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Pathology of muscular steatosis in the bovine species: report of two spontaneously arising cases and comparative overview of the condition

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Abstract

Muscular steatosis, a condition characterized by prominent fatty replacement of skeletal muscles, has been known from a long time ago to mainly involve meat animals, such as pig, sheep, and cattle. Although a variety of hypotheses are proposed for explaining the condition, its etiology and pathogenesis are still poorly understood. Spontaneously occurring lesions of muscular steatosis were recognized in two 2-year-old steers that were slaughtered for food. Significant clinical abnormalities indicative of motor dysfunction were not observed in these animals. Postmortem examination revealed a remarkable and bilaterally symmetrical deposition of adipose tissue in the semitendinosus muscle of one steer and the gluteus muscle of the other steer. Affected muscles were of normal volume but exhibited an irregularly streaked appearance due to ill-proportioned fat infiltration. On histopathology, the lesioned muscles were extensively replaced by much adipose tissue, showing complete loss of muscle fibers in some fascicles. Structure of the perimysial connective tissue network was well preserved. All fat cells did not exhibit immature morphology but were of a well-differentiated mature appearance. Although a small number of muscle fibers represented atrophic or degenerative changes, regenerative muscle fibers and proliferation of the perimysial connective tissue were not demonstrated elsewhere in the lesions. Intramuscular blood vessels and nerves showed no significant changes. Precise pathogenesis of muscular steatosis, such as that found in these steers, remained uncertain. These fatty muscular lesions were distinguished from those of advanced or end stages in previously described muscle disorders in cattle, including neurogenic muscular atrophy, nutritional myopathy, or muscular dystrophy. The present article makes a comment on the pathology of muscular steatosis involving the bovine species from the comparative viewpoint.

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References

  • Abutarbush SM, Radostits OM (2003) Congenital nutritional muscular dystrophy in a beef calf. Can Vet J 44:738–739

    PubMed  PubMed Central  Google Scholar 

  • Addison O, Marcus RL, LaStayo PC et al (2014) Intermuscular fat: a review of the consequences and causes. Int J Endocrinol 2014:11

    Article  Google Scholar 

  • Agerholm JS, Basse A (1994) Spinal muscular atrophy in calves of the Red Danish dairy breed. Vet Rec 134:232–235

    Article  CAS  PubMed  Google Scholar 

  • Aström KE, Adams RD (1981) Pathological reactions of the skeletal muscle fibre in man. In: Walton J (ed) Disorders of voluntary muscle, 4th edn. Churchill Livingstone, Edinburgh, pp. 51–298

    Google Scholar 

  • Biasibetti E, Amedeo S, Brugiapaglia A et al (2012) Lipomatous muscular ‘dystrophy’ of Piedmontese cattle. Animal 6:1839–1847

    Article  CAS  PubMed  Google Scholar 

  • Billin AN, Bantscheff M, Drewes G et al (2016) Discovery of novel small molecules that activate satellite cell proliferation and enhance repair of damaged muscle. ACS Chem Biol 11:518–529

    Article  CAS  PubMed  Google Scholar 

  • Bodine-Fowler S (1994) Skeletal muscle regeneration after injury: an overview. J Voice 8:53–62

    Article  CAS  PubMed  Google Scholar 

  • Bradley R, Fell BF (1981) Myopathies in animals. In: Walton J (ed) Disorders of voluntary muscle, 4th edn. Churchill Livingstone, Edinburgh, pp. 825–872

    Google Scholar 

  • Bruno C, Dimauro S (2008) Lipid storage myopathies. Curr Opin Neurol 21:601–616

    Article  CAS  PubMed  Google Scholar 

  • Climie ARW, Chason JL (1977) Diseases of skeletal muscle. In: Anderson WAD, Kissane JM (eds) Pathology, 7th edn. CV Mosby, Saint Louis, pp. 2055–2073

