Horses are remarkable athletes and a fascinating species in which to study the genetic bases of athletic performance, skeletal muscle biology, and neuromuscular disease. Genetic selection in horses has resulted in many breeds that possess anatomical, physiological, and metabolic variations linked to speed, power, and endurance that are beginning to be defined at the molecular level. Along with the concentration of positive traits, equine breeding programs have also inadvertently concentrated heritable muscle diseases for which mutations impacting electrical conduction, muscle contraction, and energy metabolism within and across breeds have been characterized. The study of heritable muscle diseases in horses has provided exciting insights into the normal structure and function of muscle and important diagnostic tools for veterinarians. Results empower breeders and breed associations to make difficult decisions about how to use this information to improve the overall health and well-being of horses.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Petersen JL, Mickelson JR, Rendahl AK, Valberg SJ, Andersson LS et al. 2013. Genome-wide analysis reveals selection for important traits in domestic horse breeds. PLOS Genet. 9:e1003211 [Google Scholar]
  2. Petersen JL, Valberg SJ, Mickelson JR, McCue ME. 2014. Haplotype diversity in the equine myostatin gene with focus on variants associated with race distance propensity and muscle fiber type proportions. Anim. Genet. 45:827–35 [Google Scholar]
  3. Hill EW, McGivney BA, Gu J, Whiston R, MacHugh DE. 2010. A genome-wide SNP-association study confirms a sequence variant (g.66493737C>T) in the equine myostatin (MSTN) gene as the most powerful predictor of optimum racing distance for Thoroughbred racehorses. BMC Genomics 11:552 [Google Scholar]
  4. Rudolph JA, Spier SJ, Byrns G, Rojas CV, Bernoco D, Hoffman EP. 1992. Periodic paralysis in quarter horses: a sodium channel mutation disseminated by selective breeding. Nat. Genet. 2:144–47 [Google Scholar]
  5. Jamison JM, Baird JD, Smith-Maxie LL, Hulland TJ. 1987. A congenital form of myotonia with dystrophic changes in a Quarterhorse. Equine Vet. J. 19:353–58 [Google Scholar]
  6. Montagna P, Liguori R, Monari L, Strong PN, Riva R et al. 2001. Equine muscular dystrophy with myotonia. Clin. Neurophysiol. 112:294–99 [Google Scholar]
  7. Wijnberg ID, Owczarek-Lipska M, Sacchetto R, Mascarello F, Pascoli F et al. 2012. A missense mutation in the skeletal muscle chloride channel 1 (CLCN1) as candidate causal mutation for congenital myotonia in a New Forest pony. Neuromuscul. Disord. 22:361–67 [Google Scholar]
  8. Bowling AT, Byrns G, Spier S. 1996. Evidence for a single pedigree source of the hyperkalemic periodic paralysis susceptibility gene in quarter horses. Anim. Genet. 27:279–81 [Google Scholar]
  9. Naylor JM. 1994. Equine hyperkalemic periodic paralysis: review and implications. Can. Vet. J. 35:279–85 [Google Scholar]
  10. Spier SJ, Carlson GP, Holliday TA, Cardinet GH III, Pickar JG. 1990. Hyperkalemic periodic paralysis in horses. J. Am. Vet. Med. Assoc. 197:1009–17 [Google Scholar]
  11. Reynolds JA, Potter GD, Greene LW, Wu G, Carter GK et al. 1998. Genetic-diet interactions in the hyperkalemic periodic paralysis syndrome in quarter horses fed varying amounts of potassium: III. The relationship between plasma potassium concentration and HYPP symptoms. J. Equine Vet. Sci. 18:731–35 [Google Scholar]
