Introduction
In modern clinical practice within developed regions, patients with traumatic injuries can look forward to good outcomes thanks to high-quality care. However, the picture is quite different in developing countries, especially when natural or man-made disasters strike. They easily can overwhelm already fragile health care systems and challenge the capacity of national and international aid agencies to provide humanitarian relief. For example, six of the seven most deadly earthquakes between 2001 and 2011 occurred in low- or middle-income countries, directly affecting 58.2 million people.Reference Stadler, Shaban and Tatham 1 The global trend toward urbanization means that, in the event of disasters such as earthquakes, tsunamis, floods, or storms, a large number of people may be affected in a given locality. Typhoon Yolanda made landfall on November 8, 2013 and devastated Leyte, a relatively confined region of the Philippines, killing 6,293 and injuring another 28,689.Reference Zhang, Zhang and Liu 2 Similarly, when a magnitude 7.0 earthquake leveled Port-Au-Prince (Haiti) on January 12, 2010, three million people were killed, injured, displaced, or otherwise affected. 3 These statistics highlight an important consideration for the management and development of disaster relief medical surge capacity. There are, on average, approximately three times more injured than dead in an earthquake, and this may be similar in other disasters depending on circumstances.Reference Jobe 4 Self-evidently, it is the living wounded that require immediate attention and medical care.
Natural disasters damage a country’s built infrastructure including transport, communication, utility, and medical infrastructures.Reference Phalkey, Reinhardt and Marx 5 The resultant interruptions to the supply chains for medications and consumables can severely influence the care that is provided.Reference Chapin, Daniels and Elias 6 , Reference Chu, Stokes and Trelles 7 Indeed, even if regional clinics are operational, the patient burden may stretch resources beyond the breaking point, as exemplified by the 2004 tsunami in Thailand where those impacted were treated in hospitals that were unaffected structurally but lacked sufficient operating facilities, human resources, and equipment.Reference Missair, Pretto and Visan 8
Thus, despite a rapid and comprehensive deployment of national and international medical assistance teams, the number of patients requiring treatment can be overwhelming – even for the most experienced and best resourced agencies. Médecins sans Frontières (MSF; Geneva, Switzerland) treated over 55,000 Haitians in the 10 weeks after the 2010 earthquake, a figure that includes over 4,000 surgical interventions.Reference Chapin, Daniels and Elias 6 Indeed, although the total injury figures for this disaster vary widely, they are estimated by Doocy and colleagues to lie somewhere between 110,000 and 300,000.Reference Prasartritha, Tungsiripat and Warachit 9 In such compromised health care environments, wound care options are required that are relatively cheap, in ready supply, easy to use, and have multiple therapeutic benefits. Maggot debridement therapy (MDT), also known as larval debridement therapy, is one such option which may prove to be an invaluable tool in the treatment of complex wounds in the aftermath of disasters.
Current MDT practice employs the larvae of the green bottle blowfly Lucilia (Phaenicia) sericata Meigen (Diptera: Calliphoridae) to remove necrotic tissue from wounds, to control infections, and to stimulate tissue regeneration and wound healing; although, other species have been used successfully.Reference Doocy, Jacquet and Cherewick 10 , Reference Baer 11 In the 1930s and 1940s, MDT was used for the treatment of intractable wounds and osteomyelitis, but it fell out of fashion with the advent of sulphonamides, penicillin, and new antiseptics.Reference Sherman, Hall and Thomas 12 Over the past three decades, however, MDT has emerged once again as a treatment for chronic non-healing wounds, necrotic and infected trauma injuries, burns, and post-operatively complicated wounds.Reference Whitaker, Twine and Whitaker 13 - Reference Pechter and Sherman 17 Maggots are applied either in cage-like containment dressings that cover the wound and permit maggots direct access to necrotic tissue (free-range), or in small sealed pouches made of a porous material such as polyvinyl alcohol that allow maggots to feed and debride but not explore the wound freely.Reference Wollina, Karte and Herold 18
Some of the earliest accounts of beneficial wound infestations by maggots come from the battle fields of Napoleon’s Egyptian expedition in Syria (1798-1801) and the First World War (Europe; 1914-1918).Reference Doocy, Jacquet and Cherewick 10 The US Army Special Forces Medical Handbook from 1982 describes under the heading of “Primitive Medicine” how to use wild flies for infection control and debridement in the field;Reference Čičková, Čambal and Kozánek 19 although, the use of wild unsterilized fly eggs and maggots is a measure of last resort in the total absence of medical care, and under austere conditions. While modern military medical science has not yet refined and operationalized this therapy for deployment in the theatre of war, recent research at the Walter Reed Army Institute of Research (WRAIR; Silver Spring, Maryland USA), and elsewhere, is addressing this knowledge gap. For example, Heitkamp and colleagues surveyed 180 US Army physicians, and although 83% were aware of MDT, only 10% of them had ever used it. 20
In parallel, Peck and Kirkup investigated the effect of antimicrobials, including antibiotics and antifungals, on medicinal maggots.Reference Heitkamp, Peck and Kirkup 21 These researchers found that antimicrobials can be used in combination with MDT without diminishing the therapeutic activity of the medicinal maggots. Most relevant to the application of MDT in Disaster Medicine is the latest research emerging from the WRAIR where Peck and colleagues tested the resilience of medicinal maggots during transport in US military aircraft.Reference Peck and Kirkup 22 The authors have shown that medicinal maggots can withstand conditions that exist during military evacuation and transfer flights and could, therefore, be used in the treatment of wounds during the evacuation process. These results also suggest that medicinal maggots could be sent to disaster zones on a needs basis using military and other aircraft.