    Google Scholar 

  • Costagliola A, Wojcik S, Pagano TB et al (2016) Age-related changes in skeletal muscle of cattle. Vet Pathol 53:436–446

    Article  CAS  PubMed  Google Scholar 

  • d’Amati G, di Gioia CRT, Giordano C et al (2000) Myocyte transdifferentiation. A possible pathogenetic mechanism for arrhythmogenic right ventricular cardiomyopathy. Arch Pathol Lab Med 124:287–290

    PubMed  Google Scholar 

  • Dalakas MC, Hohlfeld R (2003) Polymyositis and dermatomyositis. Lancet 362:971–982

    Article  CAS  PubMed  Google Scholar 

  • Dirksen G, Doll K, Hafner A et al (1992) Spinal muscle atrophy in Brown Swiss x Braunvieh cross calves. Dtsch Tierarztl Wochenschr 99:168–175

    CAS  PubMed  Google Scholar 

  • Doig PA (1970) Muscular dystrophy in yearling cattle. Can Vet J 11:24–25

    CAS  PubMed  PubMed Central  Google Scholar 

  • el-Hamidi M, Leipold HW, Vestweber JG et al (1989) Spinal muscular atrophy in Brown Swiss calves. Zentralbl Veterinarmed A 36:731–738

    Article  CAS  PubMed  Google Scholar 

  • Emslie-Smith AM, Engel AG (1990) Microvascular changes in early and advanced dermatomyositis: a quantitative study. Ann Neurol 27:343–356

    Article  CAS  PubMed  Google Scholar 

  • Estruch R, Grau JM, Fernández-Solá J et al (1992) Microvascular changes in skeletal muscle in idiopathic inflammatory myopathy. Hum Pathol 23:888–895

    Article  CAS  PubMed  Google Scholar 

  • Furuoka H, Doi T, Nakamura N et al (1995) Hereditary myopathy of the diaphragmatic muscles in Holstein-Friesian cattle. Acta Neuropathol 90:339–346

    Article  CAS  PubMed  Google Scholar 

  • Ganjali H, Ganjali M (2013) Fixation in tissue processing. Intl J Farm & Alli Sci 2:686–689

    Google Scholar 

  • Goedegebuure SA (1987) Spontaneous primary myopathies in domestic mammals: a review. Vet Q 9:155–171

    Article  CAS  PubMed  Google Scholar 

  • Goedegebuure SA, Hartman W, Hoebe HP (1983) Dystrophy of the diaphragmatic muscles in adult Meuse-Rhine-Yssel cattle: electromyographical and histological findings. Vet Pathol 20:32–48

    Article  CAS  PubMed  Google Scholar 

  • Gotoh T, Albrecht E, Teuscher F et al (2009) Differences in muscle and fat accretion in Japanese black and European cattle. Meat Sci 82:300–308

    Article  CAS  PubMed  Google Scholar 

  • Hadar H, Gadoth N, Heifetz M (1983) Fatty replacement of lower paraspinal muscles: normal and neuromuscular disorders. Am J Roentgenol 141:893–895

    Article  Google Scholar 

  • Hadlow WJ (1962) Diseases of skeletal muscle. In: Innes JRM, Saunders LZ (eds) Comparative neuropathology. Academic Press, New York and London, pp. 147–243

    Chapter  Google Scholar 

  • Hamaguchi Y, Kaido T, Okumura S et al (2016) Muscle steatosis is an independent predictor of postoperative complications in patients with hepatocellular carcinoma. World J Surg. doi:10.1007/s00268-016-3504-3

    PubMed  Google Scholar 

  • Hartigan PJ, Flynn JA (1973) An unusual form of lipoma in cattle: multiple subcutaneous tumours in the dewlap. Vet Rec 93:536–537

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto Y, Osaka T, Fukuda T (2016) The relationship between hepatic steatosis and skeletal muscle mass index in men with type 2 diabetes. Endocrine J 63:877–884

