Passive stretch of adult chicken muscle produces a myopathy remarkably similar to hereditary muscular dystrophy

doi:10.1016/0014-4886(88)90113-6

Experimental Neurology

Volume 100, Issue 2, May 1988, Pages 341-353

https://doi.org/10.1016/0014-4886(88)90113-6 Get rights and content

Abstract

The wings of 10 chickens between 1 and 5 years of age were passively extended. An increase in plasma creatine phosphokinase activity was observed in 30 min, continued to rise for 24 h, and then declined, suggesting mechanically induced damage to muscle fibers. Wing muscles were removed and examined histologically at various times after stretch. Patagialis muscles, but not biceps brachii, showed the development of muscle fiber pathology. The patagialis muscle is less active than the biceps brachii and is stretched to a greater degree by wing extension. Susceptibility of muscles to development of pathology appeared to be correlated with the age of the chickens. Pathology was remarkably similar to that observed in young chickens with hereditary muscular dystrophy. Necrotic fibers exhibiting segmental necrosis, abnormal shapes, enlargement, splitting, vacuolation, and phagocytosis were evident. Of particular interest was the appearance of abnormal clusters of acetylcholinesterase activity along the sarcolemma. These sites were shown to appear on fibers of 2-week-old dystrophic chicks prior to necrosis and increase in plasma creatine phosphokinase activity. It is suggested that aging of inactive muscles may promote adhesions between muscle fibers rendering them susceptible to damage when stretched and that necrosis of dystrophic fibers may be initiated by a similar mechanism. Such could occur if the genetic defect resulted in interfiber adhesions. Support for this hypothesis by other reports in the literature is discussed.

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Cited by (11)