  12. Cannon SC, Hayward LJ, Beech J, Brown RH Jr. 1995. Sodium channel inactivation is impaired in equine hyperkalemic periodic paralysis. J. Neurophysiol. 73:1892–99 [Google Scholar]
  13. Zhou J, Spier SJ, Beech J, Hoffman EP. 1994. Pathophysiology of sodium channelopathies: correlation of normal/mutant mRNA ratios with clinical phenotype in dominantly inherited periodic paralysis. Hum. Mol. Genet. 3:1599–603 [Google Scholar]
  14. Naylor JM, Nickel DD, Trimino G, Card C, Lightfoot K, Adams G. 1999. Hyperkalaemic periodic paralysis in homozygous and heterozygous horses: a co-dominant genetic condition. Equine Vet. J. 31:153–59 [Google Scholar]
  15. Carr EA, Spier SJ, Kortz GD, Hoffman EP. 1996. Laryngeal and pharyngeal dysfunction in horses homozygous for hyperkalemic periodic paralysis. J. Am. Vet. Med. Assoc. 209:798–803 [Google Scholar]
  16. Tryon RC, Penedo MC, McCue ME, Valberg SJ, Mickelson JR et al. 2009. Evaluation of allele frequencies of inherited disease genes in subgroups of American Quarter Horses. J. Am. Vet. Med. Assoc. 234:120–25 [Google Scholar]
  17. Naylor JM. 1994. Selection of quarter horses affected with hyperkalemic periodic paralysis by show judges. J. Am. Vet. Med. Assoc. 204:926–28 [Google Scholar]
  18. Diakakis N, Spanoudes K, Dessiris A. 2008. Hyperkalemic periodic paralysis-like syndrome in a Criollo Argentino horse. Equine Vet. Educ. 20:396–400 [Google Scholar]
  19. Bryant SH, Conte-Camerino D. 1991. Chloride channel regulation in the skeletal muscle of normal and myotonic goats. Pflugers Arch. 417:605–10 [Google Scholar]
  20. Lehmann-Horn F, Jurkat-Rott K. 1999. Voltage-gated ion channels and hereditary disease. Physiol. Rev. 79:1317–72 [Google Scholar]
  21. Schooley EK, MacLeay JM, Cuddon P, Valberg SJ. 2004. Myotonia congenita in a foal. J. Equine Vet. Sci. 24:483–88 [Google Scholar]
  22. Aleman M, Brosnan RJ, Williams DC, Lecouteur RA, Imai A et al. 2005. Malignant hyperthermia in a horse anesthetized with halothane. J. Vet. Intern. Med. 19:363–66 [Google Scholar]
  23. Mickelson JR, Louis CF. 1996. Malignant hyperthermia: excitation-contraction coupling, Ca2+ release channel, and cell Ca2+ regulation defects. Physiol. Rev. 76:537–92 [Google Scholar]
  24. Aleman M, Nieto JE, Magdesian KG. 2009. Malignant hyperthermia associated with ryanodine receptor 1 (C7360G) mutation in Quarter Horses. J. Vet. Intern. Med. 23:329–34 [Google Scholar]
  25. Betzenhauser MJ, Marks AR. 2010. Ryanodine receptor channelopathies. Pflugers Arch. 460:467–80 [Google Scholar]
  26. Fujii J, Otsu K, Zorzato F, de Leon S, Khanna VK et al. 1991. Identification of a mutation in porcine ryanodine receptor associated with malignant hyperthermia. Science 253:448–51 [Google Scholar]
  27. Aleman M, Riehl J, Aldridge BM, Lecouteur RA, Stott JL, Pessah IN. 2004. Association of a mutation in the ryanodine receptor 1 gene with equine malignant hyperthermia. Muscle Nerve 30:356–65 [Google Scholar]
  28. Nieto JE, Aleman M. 2009. A rapid detection method for the ryanodine receptor 1 (C7360G) mutation in Quarter Horses. J. Vet. Intern. Med. 23:619–22 [Google Scholar]
  29. Klein L, Ailes N, Fackelman GE, Kellon E, Rosenberg H. 1989. Postanesthetic equine myopathy suggestive of malignant hyperthermia. A case report. Vet. Surg. 18:479–82 [Google Scholar]
  30. Manley SV, Kelly AB, Hodgson D. 1983. Malignant hyperthermia-like reactions in three anesthetized horses. J. Am. Vet. Med. Assoc. 183:85–89 [Google Scholar]
  31. Waldron-Mease E, Klein LV, Rosenberg H, Leitch M. 1981. Malignant hyperthermia in a halothane-anesthetized horse. J. Am. Vet. Med. Assoc. 179:896–98 [Google Scholar]