    Article  Google Scholar 

  • Herrmann V (1985) Animal experiment and biopsy studies on the cause, manifestations and diagnostic relevance of perifascicular muscle fiber atrophy. Z Gesamte Inn Med 40:417–423

    CAS  PubMed  Google Scholar 

  • Hopwood D (1996) Fixation and fixatives. In: Bancroft J, Stevens A (eds) Theory and practice of histological techniques. Churchill Livingstone, New York

    Google Scholar 

  • Hulland TJ (1993) Muscle and tendon. In: Jubb KVF, Kennedy PC, Palmer N (eds) Pathology of domestic animals, 4th edn. Academic Press, San Diego, pp. 183–265

    Chapter  Google Scholar 

  • Huston K (1993) Hereditability and diagnosis of congenital abnormalities in food animals. Vet Clin North Am Food Anim Prac 9:1–9

    Article  CAS  Google Scholar 

  • Karri SB, Kannan MA, Rajashekhar L et al (2015) Clinicopathological study of adult dermatomyositis: importance of muscle histology in the diagnosis. Ann Indian Acad Neurol 18:194–199

    Article  PubMed  PubMed Central  Google Scholar 

  • Kato K, Takeshita Y, Misu H et al (2015) Liver steatosis is associated with insulin resistance in skeletal muscle rather than in the liver in Japanese patients with non-alcoholic fatty liver disease. J Diabetes Invest 6:158–163

    Article  CAS  Google Scholar 

  • Kauffman RG (2001) Meat composition. In: Hui YH, Nip WK, Rogers RW, Young OA (eds) Meat science and applications. Marcel Dekker, New York, pp. 1–19

    Google Scholar 

  • Kelley DE, He J, Menshikova EV et al (2002) Dysfunction in mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51:2944–2950

    Article  CAS  PubMed  Google Scholar 

  • Kim JK, Michael MD, Previs SF et al (2000) Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J Clin Invest 105:1719–1797

    Google Scholar 

  • Lahoria R, Selcen D, Engel AG (2016) Microvascular alterations and the role of complement in dermatomyositis. Brain. doi:10.1093/brain/aww122

    PubMed  Google Scholar 

  • Langohr IM, Stevenson GW, Valentine BA (2007) Muscular pseudohypertrophy (steatosis) in a bovine fetus. J Vet Diag Invest 19:198–201

    Article  Google Scholar 

  • Lara-Castro C, Garvey T (2008) Intracellular lipid accumulation in liver and muscle and the insulin resistance syndrome. Endocrinol Metab Clin N Am 37:841–856

    Article  CAS  Google Scholar 

  • Leipold HW, Blaugh B, Huston K et al (1973) Weaver syndrome in Brown Swiss cattle: clinical signs and pathology. Vet Small Anim Clin 68:645–647

    CAS  Google Scholar 

  • Liang WC, Nishino I (2011) Lipid storage myopathy. Curr Neurol Neurosci Rep 11:97–103

    Article  CAS  PubMed  Google Scholar 

  • Link BA, Cassens RG, Bray RW et al (1967) Fatty degeneration of bovine longissimus. J Animal Sci 26:694–700

    Article  CAS  Google Scholar 

  • Luo H, Zhou Y, Hu X et al (2015) Activation of PPARγ 2 by PPARγ1 through a functional PPRE in transdifferentiation of myoblasts to adipocytes induced by EPR. Cell Cycle 14:1830–1841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marcus RL, Addison O, Kidde JP et al (2010) Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging 14:362–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marroquin OC, Kelley DE (2008) Obesity and metabolic syndrome. In: Topel EJ (ed) Textbook of cardiovascular medicine, 3rd edn. Lippincott Williams & Wilkins, Philadelphia, pp. 27–35

    Google Scholar 

  • Matsushita S, Ikeda S, Hanyu N et al (1991) Muscular pseudohypertrophy in an adult case with centronuclear myopathy. Eur Neurol 31:172–174