Relationship between pectoralis major muscle histology and quality traits of chicken meat
2015, Poultry Science
Citation Excerpt :
The presence of muscle fibers of small caliber shown in correspondence of the abnormal fibers is a further histological appearance that supports the hypothesis of muscular disorder. Abnormal fibers surrounded by fibers of small caliber (also referred to as regenerative fibers) have been described in chickens and turkeys with various myopathies including dystrophy (Pizzey and Barnard, 1983; Ashmore et al., 1988; Sósnicki et al., 1989; Polak et al., 2009). In this study, many samples showed the presence of several muscle fibers with hyaline sarcoplasm and nuclei in the central position.
A trial was conducted to evaluate the influence of myodegeneration of pectoralis major muscle on quality traits and chemical composition of breast meat of heavy-size male broilers. For this purpose, a total of 72 pectoralis major muscles were randomly collected from broilers farmed under homogeneous conditions and graded into three categories (mild, n = 22; moderate, n = 33; and severe, n = 17) based on the presence of abnormal fibers (giant fibers, fibers with hyaline degeneration, and damaged and/or necrotic fibers) evaluated by histological and immunohistochemical analysis. Color, pH, drip loss, Allo–Kramer shear values, and chemical composition (moisture, proteins, total lipids, ashes, and collagen) were determined on nonmarinated breast meat. Purge loss and cook loss, total yield, and Allo–Kramer shear values were measured on vacuum-tumbled samples. Samples showing moderate myodegeneration had the highest mean cross-sectional area of the fibers, while samples with severe myodegeneration had myofibers of different diameter and without the characteristic polygonal shape, multifocal degeneration and necrosis, as well as infiltration of CD3-immunoreactive cells. Cooking losses of nonmarinated meat were lower in the mild group with respect to moderate and severe groups (21.4 vs. 24.7 and 24.7%; P < 0.001). Breast muscles with severe damage, in comparison with mild degenerated samples, showed higher moisture (75.4 vs. 74.4%; P < 0.05) and lower protein percentages (21.1 vs. 22.6%; P < 0.001). The lipid percentage of severely degenerated samples was higher than that from moderate group (2.94 vs. 2.36; P < 0.05), while collagen content was not modified by histological lesion levels. Marinated meat from the mild group had higher uptake and total marinade yield after cooking. In conclusion, almost all breast fillets of heavy broiler chickens produced under intensive farming systems had histological lesions, which reflected on the chemical composition of the meat and the impaired water holding/binding capacities of the meat.
Comparison of breast muscle traits and meat quality characteristics in 2 commercial chicken hybrids
2013, Poultry Science
Citation Excerpt :
These alterations were frequently accompanied by inflammatory infiltrate (lymphocytes, micro- and macro-phages) and necrosis of some muscle fibers; in the latter, a sarcoplasmatic vacuolation was sometimes identified. Histopathological anomalous features such as hypertrophy and modification of the muscle fiber profile, central nuclei, proliferation of endomysial and perimysial collagen, inflammatory infiltrate, and necrosis of the fibers, entirely because of what we have above mentioned, have been reported by several authors in chickens (Pizzey and Barnard, 1983; Ashmore et al., 1988; Ishimoto et al., 1988; MacRae et al., 2006; Polak et al., 2009; Nishita et al., 2012) and in turkeys (Sósnicki et al., 1989, 1991). The same authors mentioned above described how these histopathological changes accompanied by ultrastructural and enzyme abnormalities were identified as characteristic of congenital muscular dystrophy.
A trial was conducted to compare muscle traits and meat quality characteristics of the pectoralis muscle in 2 chicken commercial hybrids having standard (SBY) and high breast yield (HBY), respectively. A total of 2,124 one-day-old male chicks, equally divided into 2 experimental groups represented by strains (SBY and HBY), were grown using homogenous conditions and fed the same standard diets until reaching live weight of 4.2 kg at 53 and 55 d for the SBY and HBY groups, respectively. Thirty-six birds per each genotype were randomly selected, and their pectoralis major muscles were used to assess meat quality properties (color attributes, pH, drip loss, cook loss, Allo-Kramer shear values after cooking, moisture, proteins, total lipids, and ashes) as well as histological traits (cross-sectional area, frequency of abnormal fibers, and intramuscular fat infiltration). As expected, HBY genotype had higher breast yield (31.0 vs. 30.0%; P ≤ 0.05). Histological evaluations showed that HBY pectoralis muscles had higher cross-sectional fiber area coupled with a dramatically higher (P ≤ 0.001) incidence of abnormal fibers and more abundant infiltration of intramuscular fat. Moreover, histopathological anomalous features such as central nuclei, proliferation of endomysial and perimysial collagen, inflammatory infiltrate, and necrosis of the fibers were also observed. As for meat quality, SBY hybrid showed lower ultimate pH values (5.97 vs. 6.07; P ≤ 0.01), whereas overall color parameters were not affected by genotype. Breast meat from the HBY genotype also exhibited significantly lower ability to retain liquid during refrigerated storage (drip loss, 2.46 vs. 2.06%; P ≤ 0.05) and cooking (26.2 vs. 21.1%; P ≤ 0.05) as well as higher shear-force values (2.59 vs. 2.11 kg/g; P ≤ 0.001). Finally, with regard to chemical composition, significant differences (P ≤ 0.05) were detected in protein (22.8 vs. 23.5%) and lipid (1.65 vs. 1.82%) contents, which were significantly lower in the HBY hybrid, whereas moisture content tended (P = 0.07) to be inferior in the SBY hybrid.
Lack of effect of moderate-duration static stretching on plantar flexor force production and series compliance
2012, Clinical Biomechanics
Citation Excerpt :
Whilst previous research has been suggestive of neural mechanisms underpinning stretch-induced force decrements, the deficits could in fact result from structural disruption of the muscle cell. A moderate level of t-tubular and sarcoplasmic reticulum damage has been observed after passive stretch in both animal (Ashmore et al., 1988) and human muscle (Smith et al., 1993); disturbed calcium kinetics could impact muscle force production. Such a mechanism has been shown after damaging eccentric exercise in humans (Takekura et al., 2001), although it is not currently known whether this results from strenuous, but passive, muscle stretching.
