methods of application were used: 1) hoof bandage or orthopaedic shoe with a plate, 2) stent bandage and 3) nonocclusive, sleeve bandage. With the first method of application, a specific shoe with treatment plate was adapted to the foot. If the farrier was not available, a 120 Equine Veterinary Journal 44, Suppl. 43 (2012) EVJ Ltd

2 O. M. Lepage et al. Maggot debridement therapy in equids a) a) c) Fig 1: Direct contact application of maggots in a stallion with streptococcus zooepidermicus abscess around the genital region. a) After surgical opening and light debridement, a net is preplaced under the margin and free range maggots are poured into the cavity before ( closing the net. temporary full nonocclusive bandage was applied. A biobag or free range maggots were applied to the surface of the wound of the foot, which was then covered with net and gauze sponges. The stent bandage method was used for wounds involving regions difficult to cover by conventional means, particularly lacerations of the body and upper limb. In these cases, the Fig 3: Adult horse with wound dehiscence of the linea alba after an exploratory laparotomy. a) Aspect of the wound before maggot debridement therapy; free range application of maggots and c) aspect of the wound after 4 days contact with 600 maggots. biobag was secured in position by partially closing the skin over the wound with one or 2 sutures, leaving sufficient space to allow drainage to occur. When free range maggots were used, a net was placed over the wound, taped into place and then covered with an absorbent cotton pad or nappy. A nonocclusive sleeve was created by applying elastic adhesive bandages proximal and distal to the wound (Tensoplast Vet) b. The net was then applied to encircle the limb and sealed to the distal adhesive bandage. The maggots were poured into the sleeve, which was then fixed to the proximal elastic adhesive bandage. A cotton pad was applied over the area to absorb secretions and a rigid prosthesis added if necessary. The outer dressing was changed daily. Maggots were left in place for approximately 72 h and if further debridement was required, a second treatment was performed, with fresh larvae for an additional 3 4 days. All used dressings were disposed of as clinical waste [6]. Histology was performed on 6 biopsies obtained from 4 working donkeys with supraspinous bursitis and from 2 horses with chronic proliferative infected wounds of the limbs. Results Fig 2: Maggots applied for 2 days with the indirect contact technique (biobag, maggots are present between pieces of foam within a closed polyester net). Equine Veterinary Journal 44, Suppl. 43 (2012) EVJ Ltd Forty-one equids were admitted for maggot debridement therapy during the study period; 35 horses, 4 donkeys and 2 ponies of all ages and both sexes. Maggots were applied in 36 cases with the direct contact technique and in 5 cases within a biobag (Table 1). Surgical debridement was performed in the chronic wounds and in 3 cases of linea alba wound dehiscence (Fig 3). If haemorrhage occurred 121

3 Maggot debridement therapy in equids O. M. Lepage et al. TABLE 1: Clinical injury or problem, type of maggot application, associated procedures and secondary wound healing evolution in 41 equids No. Injury or problem Maggot application Associated procedure Secondary wound healing 1 2 Septic navicular bursa Biobag Street nail procedure + loco-regional Completed antibiotherapy 3 Fistulous withers in a donkey Biobag LSD Completed 4 Fistulous withers in a donkey Biobag LSD Death from tetanus before complete healing 5 Fistulous withers in a donkey with Biobag LSD Completed onchocerca cervicalis 6 8 Septic navicular bursa Free range Street nail procedure + loco-regional Completed (one case after 2 MDT) antibiotherapy 9 Keratoma Free range Hoof wall resection, LSD Completed Septic pedal bone osteitis Free range Sole resection Completed after 2 MDT Chronic heel bulb laceration Free range Cast immobilisation after MDT Completed 15 Chronic proliferative wound dorsal LH Free range LSD Completed after removal of a sequestrum cannon bone 16 Chronic proliferative wound proximo plantar aspect RH tarsus Free range SD Melanoma proliferation, debridement and granulation tissue production after MDT but incomplete healing, euthanasia 17 Chronic proliferative wound dorsoproximal RH fetlock Free range SD Squamous cell carcinoma recidive, incomplete healing, euthanasia Various acute or subacute limb laceration Free range LSD Completed with various size of scar 28 Chronic tuber coxae fracture with Free range LSD to remove a bone fragment Completed fistulisation 29 Cannon bone fracture with MRSA infection Free range LSD with removal of 2 loose screws Completed after 2 MDT in regards of a DCP reconstruction Soft tissue abscess (1 buttock, 3 neck, 1 Free range LSD Completed scrotum, 1 prepuce) 36 