    Article  CAS  PubMed  Google Scholar 

  • McGavin MD (1995) Thomson’s special veterinary pathology, 2nd edn. Mosby, London, pp. 393–422

    Google Scholar 

  • McGavin MD, Baynes ID (1969) A congenital progressive ovine muscular dystrophy. Pathol Vet 6:513–524

    Article  CAS  PubMed  Google Scholar 

  • McHale MJ, Sarwar ZU, Cardenas DP et al (2012) Increased fat deposition in injured skeletal muscle is regulated by sex-specific hormones. Am J Physiol Regul Integr Comp Physiol 302:R331–R339

    Article  CAS  PubMed  Google Scholar 

  • Miranda A, DiMauro S, Eastwood A et al (1979) Lipid storage myopathy, ichthyosis, and steatorrhea. Muscle Nerve 2:1–13

    Article  CAS  PubMed  Google Scholar 

  • Moisan PG, Steffen DJ, Sanderson MW et al (2002) A familial degenerative neuromuscular disease of Gelbvieh cattle. J Vet Diagn Investig 14:140–149

    Article  Google Scholar 

  • Monlux WS, Monlux AW (1972) Atlas of meat inspection pathology. United States Department of Agriculture, Washington, DC, pp. 139–140

    Google Scholar 

  • Muellar RE (1980) Brown Swiss weaver syndrome: studies of muscle pathology. Kansas State University, Dissertation

    Google Scholar 

  • Ohfuji S (1999) Neurogenic muscular steatosis in cattle. J Jpn Vet Med Assoc 52:525–528 (in Japanese)

    Article  Google Scholar 

  • Ohfuji S (2013) Generalized muscular steatosis (pseudohypertrophy) in a heifer. Comp Clin Pathol 22:785–788

    Article  CAS  Google Scholar 

  • Pestronk A, Schmidt RE, Choksi R (2010) Vascular pathology in dermatomyositis and anatomic relations to myopathology. Muscle Nerve 42:53–61

    Article  PubMed  Google Scholar 

  • Petersen KF, Befroy D, Dufour S et al (2003) Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300:1140–1142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen KF, Dufour S, Befroy D et al (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Platt SR, Chrisman CL, Shelton GD (1999) Lipid storage myopathy in a cocker spaniel. J Small Animal Prac 40:31–34

    Article  CAS  Google Scholar 

  • Preuße C, Allenbach Y, Hoffmann O et al (2016) Differential roles of hypoxia and innate immunity in juvenile and adult dermatomyositis. Acta Neuropathol Commun 4:45

    Article  PubMed  PubMed Central  Google Scholar 

  • Pumarola M, Arior S, Majo N et al (1997) Spinal muscular atrophy in Holstein-Friesian calves. Acta Neuropathol 93:178–183

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen BB, Fujita S, Wolfe RR et al (2006) Insulin resistance of muscle protein metabolism in aging. FASEB J 20:768–769

    CAS  PubMed  PubMed Central  Google Scholar 

  • Richards RB, Passmore IK (1989) Ultrastructural changes in skeletal muscle in ovine muscular dystrophy. Acta Neuropathol 79:168–175

    Article  CAS  PubMed  Google Scholar 

  • Roberts CJ, Reid IM, Rowlands GJ et al (1981) A fat mobilization syndrome in dairy cows in early lactation. Vet Rec 108:7–9

    Article  CAS  PubMed  Google Scholar 

  • Roberts CJ, Turfrey BA, Bland AP (1983) Lipid deposition in different fiber types of skeletal muscle of periparturient dairy cows. Vet Pathol 20:23–31

    Article  CAS  PubMed  Google Scholar 

  • Schmidt RE, Reavill DR, Phalen DN (2015) Pathology of pet and aviary birds, 2nd edn. Wiley Blackwell, Singapore, pp. 199–220