The effects of an acute bout of moderate-duration static stretching on plantar flexor force production, series compliance of the muscle–tendon unit, and levels of neuromuscular activation were examined.
Eighteen active individuals (9 men and 9 women) performed four 45-s static plantar flexor stretches and a time-matched control of no stretch (where subjects remained seated in the dynamometer for 4 min with no stretch being performed). Measures of peak isometric moment, rate of force development, neuromuscular activation (interpolated twitch technique and electromyography), twitch force characteristics, passive moment during stretch, and tendon elongation during maximal voluntary contractions were taken before and after the stretching.
Despite a significant stress–relaxation response during stretch (9.3%, P < 0.01) there were no significant differences in peak isometric moment (P = 0.35; effect size 0.13), rate of force development (P = 0.93; effect size 0.01), neuromuscular activation (interpolated twitch: P = 0.86; electromyography: P = 0.09; effect size 0.02), or tendon elongation (P = 0.61; effect size 0.07) after stretching. Twitch characteristics were also unchanged after stretching, although there was a reduction in the rate of twitch torque relaxation (RR_t; P < 0.01).
The acute bout of moderate-duration static stretching did not impair the force generating capacity of the plantar flexors or negatively affect muscle–tendon mechanical properties. Static stretching may not always have detrimental consequences for force production. Thus, clinicians may be able to apply moderate-duration stretches to patients without risk of reducing muscular performance.
Regional injury and the terminal differentiation of satellite cells in stretched avian slow tonic muscle
1992, Developmental Biology
In the avian stretch model, the application of a weight overload to the humerus induces enlargement of the anterior latissimus dorsi (ALD) muscle and an increase in muscle fiber number which is accompanied by satellite cell activation. Myofiber injury may be an important stimulus to muscle fiber hyperplasia; therefore, light and electron microscopic evaluation was undertaken to determine if myofiber injury occurs in the stretch-enlarged ALD muscle of the adult quail. Autoradiographic studies were used to determine the terminal differentiation of labeled myogenic cells. A weight equal to 10% of body mass was attached to one wing of 27 adult quail and 3 birds were euthanized at 9 intervals of stretch, from 1 to 30 days. Birds were injected with tritiated thymidine at intervals ranging from 1 hr to 3 days prior to euthanization. Labeled nuclei were detected by light microscopic examination and identified by electron microscopy of a serial section. Three regions of the muscle were examined for disorganization of contractile elements, presence of cytoplasmic vacuoles, and/or phagocytic cell infiltration. The percentage of fibers exhibiting one or more of these criterion was significantly greater in the stretched ALD by Days 5 and 7 and declined at Day 10, reaching near control values by Day 14. Myofiber necrosis and phagocytic cell infiltration were only observed in the middle and distal regions of the stretched ALD muscle. Traditional signs of regeneration and repair were observed, including clusters of labeled myoblast-like cells and myotube formation within an existing basal lamina. New myotube formation with labeled central nuclei was also noted in the interstitial space, outside of basal lamina of persisting fibers. Labeled myonuclei were observed in the stretched fibers. These results demonstrate that chronic stretch produces regional injury and fiber degeneration and resultant regeneration in the ALD muscle of the adult quail. This may be an important stimulus for new fiber formation in this model.
An injury model myopathy mimicking dystrophy: Implications regarding the function of dystrophin
1991, Medical Hypotheses
The pathogenesis of dystrophin deficient myopathies remains unknown. Rat and human muscles subjected to severe injury following repeated eccentric muscle actions demonstrate histopathological alterations which mimic a dystrophic process. Immunofluorescent histochemical examination of these injured muscles demonstrates a separation of proteoglycans of the basal lamina from the muscle plasma membrane, the identical histopathological alteration observed in Duchenne muscular dystrophy. These findings are consistent with the hypothesis that dystrophin is essential for maintenance of the structural integrity of the sarcolemma.
Fatty acid composition of lipids in tongue and hindleg muscles of muscular dystrophic mice
1989, Journal of the Neurological Sciences
In order to understand the pathogenesis of mouse muscular dystrophy, fatty acid and lipid compositions in tongue and hindleg muscles of dystrophic mice were analyzed. The phospholipid contents in tongue and hindleg muscles were 71–73% and 23–24% of the total lipids, respectively. The content of triglyceride in tongue and hindleg muscles was 8% and 66% of the total lipids, respectively. There were no significant differences in the phospholipid content of the tongue or hindleg muscles between normal and dystrophic mice. However, analyses of the fatty acid composition in phospholipids showed that the content of 16:0 and 22:6 in the hindleg muscles of dystrophic mice decreased significantly, while the content of C-18 fatty acids (18:0, 18:1 and 18:2) increased. In addition, the fatty acid composition in phospholipids of tongues of dystrophic mice was identical to that of normal mice. This latter result supports the bone-muscle imbalance hypothesis for the pathogenesis of mouse muscular dystrophy.

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Passive stretch of adult chicken muscle produces a myopathy remarkably similar to hereditary muscular dystrophy

Abstract

Biochem. Med.

Exp. Neurol.

Exp. Neurol.

Exp. Neurol.

Biochem. Biophys. Res. Commun.

J. Neurol. Sci.

Comp. Biochem. Physiol.

Stretch-induced growth in chicken wing muscles: Effects on hereditary muscular dystrophy

J. Am. Physiol.

Phosphorylase in skeletal muscle of normal and selected lines of dystrophic chickens

Stretch-induced growth in chicken wing muscles: Nerve muscle interaction in muscular dystrophy

Am. J. Physiol.

Human growth hormone in myopathy

South. Med. J.