Fistulous withers in a horse Free range Two LSD at one week interval Completed after 2 MDT 37 Fistulous withers in a donkey with Free range LSD Completed onchocerca cervicalis Wound dehiscence of the linea alba including 2 cases of multidrug resistant infection Free range LSD in 3 out of 4 cases Completed (one case after 2 MDT) LSD = light surgical debridement; SD = surgical debridement; MDT = maggot debridement therapy; LH = left hind; RH = right hind; MRSA = methicillin-resistant Staphylococcus aureus; DCP = dynamic compression plate. duringdebridement,acompressivebandagewasappliedforapproximately 1 h before the maggots were applied to the wound. After h a red-brown exudate was produced from the wounds (Fig 4). Signs of discomfort were evident in 7 horses between 24 and 36 h of onset of treatment, including repeated rubbing of the wound or moving of a treated limb. Because the effects of the initial period of maggot debridement therapy were unsatisfactory in 5 cases, a second period of maggot debridement therapy was performed 1 3 days later. There was one case each of MRSA infection (Fig 5), pedal bone osteomyelitis, navicular bursa infection, linea alba dehiscence and a chronic hindlimb laceration. All other cases had one maggot debridement therapy with a number of maggots varying from 300 to 900. Debridement, disinfection and healing occurred in all (Fig. 6) but 3 cases, one of which was complicated by the presence of melanomas (Fig 7). An unsatisfactory response to maggot debridement therapy also occurred in a horse with a mass on the dorsolateral aspect of the limb that was subsequently determined to be a squamous cell carcinoma. This horse was subsequently subjected to euthanasia. The third case had a degloving injury that responded to maggot debridement therapy with granulation of the wound except for a cleft over the dorsoproximal third metacarpal bone. Radiographic examination revealed a sequestrum, which was removed surgically; the wound then healed uneventfully. Histological examination of biopsies obtained from 4 working donkeys with supraspinous bursitis demonstrated onchocera cervicalis in 2 cases. One of these donkeys died from tetanus before the wound healed. Discussion Only a few species of fly maggots, primarily blowflies, are suitable for medical purposes. Those used in this study were certified germ-free by the producer. This was possible because the fly embryo of Lucilia sericata inside the blowfly egg was sterile and the chorion enveloping the egg extremely resistant to disinfectants. Therefore, fly eggs can be sterilised by disinfecting the surface of the egg and allowing the larvae to hatch in a sterile container. A variety of sterilisation techniques are described in the literature [11] with the optimal disinfectant having a high antibacterial potency with a low level of toxicity for the egg. When maggot debridement therapy is used in horses as an adjunctive treatment for puncture wounds to the navicular bursa, free range larvae have been recommended [12]. In the current study, the number of larvae used for treatment of wounds deeper than 2 cm was increased to account for the depth of the wound. By the second day of treatment, the majority of wounds had developed a reddish-brown exudate. This was considered evidence of removal of necrotic tissue by the maggots as their secretions are antiseptic in nature [6]. The discomfort observed in 7 horses may be explained by the crawling action of the larvae on healthy sensitive tissue, as some human patients undergoing maggot debridement therapy have reported feeling a tickling or itching sensation [11]. In a previous study in equids, maggots placed onto wounds of the navicular bursa were reported to survive for 5 7 days [12]. This finding was not duplicated in the current study in which maggot debridement therapy was applied at different sites and the maggots typically were ineffective or had failed to survive longer than 4 days. 122 Equine Veterinary Journal 44, Suppl. 43 (2012) EVJ Ltd

4 O. M. Lepage et al. Maggot debridement therapy in equids antimicrobials (e.g. gentamicin) while not altering that of other antimicrobials (e.g. tobramycyin). The synergy between gentamicin and maggot excretions/secretions may be valuable in equine clinical cases and may help explain the high success rate with maggot debridement therapy in this study and others [12]. As with many forms of wound therapy, different types of bandages may need to be used depending on the location and type of wound. The combined use of a specific foot bandage and therapeutic shoeing with a treatment plate is well documented for maggot debridement therapy [12]. In this study, 2 additional methods of bandaging were found to be efficient and were usually changed after 24 h. Based on the amount of secretions produced, these bandages were subsequently changed 