Study contribution

Capture myopathy is a disease that occurs in different animals worldwide, such as wild mammals and birds. This is a pathology probably induced by stress, which cause damage to the myofibers, that can render a bird unable to stand, walk or fly, in addition to inducing alterations in certain blood clinical biochemistry parameters like creatine kinase and aspartate aminotransferase enzymes. The aims of this study were to collect, summarize and classify taxonomic information, clinical signs, diagnostic methods, and treatments described in the literature about capture myopathy in wild birds performing a systematic review and is intended to be a reference material for students and professionals who work with these animals in clinical practice.

Introduction

Capture myopathy (CM) is a multifactorial disease associated with the capturing and handling of certain species of wild mammals and birds which can occur secondarily to other pathologies.^1,2 It is a condition with worldwide distribution, with marked morbidity and mortality and their predisposing factors include specific environmental conditions (e.g., high temperature and humidity), capture techniques that induce exacerbated stress response in the animal, prolonged immobilization times, and underlying diseases that compromise the animal’s health.^3,4 The disease has implications for the survival of the individuals, and this is very relevant, for example in endangered species.⁵

CM causes muscle tissues to break down, making it difficult for birds to stand, walk, or fly.⁶ Four different forms of the disease have been described: 1) hyperacute, characterized by sudden death due to heart failure after a short period (minutes), 2) acute, less severe, characterized by muscle rupture, ataxia, and death within 24-48 hours, 3) subacute, less severe, characterized by muscle and kidney damage, and death after a few days, and 4) chronic: characterized by survival for several days or months, followed by sudden death from a heart attack.⁷

McEntire and Sánchez⁸ indicated that stress and undue fear are two of the most important factors contributing to CM. The authors observed that many birds experience stress when they enter a veterinary hospital setting, which can lead to them moving excessively. This additional movement causes muscle damage and prevents its regeneration. The extreme and prolonged stress response is associated with increased catecholamines, cortisol, and aldosterone blood levels, potentially damaging cardiac and skeletal muscles. It has been suggested that ischemia and reperfusion may play a central role in CM through stress-induced muscle necrosis.⁹

The pathogenesis of CM is not fully understood, but it is believed to be caused by the anaerobic oxygen-free metabolic pathway, which is associated with intense muscular activity. Anaerobic metabolism ends with lactic acid accumulation, which leads to severe metabolic acidosis and secondary muscular necrosis.^10,11 When muscles work at high intensity, they consume oxygen faster than the blood can deliver, resulting in oxygen deficiency. In the absence of oxygen, the muscles produce lactic acid as product instead of carbon dioxide. If lactic acid accumulates in muscle cells, it destroys their cell membranes, causing muscle damage characterized by the release of the cell content.¹⁰ When muscles are injured, the basal membrane and the sarcolemma of myofibers release cytoplasmic components such as myoglobin and creatine kinase into the bloodstream, generating an increase in their levels in the blood.^12,13

This systematic review aims to 1) give taxonomic information regarding some species of wild birds that have been reported to have CM, according to the literature, 2) describe the clinical signs associated with CM in wild birds, 3) identify the methods used to diagnose CM, and 4) summarize different treatments for CM in wild birds.

Materials and methods

Data extraction

Information regarding the taxonomy of the birds described (family, genus, and specie), clinical signs specified for CM according to the species of birds were extracted from each publication selected. Creatine kinase and aspartate animotransferase levels and the described reference values were also recorded, as well as necropsy findings (macroscopic and microscopic lesions, type of sample and species of bird where these findings were described). Finally, treatments reported in the literature for CM (fluid therapy, anti-inflammatories, vitamin treatments, mineral supplement treatments, central nervous system depressant drugs, pH control treatment, forms of rehabilitation and physiotherapy) were also compiled. The PRISMA statement (Preferred Reporting Items for Systematic Reviews and Meta-Meta-analyses)¹⁶ was followed to write this study.

Results

Bibliographic search

In the bibliographic search, 548 potentially eligible articles were identified in the databases and the search engine, of which 241 remained, and 210 were retrieved by the exclusion criteria. Finally, 31 studies were completely analyzed and 19 were excluded through the critical analysis, leaving a total of 12 documents chosen for the systematic review (Figure 1).