Given that military medical innovation often paves the way for civilian applications,Reference Peck, Helgeson and Powell 23 the research conducted at the WRAIR supports the fundamental contention of this report that the use of MDT in disaster medical aid has potential merit. Furthermore, a review of the literature, using five electronic databases (PubMed (National Center for Biotechnology Information; Bethesda, Maryland USA), CINAHL Plus with full text (EBSCO Information Services; Ipswich, Massachusetts USA), SCOPUS Life Sciences & Health Sciences (Elsevier; Amsterdam, Netherlands), ProQuest (Ann Arbor, Michigan USA), and Web of Science BIOSIS (Thomson Reuters; New York, New York USA)) from inception to December 2014, suggests that MDT in disaster medical aid has not been investigated previously.
Aim
With this introduction in mind, the aim of this study was to demonstrate how medicinal maggots could contribute to the treatment of intractable wounds in Disaster Medicine. To achieve this aim, the report consists of an overview of the wound burden of natural disasters, followed by a discussion of current treatment approaches for various injury categories, and the role medicinal maggots could play in their treatment. The report concludes with research gaps emerging from this initial investigation.
Report/Discussion
Disasters reflect a broad range of causalities that include the impact of earthquakes, tsunamis, floods, cyclones, typhoons and hurricanes, and man-made technology-related events. Wounds are a common consequence of disasters. Table 1 presents a summary of such disasters, their injury mechanisms, and resulting wound types.Reference Glassberg, Nadler and Erlich 24 - Reference Smith, Dyer and Antonangeli 52
Table 1 Common Disaster and Emergency Categories, Their Injury Mechanisms, and Resulting Wound Types
Abbreviation: LPG, liquefied petroleum gas.
The presence of necrotic devitalized tissue and wound infection are prime indications for the use of MDT in the clinical setting. It is safe to assume that this is also the case in an austere health care setting such as in the aftermath of disasters and other emergencies. Indeed, the ability of medicinal maggots to control the microbial burden in wounds under the most extreme conditions is remarkable, it suggests that MDT can debride wounds and stimulate wound healing under such circumstances, and it’s without the need to close wounds for fear of infection. For example, Terterov and colleagues document a case of human cerebral myiasis which, in all likelihood, saved the life of an assault victim.Reference Sato and Ichioka 53 The patient lay abandoned in a ditch for two weeks with severe facial injuries, including a skull fracture and maggot infestation of the left frontal lobe. To the surprise of the authors, the patient did not succumb to meningitis or encephalitis, and this they attributed to the antimicrobial properties of the maggots. It should be stressed, however, that the infestation of wounds by wild flies should be avoided, particularly if treating physicians are not familiar with medical entomology and alternative MDT species. This is because some fly species, like the New World screwworm Cochliomyia hominivorax, feed on living flesh, and if left in the wound, they would cause further harm.Reference Terterov, Taghva and MacDougall 54 Myiasis can also lead to additional contamination of the wound with fly-borne pathogens.Reference Lindsay, Stancil and Ray 55
Natural Disasters
In response to the devastating 2010 earthquake in Haiti, a US medical team sponsored by the nongovernmental organization “Partners in Health” (Boston, Massachusetts USA) was assigned to Hospital St. Nicholas in St. Marc, 80 miles outside the capital. In the first seven to eight days post-injury, the team performed critical soft tissue interventions and amputations. From day nine to day 14 after the quake, external fixations of fractures were undertaken. Surgical debridement and amputations were performed from day seven onward, as many patients had developed critical wound infections. Wound closures were performed from day 11 onward. Sepsis, compartment syndrome, and the presence of necrotic wounds were significant indicators of amputation. 51