2 or 3 times a day until removal of the maggots. If complete debridement of the wound does not occur or if there is evidence of a persistent infection, a second round of maggot debridement therapy is required. In the current study, no more than 2 maggot debridement therapy treatments were needed, which is unlike some previous reports in the literature [10]. Presumably, this difference was due to the preliminary light surgical debridement performed in most of the cases. In 3 cases, complete healing of the wound failed to occur. In one of these cases, healing occurred uneventfully after a bony sequestrum was removed. The other 2 cases were complicated by the presence of melanoma or squamous cell carcinoma in the wounds. From this retrospective study it is not possible to determine whether maggot debridement therapy accelerated wound closure compared with other forms of therapy. The equids in this study were presented with a) Fig 4: A fistulous withers donkey treated with maggot debridement therapy: red-brown exudate is commonly present after h of treatment. In the current study, the use of maggot debridement therapy was limited by the relatively high cost of treatment, time required for shipping and the fact that a portion of maggots failed to survive on arrival. However, after a 2-day shipment from the United Kingdom to Mali, more than 50% of the maggots were alive and able to debride, control infection and stimulate wound healing in warm weather. For example, maggot debridement therapy was successful in donkeys with fistulous withers including 2 cases involving onchocerca cervicalis (Fig. 4). The manufacturer advises that in a biobag, the presence of tiny pieces of foam within the net provides a physical environment that stimulates the activity and development of the maggots while assisting with exudate management [14]. However, the results of an in vivo study on 64 human patients with gangrenous or necrotic tissues suggest that better results were obtained when free range maggots were used instead of a biobag [15]. Our subjective assessment of the responses obtained in the current study is that the treatment of choice in equids is the direct contact technique with free range maggots, except when a very focal cavity or area is involved. An excellent outcome was obtained with maggot debridement therapy in a 3-week-old foal with MRSA infection over internal fixation materials used to stabilise a fracture. This positive outcome may have been related to a combination of a direct antibacterial effect of maggot debridement therapy and dissolution [12] and inhibition of biofilm formation [9]. It has been previously reported that excretions and secretions from Lucilia sericata have potent, thermally stable, protease resistant antibacterial activity against MRSA in vitro [16]. Although maggots are recommended for the treatment of wounds infected with Gram-positive bacteria, they are less active for wounds infected with Gram-negative bacteria, particularly Proteus spp. and Pseudomonas spp. strains [17]. However, it should be noted that a donkey with a severe localised multidrug-resistant, Pseudomonas aeruginosa and Escherichia coli infection was successfully treated with 6 applications of maggots [10]. In the current study, systemic administration of antimicrobials was discontinued during maggot debridement therapy to better assess the efficacy of this treatment. The results of one study [18] indicate that excretions/secretions from maggots result in a dose-dependent increase in the antibacterial effect of certain Equine Veterinary Journal 44, Suppl. 43 (2012) EVJ Ltd Fig 5: A 3-week-old foal with a methicilin-resistant staphylococcus aureus (MRSA) infection over an internal fixation device used in fracture repair. a) Before maggot debridement therapy, the dynamic compression plate (DCP) plate was visible in the wound after a loose screw had been removed. After 3 days treatment, all necrotic tissue has been replaced by granulation tissue and the DCP plate is no longer visible. 123

5 Maggot debridement therapy in equids O. M. Lepage et al. different types of lesions at different stage of healing. For example, some wounds had not been treated previously whereas others had received several treatments. However, in all cases, maggot debridement therapy was initiated approximately 48 h after the animal entered the clinic and healthy granulation tissue was present after 3 days of treatment. Based on these findings, we conclude that maggot debridement therapy can be recommended for debridement of wounds and its potent antibacterial effects, including the control of difficult infections such as MRSA or other multi-antibiotic resistant bacteria. Maggot debridement therapy can also be used to treat many types of lesions including complicated and deep lacerations, abscesses, abdominal wound dehiscence and