Figure 1 Flow chart for study selection. 

The Table 1 provides a summary of the 12 documents that were included in this systematic review, indicating the author(s), journal, year of publication, country where the study was conducted, type of publication, and database or search engine where the reference was found.

Table 1 Studies for this systematic review 

Author(s)	Year	Journal	Country	Type of publication	Database/ search engine
McEntire and Sánchez8	2017	Journal of Avian Medicine and Surgery	USA	Scientific article	EBSCOhost
Hurtado et al.17	2021	Journal of Avian Medicine and Surgery	Brazil	Scientific article	EBSCOhost
Businga et al.18	2007	Journal of Avian Medicine and Surgery	USA	Scientific article	EBSCOhost
Höfle et al.19	2004	Wildlife Society Bulletin	Spain	Scientific article	EBSCOhost
Hanley et al.20	2005	Journal of Zoo and Wildlife Medicine	USA	Case report	EBSCOhost
Hayes et al.21	2003	Journal of Wildlife Diseases	USA	Scientific article	PubMed
Ward et al.1	2011	Journal of Wildlife Diseases	New Zealand	Scientific article	Google Scholar
Rogers et al.22	2004	Journal of Field Ornithology	Australia	Scientific article	Google Scholar
Finlay y Jeske23	1999	Wildfowl	USA	Scientific article	Google Scholar
Dunne and Miller24	2009	Conference proceeding	USA	Case report	Google Scholar
Tully et al.25	1996	Journal of Avian Medicine and Surgery	USA	Scientific article	Google Scholar
Carpenter et al.26	1991	Journal of Zoo and Wildlife Medicine	USA	Scientific article	Google Scholar

Discussion

CM accounts with a considerable frequency of deaths associated with wildlife, which have considerable impacts on conservation efforts.⁴ The present study was aimed at analyzing, organizing, and synthesizing relevant literature information about CM in wild birds. The data collected was then used to describe the clinical signs associated with CM, diagnostic biochemical analyses, and postmortem examination. Finally, treatments applied in different studies were analyzed. The current number of studies examining CM in wild birds is limited. However, Hayes et al.²¹⁾ observed that CM has been well-studied in mammals, suggesting that there is a need for further research on this disease in birds.

Taxonomic classification of birds suffering from CM (Table 2) revealed that certain families and species were overrepresented. The studies recovered in the literature were conducted in countries such as the United States and Australia, and there are not many studies on CM in Latin America, which does not mean that the disease is not present in this region. In this regard, McEntire and Sánchez.⁸⁾ suggested that long-legged wading birds are especially susceptible to CM, pointing to cases in different flamingo species, including the Chilean flamingo (Phoenicopterus chilensis).

The studies included in this review found that the most common clinical signs of CM in wild birds were the inability to sit up, ataxia, paresis, and paralysis (Table 3). This is consistent with the findings of Ward et al.,¹ who suggested that these clinical signs are associated with reduced muscle function as a result of the physiological cascade of CM initiated by hyperthermia, anaerobic glycolysis, metabolic acidosis, decreased tissue perfusion, and hypoxia.¹² The antemortem diagnosis of CM in wild birds was performed by assessing the clinical history, clinical signs, and concentration of muscle enzymes. As shown in Table 4, CK and AST levels have been traditionally used to diagnose muscle disorders or injuries.

Hanley et al.²⁰ indicated that although the biochemical evaluation of muscle enzymes is useful for diagnosis, it does not seem valuable for prognosis, as enzyme values can take weeks to return to normal reference ranges. The physiological cascade of CM can be initiated by increased muscle contractions and lactic acid buildup during the capture, a process that ultimately leads to cell lysis and the release of CK and AST enzymes into the blood.²⁸ Indeed, high levels of these enzymes in the blood have been suggested to be an index of muscle damage in mammals and birds.²⁹ Consistent with this, biochemical analyses revealed increased CK and AST levels in the included species compared to physiological levels.