In extremity crush and compartment syndrome, the decision to perform a fasciotomy appears to be influenced, in part, by the actual and perceived risk of wound infection and the danger of necrosis and muscle damage if the fasciotomy is not performed. Following the 1999 Marmara earthquake in Turkey, trauma to the extremities, and particularly the lower limbs, was most common.Reference Roudiere, Jean-Pierre and Comte 56 Crush syndrome resulted in high incidence of fasciotomy and amputation, but 24.8% of fasciotomies developed sepsis, while 13% of non-fasciotomized injuries also suffered sepsis. Moreover, late fasciotomies often have poor outcomes resulting in high infection and amputation rates.Reference Sever, Erek and Vanholder 57 Follow-up complications from infection in a crushed limb after fasciotomy are considered worse than muscle fibrosis and contracture. 51 , Reference Ritenour, Dorlac and Fang 58 Fasciotomy is contraindicated when compartment syndrome in closed lower limb injuries exists for more than eight to 10 hours. Instead, conservative treatment of late compartment syndrome is recommended to preserve skin and avoid infection. Any corrective surgery and late excision of necrotic muscle can occur at a later date.Reference Ritenour, Dorlac and Fang 58 However, experience with combat patients suggests that fasciotomy revisions and delayed compartment release is associated with a significant increase in mortality, a two-fold increase in amputation, and a three-fold mortality rate.Reference Sever, Erek and Vanholder 57 With respect to the management of a fasciotomy wound, Duman and colleagues advocate monitoring for infection, timely debridement, antibiotic treatment, and amputation if necessary,Reference Finkelstein, Hunter and Hu 59 while the consensus view advises against amputation of crushed limbs.Reference Duman, Kulahci and Sengezer 60
Maggot debridement therapy can control some wound infections and associated necrosis successfully and could play an important part in the prevention of amputation when fasciotomy has been performed. MacDougall and Rodgers document the successful treatment of a non-healing fasciotomy wound with MDT in the community setting.Reference Greaves and Porter 61 Maggot debridement therapy also has been highly successful in the treatment of postsurgical wound infection after scoliosis correction.Reference MacDougall and Rodgers 62 Consequently, infection concerns may not influence the decision to perform a fasciotomy if MDT was freely available to treat some wound complications. It follows that MDT could support both the decision to perform an emergency or a delayed fasciotomy. This is because infections can be treated successfully with MDT, as well as tissue necrosis in compartment syndrome, where fasciotomy has been performed too late or not at all. Indeed, compartment syndrome may no longer be considered a limb-threatening injury because the window for effective surgical treatment and limb salvage has become much larger with MDT.
The option to apply maggots directly or in bags also allows for a tailored application, depending on which wound closure strategy is used. Vacuum-assisted closure (VAC) has been used to assist in the closure of fasciotomy wounds.Reference Hwang, Modi and Suh 63 However, it is unlikely that VAC will be available widely to responders of mass-casualty disasters unless they receive patients in well-equipped regional hospitals; even there, the high patient load may outstrip the availability of specialized equipment. Other standard treatment modalities are saline-soaked gauze packing and the application of dermatotraction,Reference Saziye, Mustafa and Ilker 64 , Reference Eid and Elsoufy 65 and it appears that maggots are quite compatible with the latter treatment options. Indications for the use of bagged maggots suggest they may be used in open fasciotomy wounds either in combination with, or in place of, saline-soaked gauze. Debridement of necrotic tissue and control of infection in wounds obstructed by dermatotraction systems is probably best achieved with maggots that are applied directly into the wound (free-range) and are contained by a cage-like dressing. In this case, periodic removal of maggots would be simply a matter of irrigating the wound with saline. Furthermore, free-range MDT would allow the dermatotraction device to remain in place and maintain wound closure gains while necrosis and infection is treated. In addition, free-range maggots have been shown to be more effective in debriding necrotic tissue, particularly in wounds with uneven wound edges, undercuts, and a complex mix of necrotic and viable tissue.Reference Matt, Johnson and Shupp 66 , Reference Steenvoorde, Jacobi and Oskam 67
The limb-saving potential of MDT is not restricted to fasciotomy wound management. Severe injuries to limbs are often deemed unsalvageable under austere conditions, but case reports of successful interventions with MDT, including extreme degloving injuriesReference Thomas, Wynn and Fowler 68 , Reference Chan, Hussain and Milovic 69 and chronic infections,Reference Husain and Fallat 70 demonstrate that MDT can debride extensive necrosis and effectively control wound infections and save limbs. Consequently, MDT has the potential to reduce the amputation rate in victims of disasters.