  32. Valberg SJ, Dyson S. 2003. Skeletal muscle and lameness. Diagnosis and Management of Lameness in the Horse Ross M, Dyson S. 723–43 Philadelphia: Elsevier Health Sci. Div. [Google Scholar]
  33. MacLeay JM, Valberg SJ, Pagan JD, De La Corte F, Roberts J et al. 1999. Effect of diet on thoroughbred horses with recurrent exertional rhabdomyolysis performing a standardised exercise test. Equine Vet. J. Suppl. 30:458–62 [Google Scholar]
  34. MacLeay JM, Sorum SA, Valberg SJ, Marsh WE, Sorum MD. 1999. Epidemiologic analysis of factors influencing exertional rhabdomyolysis in Thoroughbreds. Am. J. Vet. Res. 60:1562–66 [Google Scholar]
  35. McKenzie EC, Valberg SJ, Godden SM, Pagan JD, MacLeay JM et al. 2003. Effect of dietary starch, fat, and bicarbonate content on exercise responses and serum creatine kinase activity in equine recurrent exertional rhabdomyolysis. J. Vet. Intern. Med. 17:693–701 [Google Scholar]
  36. Lentz LR, Valberg SJ, Balog EM, Mickelson JR, Gallant EM. 1999. Abnormal regulation of muscle contraction in horses with recurrent exertional rhabdomyolysis. Am. J. Vet. Res. 60:992–99 [Google Scholar]
  37. Valberg SJ, Mickelson JR, Gallant EM, MacLeay JM, Lentz L, de la Court F. 1999. Exertional rhabdomyolysis in quarter horses and thoroughbreds: one syndrome, multiple aetiologies. Equine Vet. J. Suppl. 30:533–38 [Google Scholar]
  38. Isgren CM, Upjohn MM, Fernandez-Fuente M, Massey C, Pollott G et al. 2010. Epidemiology of exertional rhabdomyolysis susceptibility in Standardbred horses reveals associated risk factors and underlying enhanced performance. PLOS ONE 5:e11594 [Google Scholar]
  39. McGowan CM, Fordham T, Christley RM. 2002. Incidence and risk factors for exertional rhabdomyolysis in thoroughbred racehorses in the United Kingdom. Vet. Rec. 151:623–26 [Google Scholar]
  40. Lindholm A, Johansson HE, Kjaersgaard P. 1974. Acute rhabdomyolysis (“tying-up”) in standardbred horses. A morphological and biochemical study. Acta Vet. Scand. 15:325–39 [Google Scholar]
  41. Beech J, Lindborg S, Fletcher JE, Lizzo F, Tripolitis L, Braund K. 1993. Caffeine contractures, twitch characteristics and the threshold for Ca2+-induced Ca2+ release in skeletal muscle from horses with chronic intermittent rhabdomyolysis. Res. Vet. Sci. 54:110–17 [Google Scholar]
  42. Lentz LR, Valberg SJ, Herold LV, Onan GW, Mickelson JR, Gallant EM. 2002. Myoplasmic calcium regulation in myotubes from horses with recurrent exertional rhabdomyolysis. Am. J. Vet. Res. 63:1724–31 [Google Scholar]
  43. Mlekoday JA, Mickelson JR, Valberg SJ, Horton JH, Gallant EM, Thompson LV. 2001. Calcium sensitivity of force production and myofibrillar ATPase activity in muscles from Thoroughbreds with recurrent exertional rhabdomyolysis. Am. J. Vet. Res. 62:1647–52 [Google Scholar]
  44. Ward TL, Valberg SJ, Gallant EM, Mickelson JR. 2000. Calcium regulation by skeletal muscle membranes of horses with recurrent exertional rhabdomyolysis. Am. J. Vet. Res. 61:242–47 [Google Scholar]
  45. Edwards JG, Newtont JR, Ramzan PH, Pilsworth RC, Shepherd MC. 2003. The efficacy of dantrolene sodium in controlling exertional rhabdomyolysis in the Thoroughbred racehorse. Equine Vet. J. 35:707–11 [Google Scholar]
  46. McKenzie EC, Valberg SJ, Godden SM, Finno CJ, Murphy MJ. 2004. Effect of oral administration of dantrolene sodium on serum creatine kinase activity after exercise in horses with recurrent exertional rhabdomyolysis. Am. J. Vet. Res. 65:74–79 [Google Scholar]