West et al.³⁰ highlighted the importance of postmortem diagnosis by necropsy and histopathology in CM. The post-mortem signs of CM may include dark red, enlarged kidneys, and an empty or reddish-brown fluid in the bladder. The flexor and extensor muscles of the hindlimbs may show soft, pale, dry areas with central white foci. This is a sign of severe muscle necrosis, a hallmark of CM.³¹ Myonecrosis was also described as one of the main histopathological hallmarks in CM muscles. Subacute and chronic CM manifestations were distinguished by sarcolemma proliferation, muscle regeneration, and fibrosis.^12,32

The treatment for CM is complex due to the multifactorial nature of the disease. It revolves around the early administration of fluid therapy, steroidal and nonsteroidal anti-inflammatory drugs, sodium bicarbonate, vitamin E, and selenium (Table 6). The use of vitamin E combined with selenium has been reported to help reduce free radicals from the muscle. For example, Paterson et al.³² reported an association between the survival of the Virginia quail (Colinus virginianus) population and the treatment with vitamin E and selenium after capture. Central nervous system depressants, such as diazepam, have also been used as support therapy in birds recovering from CM. Diazepam is a benzodiazepine drug that can minimize stress at low doses.

Hurtado et al.¹⁷ reported that benzodiazepines are particularly useful during the last stages of rehabilitation in seabird species. Benzodiazepines can help to reduce physiological stress associated with the regurgitation process and self-inflicted injuries in the veterinary setting. Haloperidol, midazolam, and methocarbamol have been reported to have some effectiveness against myopathy in wild birds. McEntire and Sánchez⁸ highlighted the importance of using these tranquilizers to keep the bird calm enough to be handled and fed regularly with an esophageal tube during its recovery. The efficacy of these drugs is variable and depends on the dose administered and the bird species. Moreover, the success of the treatment will also depend on the initial care after the development of the disease and the intensive support during the recovery phase.

A treatment protocol for wild birds admitted to wildlife rehabilitation centers is needed. This study proposes to develop a protocol focused on stress control, minimizing handling, and using CNS depressants to generate muscle relaxation and reduce stress in the bird while it recovers during the hospitalization phase. The course of the bird’s recovery should be managed with a combination of treatments, including treatment of the root cause of the pathology, fluid therapy (e.g., lactated Ringer’s solution), anti-inflammatories and supplementation with vitamin E and selenium^18,20,21,24. Cage rest, with a sling, may be important in myopathy therapies. This helps to immobilize the individual and prevent muscle contractions, which can help to support a successful recovery (Table 7). The use of physiotherapy (Table 8), compresses, flexion, and extension movements in the hind limbs can further help birds with CM to regain muscle mass and start the recovery process until animals are released.^8,18,20,24

Conclusions

CM in wild birds is a complex disease from clinical, diagnostic, and therapeutic standpoints, with a multifactorial etiology that frequently occurs in clinical practice. Wildlife specialists must be aware of the complex nature of CM and the challenges of diagnosing and treating it. They should adopt a preventive approach, especially in birds of families Scolopacidae, Gruidae, and Anatidae, where the disease has been more frequently described. The clinical signs associated with CM are not always indicative of the disease. However, their identification is important for a correct diagnosis, which should be conducted by considering the clinical manifestation of CM and blood biochemical analyses.

The stress response of birds to capture and handling is a major factor in the development of CM. Therefore, reducing stress reactions could help to prevent the disease. Alternatively, the presence of enzymatic indicators in blood samples can be a useful diagnostic tool in clinical pathology to evidence whether an individual is suffering from the condition. In birds, postmortem diagnosis of CM can be performed by examining pectoral, gastrocnemius, and leg muscles. The most frequent macroscopic lesions are associated with changes in the coloration of the muscle tissue and the observation of hemorrhagic areas. Microscopic lesions can also be observed in skeletal muscle fibers, which can progress to necrosis and loss of the structural conformation of the muscle and organs.

The treatment for CM is complex and requires a comprehensive approach. It should include preventive measures, as well as different types of management approaches, drugs, and physiotherapy. The publicly available information on CM in wild birds is scarce, with most published data coming from the United States and Australia. There is limited research on CM in Latin America. Therefore, further national and/or local studies of this disease in Latin American countries should be undertaken. This systematic review provides a baseline of information for future research and as reference material for students, professionals, and wildlife rehabilitation centers.