    Book  Google Scholar 

  • Schmitt HP, Krause KH (1981) An autopsy study of a familial oculopharyngeal muscular dystrophy (OPMD) with distal spread and neurogenic involvement. Muscle Nerve 4:296–305

    Article  CAS  PubMed  Google Scholar 

  • Sickinger M, von Erichsen J, Koehler K et al (2009) Congenital infiltrative lipomas in a calf. J Vet Diagn Investig 21:719–721

    Article  Google Scholar 

  • Song MY, Ruts E, Kim J et al (2004) Sarcopenia and increased adipose tissue infiltration of muscle in elderly African American women. Am J Clin Nutr 79:874–880

    CAS  PubMed  Google Scholar 

  • Swatland HJ (1974) Developmental disorders of skeletal muscle in cattle, pigs and sheep. Vet Bull 44:179–202

    Google Scholar 

  • Swatland HJ (1994) Structure and development of meat animals and poultry. Technomic Publishing, Lancaster, pp. 65–142

    Google Scholar 

  • Swatland HJ (1995) On-line evaluation of meat. Technomic Publishing, Lancaster, pp. 259–270

    Google Scholar 

  • Szendroedi J, Kaul K, Kloock L et al (2014) Lower fasting muscle mitochondrial activity relates to hepatic steatosis in humans. Diabetes Care 37:468–474

    Article  CAS  PubMed  Google Scholar 

  • Teboul L, Gaillard D, Staccini L et al (1995) Thiazolidinediones and fatty acids convert myogenic cells into adipose-like cells. J Biol Chem 270:28183–28187

    Article  CAS  PubMed  Google Scholar 

  • Troyer D, Cash WC, Vestweber J et al (1993) Review of spinal muscular atrophy (SMA) in Brown Swiss cattle. J Vet Diagn Investig 5:303–306

    Article  CAS  Google Scholar 

  • Valberg SJ (2008) Skeletal muscle function. In: Kaneko JJ, Harvey JW, Bruss MK (eds) Clinical biochemistry of domestic animals, 6th edn. Academic Press, Amsterdam, pp. 459–484

    Chapter  Google Scholar 

  • Valentine BA, McGavin MD (2012) Skeletal muscle. In: Zachary JF, McGavin MD (eds) Pathologic basis of veterinary disease, 5th edn. Elsevier, St. Louis, pp. 871–919

    Google Scholar 

  • Visser M, Goodpaster BH, Kritchevsky SB et al (2005) Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci 60:324–333

    Article  Google Scholar 

  • Wheeler TL, Cundiff LV, Koch RM (1994) Effect of marbling degree on beef palatability in Bos taurus and Bos indicus cattle. J Anim Sci 72:3145–3151

    CAS  PubMed  Google Scholar 

  • Winsor L (1994) Tissue processing. In: Woods A, Ellis R (eds) Laboratory histopathology. Churchill Livingstone, New York

    Google Scholar 

  • Yu YH, Liu BH, Mersmann HJ et al (2006) Porcine peroxisome proliferator-activated receptor gamma induces transdifferentiation of myocytes into adipocytes. J Animal Sci 84:2655–2665

    Article  CAS  Google Scholar 

  • Zachary JF, McGavin MD (2012) Pathologic basis of veterinary disease, 5 ed. Elsevier, St. Louis, pp. 888–893

    Google Scholar 

  • Zimmerman JJ, Karriker LA, Raminez A et al (2012) Diseases of swine, 10th edn. Wiley-Blackwell, Oxford, pp. 294–328

    Google Scholar 

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  1. Department of Histopathology, Diagnostic Animal Pathology Office, Nishino 11-9/20-25, Sapporo, Hokkaido, 063-0041, Japan

    S. Ohfuji

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Ohfuji, S. Pathology of muscular steatosis in the bovine species: report of two spontaneously arising cases and comparative overview of the condition. Comp Clin Pathol 26, 237–245 (2017). https://doi.org/10.1007/s00580-016-2376-0

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