Premature closure of wounds sustained in disasters is not desirable but happens too often.Reference Missair, Pretto and Visan 8 , Reference Benedict and Park 31 , Reference Mumcuoglu, Ingber and Gilead 71 For example, many of the Swedish citizens injured in the 2004 tsunami required further corrective treatment upon their return to Stockholm (Sweden). Primary closure performed in Thailand had to be reversed, and wounds had to be excised and left open for delayed closure.Reference Benedict and Park 31 Because MDT targets only dead necrotic tissue, it ideally is placed to precisely debride complex wounds with a mixture of viable and necrotic tissue in the case of unsuccessful premature closure.Reference Doung-ngern, Vatanaprasan and Chungpaibulpatana 72
Moreover, the effects of natural disasters typically impact survivors many months after. Latent or complicating infections with progressing and migrating abscesses have occurred due to mycobacterial and fungal infection.Reference Benedict and Park 31 While large wounds pose the highest risk of infection, small scratches, punctures, pricks, and lacerations also allow bacterial and fungal pathogens to pass the skin barrier, and these can cause severe infection of underlying tissues. Such minor wounds can deteriorate within days and become life-threatening sources of sepsis.Reference Missair, Pretto and Visan 8 Maggot debridement therapy has been used successfully in the treatment of such cases in a non-disaster context. For example, Chaffey documents the treatment of a small insect bite that deteriorated and led to a severe infection and tissue necrosis on the leg.Reference Fenn-Smith 73 Maggot debridement therapy successfully debrided the wound and promoted granulation and healing.
Pressure wounds are a little-recognized, secondary injury source in sudden-onset disasters and may affect the geriatric population, the disabled, and the immobilized wounded. Impaired mobility is the primary cause for pressure ulcers.Reference Wolbarst, Wiley and Nemhauser 50 Victims of disasters that suffer spinal cord injuries, or any other injury that restricts mobility, are also at high risk of developing pressure ulcers.Reference Benedict and Park 31 Moreover, because of the austere conditions prevailing in the aftermath of disasters, the immobilized victims may necessarily rest on hard and unsuitable surfaces which can contribute to the development of pressure ulcers. 51
This potential source of injury is exacerbated by the likelihood of interruptions to power supplies and supply chains for health care provision. This was evident in the aftermath of the Great East Japan (Fukushima) Earthquake in 2011 when there was a surge of elderly people in home care and evacuation centers developing pressure ulcers. Alternating-pressure air mattresses failed without power, and other devices for pressure ulcer prevention could not be distributed in time.Reference Smith, Dyer and Antonangeli 52 Of course, the best treatment for pressure ulcers is prevention, but it appears unlikely that pressure ulcers can be avoided altogether when disaster strikes.
Maggot debridement therapy should be considered for the treatment of pressure ulcers in austere settings and in response to a surge in the incidence of pressure ulcers in the community. Sherman reports complete debridement in 80% of pressure wounds treated with MDT, while in the same study, only 48% debridement was achieved with traditional wound care methods. Sherman also notes the rapid growth of granulation tissue, which is a vital sign of healing and tissue regeneration.Reference Chaffey 74 Importantly, in a disaster situation, it is unlikely that pressure ulcers will receive focused attention from surgeons who would, in all probability, be concerned with more pressing interventions. Access to MDT would, thus, allow non-physician health care workers to take the lead in debridement of pressure ulcers and infection control.
Technological Disasters
As far as technological disasters, such as building collapses and mass transport accidents, are concerned, many of the injuries are likely to be similar to those sustained in natural disasters. However, there are injury categories unique to particular human activities. Some of the most catastrophic man-made disasters involve industrial explosions - particularly gas, oil, and petroleum explosions.Reference Wachira and Smith 35 , Reference Arturson 36 , Reference Woltering and Schneider 38 Likewise, the impact of the two atomic bombs detonated over Hiroshima and Nagasaki (Japan) suggests that a thermo-nuclear attack on any densely populated center would have catastrophic consequences with thousands of victims suffering from severe burns and complex trauma.