  47. MacLeay JM, Valberg SJ, Sorum SA, Sorum MD, Kassube T et al. 1999. Heritability of recurrent exertional rhabdomyolysis in Thoroughbred racehorses. Am. J. Vet. Res. 60:250–56 [Google Scholar]
  48. Dranchak PK, Valberg SJ, Onan GW, Gallant EM, MacLeay JM et al. 2005. Inheritance of recurrent exertional rhabdomyolysis in thoroughbreds. J. Am. Vet. Med. Assoc. 227:762–67 [Google Scholar]
  49. Oki H, Miyake T, Hasegawa T, Sasaki Y. 2005. Estimation of heritability for Tying-up syndrome in the Thoroughbred racehorse by Gibbs sampling. J. Anim. Breed. Genet. 122:289–93 [Google Scholar]
  50. Dranchak PK, Valberg SJ, Onan GW, Gallant EM, Binns MM et al. 2006. Exclusion of linkage of the RYR1, CACNA1S, and ATP2A1 genes to recurrent exertional rhabdomyolysis in Thoroughbreds. Am. J. Vet. Res. 67:1395–400 [Google Scholar]
  51. Tozaki T, Hirota K, Sugita S, Ishida N, Miyake T et al. 2010. A genome-wide scan for tying-up syndrome in Japanese Thoroughbreds. Anim. Genet. 41:Suppl. 280–86 [Google Scholar]
  52. Fritz KL, McCue ME, Valberg SJ, Rendahl AK, Mickelson JR. 2012. Genetic mapping of recurrent exertional rhabdomyolysis in a population of North American Thoroughbreds. Anim. Genet. 43:730–38 [Google Scholar]
  53. Ward TL, Valberg SJ, Adelson DL, Abbey CA, Binns MM, Mickelson JR. 2004. Glycogen branching enzyme (GBE1) mutation causing equine glycogen storage disease IV. Mamm. Genome 15:570–77 [Google Scholar]
  54. McCue ME, Valberg SJ, Miller MB, Wade C, DiMauro S et al. 2008. Glycogen synthase (GYS1) mutation causes a novel skeletal muscle glycogenosis. Genomics 91:458–66 [Google Scholar]
  55. Carlström B. 1932. Uber die atiologie und pathogenese der kreuzlahme des pferdes (Haemaglobinaemia paralytica). Scand. Archiv. 62:1–62 [Google Scholar]
  56. Valberg SJ, Cardinet GH III, Carlson GP, DiMauro S. 1992. Polysaccharide storage myopathy associated with recurrent exertional rhabdomyolysis in horses. Neuromuscul. Disord. 2:351–59 [Google Scholar]
  57. Valentine BA, Credille KM, Lavoie JP, Fatone S, Guard C et al. 1997. Severe polysaccharide storage myopathy in Belgian and Percheron draught horses. Equine Vet. J. 29:220–25 [Google Scholar]
  58. Firshman AM, Baird JD, Valberg SJ. 2005. Prevalences and clinical signs of polysaccharide storage myopathy and shivers in Belgian draft horses. J. Am. Vet. Med. Assoc. 227:1958–64 [Google Scholar]
  59. De La Corte FD, Valberg SJ, MacLeay JM, Mickelson JR. 2002. Developmental onset of polysaccharide storage myopathy in 4 Quarter Horse foals. J. Vet. Intern. Med. 16:581–87 [Google Scholar]
  60. Byrne E, Jones SL, Valberg SJ, Zimmel DN, Cohen N. 2000. Rhabdomyolysis in two foals with polysaccharide storage myopathy and concurrent pneumonia. Compend. Contin. Educ. Pract. Vet. 22:503–7 [Google Scholar]
  61. Valberg SJ, MacLeay JM, Billstrom JA, Hower-Moritz MA, Mickelson JR. 1999. Skeletal muscle metabolic response to exercise in horses with ‘tying-up’ due to polysaccharide storage myopathy. Equine Vet. J. 31:43–47 [Google Scholar]
  62. Firshman AM, Valberg SJ, Bender JB, Annandale EJ, Hayden DW. 2006. Comparison of histopathologic criteria and skeletal muscle fixation techniques for the diagnosis of polysaccharide storage myopathy in horses. Vet. Pathol. 43:257–69 [Google Scholar]
  63. McCue ME, Armien AG, Lucio M, Mickelson JR, Valberg SJ. 2009. Comparative skeletal muscle histopathologic and ultrastructural features in two forms of polysaccharide storage myopathy in horses. Vet. Pathol. 46:1281–91 [Google Scholar]