infections even in the presence of internal fixation. However, maggot debridement therapy is not recommended for treatment of wounds occuring in association with neoplasia or if bone sequestration is suspected. Due to the actual cost associated with this form of therapy, maggot debridement therapy should be considered for lesions that fail to respond to conventional methods. Maggot debridement therapy potentially has an integral place in modern veterinary wound care but additional clinical studies are needed to assess its impact and value. Authors declaration of interests No competing interests have been declared. a) Fig 7: a) A chronic nonhealing wound on the dorsal aspect of the hock in an adult horse. Although debridement and cleaning of the wound occurred 3 days after light surgical debridement of the wound and maggot debridement therapy, underlying tissues were found to contain melanomas. Sources of funding None. a) Authorship O.M. Lepage was involved in experimental design, data acquisition, funding and manuscript preparation. A. Doumbia was involved in experimental design, data acquisition, and manuscript preparation. M.F. Perron-Lepage was involved in histology and manuscript preparation. M. Gangl was involved in data acquisition and manuscript preparation. Manufacturers addresses a ZooBiotic Ltd, Bridgend, England. b BSN medical, France. References Fig 6: a) Free range maggots after 2 days debriding a chronic heel bulb laceration; the net used to secure the maggots in place. 1. Jurga, F. and Morrison, S.E. (2004) Maggot debridement therapy. Alternative therapy for hoof infection and necrosis. Hoofcare & Lameness 78, Dumville, J.C., Worthy, G., Bland, J.M., Cullum, N., Dowson, C., Iglesias, C., Mitchell, J.L., Nelson, E.A., Soares, M.O. and Torgerson, D.J. (2009) Larval therapy for leg ulcers (VenUS II): randomised controlled trial. Br. Med. J. 19, Morrison, S.E. (2005) How to use sterile maggot debridement therapy for foot infections of the horse. Proc. Am. Ass. Equine Practnrs. 51, Lepage, O.M., Robert, M. and Doumbia, A. (2008) Biosurgery the comeback of maggot debridement. Proceedings 14th ESVOT Congress 14, Casu, R.E., Pearson, R.D., Jamey, J.M., Cadogan, L.C., Riding, G.A. and Tellam, R.L. (1994) Excretory/secretory chymotrypsin from Lucilia Cuprina: purification, enzymatic specificity and amino acid sequence deduced from mrna. Insect Mol. Biol. 3, Daeschlein, G., Mumcuoglu, K.Y., Assadian, O., Hoffmeister, B. and Kramer, A. (2007) In vitro antibacterial activity of Lucilia sericata maggot secretions. Skin Pharmacol. Physiol. 20, Prete, P.E. (1997) Growth effects of Phaenicia sericata larval extracts on fibroblasts: mechanism for wound healing by maggot therapy. Life Sci. 60, Cazander, G., Veen, K.E., Bouwman, L.H., Bernards, A.T. and Jukema, G.N. (2009) The influence of maggot excretions on PAO1 biofilm formation on different biomaterials. Clin. Orthop. Relat. Res. 467, Cazander, G., van de Veerdonk, M., Vandenbroucke-Grauls, C., Schreurs, M. and Jukema, G. (2010) Maggot excretions inhibit biofilm formation on biomaterials. Clin. Orthop. Relat. Res. 468, Equine Veterinary Journal 44, Suppl. 43 (2012) EVJ Ltd

6 O. M. Lepage et al. Maggot debridement therapy in equids 10. Bell, N. and Thomas, S. (2001) Use of sterile maggots to treat panniculitis in an aged donkey. Vet. Rec. 149, Fleischmann, W., Grassberger, M. and Sherman, R. (2004) Maggot Therapy: A Handbook of Maggot-Assisted Wound Healing, Georg Thieme Verlag, Stutgart. p Bras, R.J. and Morrison, S. (2009) Retrospective case series of 20 horses ( ) sustaining puncture wounds to the navicular bursa with maggot debridement therapy as an adjunctive treatment. Proc. Am. Ass. Equine Practnrs. 55, Pearson, C. (2007) Something old is new again: debriding and reducing local wound infection with maggots. Clin. Pract. Wound Care Can. 5, Lodge, A., Jones, M. and Thomas, S. (2006) Maggots n chips: a novel approach to the treatment of diabetic ulcers. Br. J. Community Nurs. Suppl. 11, Steenvoorde, P., Jacobi, C.E. and Oskam, J. (2005) Maggot debridement therapy: free-range or contained? An in-vivo study. Adv. Skin Wound Care 18, Bexfield, A., Nigam, Y., Thomas, S. and Ratcliffe, N.A. (2004) Detection and partial characterization of two antibacterial factors from the excretions/secretions of the medicinal maggot Lucilia sericata and their activity against methicillin-resistant Staphylococcus aureus (MRSA). Microbes Infect. 6, Jaklič, D., Lapanje, A., Zupančič, K., Smrke, D. and Gunde-Cimerman, N. (2008) Selective antimicrobial activity of maggots against pathogenic bacteria. J. Med. Microbiol. 57, Cazander, G., Pawiroredjo, J.S., Vandenbroucke-Grauls, C.M.J., Schreurs, M.W.J. and Jukema, G.N. (2010) Synergism between maggot excretions and antibiotics. Wound Repair Regen. 18, Equine Veterinary Journal 44, Suppl. 43 (2012) EVJ Ltd 125