Burns are among the most challenging injuries encountered and demand significant health care resources if the patients’ clinical needs are to be met and suffering is to be minimized.Reference Sherman 75 Of immediate concern are fluid-loss or shock, as well as airway obstruction and immune-compromise, and coincidental trauma, while escharotomies may be necessary to prevent further tissue damage.Reference Atiyeh, Gunn and Dibo 76 The risk of bacterial and fungal infection of burn wounds is also significant.Reference Jeng, Gibran and Peck 77 , Reference Branski, Al-Mousawi and Rivero 78 The disaster impact itself introduces dirt and debris into the wound and leaves large amounts of dead tissue. Extensive burns continue to be vulnerable to contamination during first aid, emergency fasciotomy or escharotomy,Reference Struck and Gille 79 and during burn care at the hospital.Reference Kennedy, Brammah and Wills 80 Once the patient is stabilized, infection prevention is initiated and includes whole body cleaning, shaving, and microbiological monitoring. Surgical debridement under general anaesthesia is performed to prepare the wound for skin grafting.Reference Branski, Al-Mousawi and Rivero 78 After a pipeline explosion in Abule-Egba, Nigeria, badly burnt patients were treated at Lagos State University Teaching Hospital (Ikeja, Lagos, Nigeria). Wound care included escharectomies and escharotomies, scrubbing, closed wound dressings, monitoring of microbial load, tailored antibiotics, skin grafting, and contracture release.Reference Carlson, Rogers and Kamara 40
In mass burn disasters, analgesics, anaesthetics, and antibiotics may not be available, or may be in short supply, particularly in austere health care settings and resource-constrained, low-income countries. In such settings, patients may benefit from MDT as it has proven to be effective in the treatment of burns.Reference Hassen, Khalifa and Raddaoui 81 - Reference Namias, Varela and Varas 83 The ability of maggots to perform extensive debridement equal to surgical intervention has been demonstrated by Akhtar and colleagues who had success in debriding full thickness burns in patients that were not fit for anaesthesia and surgery.Reference Thornton, Berry and Ralston 84 Likewise, Namias and colleagues achieved remarkable recovery of fourth degree burns to both legs with MDT.Reference Edwards 82 In China, MDT has been used to treat a patient with horrendous hot-crush injuries,Reference Akhtar, Abdel-Rehim and Rodrigues 85 where Li and colleagues used Musca domestica, a species of fly not normally used in MDT, but achieved good results with complete debridement and wound closure.
The affected body surface area in disaster burn victims is often extensive, which makes the application of MDT dressings difficult. To overcome this problem, Felder and colleagues modified VAC technology to accommodate medicinal maggots.Reference Li, Lu and Huo 86 According to these authors, this technology allows coverage of irregular and extensive wound areas and may be used for the removal of extensive burn eschar. Moreover, they suggest that such a combined VAC/MDT dressing may be applied to wounds without prior sharp debridement due to the unique wound-healing properties of medicinal maggots. This would facilitate the rapid treatment of mass casualties in burn disasters greatly. However, the use of VAC technology might be problematic in austere environments due to the need for reliable power supply to run vacuum pumps.
Conclusion
Natural and man-made technological disasters will remain an ongoing concern for the international emergency and disaster management community. Such events frequently lead to a surge of casualties that can overwhelm first responders and medical assistance teams. While waiting for treatment, patients can deteriorate rapidly and limbs may be amputated prematurely for fear of sepsis. Victims may also present late with neglected and infected wounds. The standard approach to such complex traumatic wounds and wound infection is surgical debridement, but this is time consuming and has to be performed by trained physicians. Furthermore, antibiotics may not be effective in controlling resistant infections. Consequently, wound care options are needed that are efficacious, can free up physicians to perform vital surgical interventions, and allow nurses to manage wound debridement and infection control – regardless of the clinical environment, location, or patient burden.
With this in mind, it is suggested that MDT could play a significant role in meeting this wound care need in disaster medical aid. Maggot debridement therapy is highly precise, provides infection control against a broad spectrum of microbes, stimulates healing, and prepares the wound bed for grafting or closure. In addition, MDT can be performed by nurses without the need of a physician.
However, there are social, medical, and logistic hurdles to be overcome before MDT can be added to the tool box of disaster medical aid teams. For instance, there remains an aversion among the medical profession to the use of maggots in wound care, and a belief that current approaches to wound care are appropriate. 20 Therefore, it is argued that the benefits of MDT in trauma care should be further explored. To this end, physicians and nurse practitioners are encouraged to publish case reports of successful maggot therapy in trauma care. In addition, research is needed to support the establishment of reliable supply chain networks for MDT and to understand (and, where possible, overcome) the logistic barriers that may prevent the successful use of MDT.