  64. Annandale EJ, Valberg SJ, Mickelson JR, Seaquist ER. 2004. Insulin sensitivity and skeletal muscle glucose transport in horses with equine polysaccharide storage myopathy. Neuromuscul. Disord. 14:666–74 [Google Scholar]
  65. Valentine BA, Flint TH, Fischer KA. 2006. Ubiquitin expression in muscle from horses with polysaccharide storage myopathy. Vet. Pathol. 43:270–75 [Google Scholar]
  66. Naylor RJ, Luis-Fuentes V, Livesey L, Mobley CB, Henke N et al. 2012. Evaluation of cardiac phenotype in horses with type 1 polysaccharide storage myopathy. J. Vet. Intern. Med. 26:1464–69 [Google Scholar]
  67. Valberg SJ, Geyer C, Sorum SA, Cardinet GH III. 1996. Familial basis of exertional rhabdomyolysis in quarter horse-related breeds. Am. J. Vet. Res. 57:286–90 [Google Scholar]
  68. Baird JD, Valberg SJ, Anderson SM, McCue ME, Mickelson JR. 2010. Presence of the glycogen synthase 1 (GYS1) mutation causing type 1 polysaccharide storage myopathy in continental European draught horse breeds. Vet. Rec. 167:781–84 [Google Scholar]
  69. Herszberg B, McCue ME, Larcher T, Mata X, Vaiman A et al. 2008. A GYS1 gene mutation is highly associated with polysaccharide storage myopathy in Cob Normand draught horses. Anim. Genet. 40:94–96 [Google Scholar]
  70. McCue ME, Anderson SM, Valberg SJ, Piercy RJ, Barakzai SZ et al. 2010. Estimated prevalence of the Type 1 Polysaccharide Storage Myopathy mutation in selected North American and European breeds. Anim. Genet. 41:Suppl. 2145–49 [Google Scholar]
  71. Stanley RL, McCue ME, Valberg SJ, Mickelson JR, Mayhew IG et al. 2009. A glycogen synthase 1 mutation associated with equine polysaccharide storage myopathy and exertional rhabdomyolysis occurs in a variety of UK breeds. Equine Vet. J. 41:597–601 [Google Scholar]
  72. Naylor RJ, Livesey L, Schumacher J, Henke N, Massey C et al. 2012. Allele copy number and underlying pathology are associated with subclinical severity in equine type 1 polysaccharide storage myopathy (PSSM1). PLOS ONE 7:e42317 [Google Scholar]
  73. McCue ME, Valberg SJ, Lucio M, Mickelson JR. 2008. Glycogen synthase 1 (GYS1) mutation in diverse breeds with polysaccharide storage myopathy. J. Vet. Intern. Med. 22:1228–33 [Google Scholar]
  74. McCue ME, Valberg SJ, Jackson M, Lucio M, Mickelson JR. 2008. Polysaccharide storage myopathy phenotype in Quarter Horse-related breeds is modified by the presence of an RYR1 mutation. Neuromuscul. Disord. 19:37–43 [Google Scholar]
  75. Valberg SJ, Jones JH, Smith BL, Sommerville B. 1995. Limitations to performance caused by skeletal muscle enzyme deficiencies. Equine Vet. J. Suppl. 18:205–8 [Google Scholar]
  76. Kollberg G, Tulinius M, Gilljam T, Ostman-Smith I, Forsander G et al. 2007. Cardiomyopathy and exercise intolerance in muscle glycogen storage disease 0. N. Engl. J. Med. 357:1507–14 [Google Scholar]
  77. Cameron JM, Levandovskiy V, MacKay N, Utgikar R, Ackerley C et al. 2009. Identification of a novel mutation in GYS1 (muscle-specific glycogen synthase) resulting in sudden cardiac death, that is diagnosable from skin fibroblasts. Mol. Genet. Metab. 98:378–82 [Google Scholar]
  78. Annandale EJ, Valberg SJ, Essen-Gustavsson B. 2005. Effects of submaximal exercise on adenine nucleotide concentrations in skeletal muscle fibers of horses with polysaccharide storage myopathy. Am. J. Vet. Res. 66:839–45 [Google Scholar]
  79. Barrey E, Mucher E, Jeansoule N, Larcher T, Guigand L et al. 2009. Gene expression profiling in equine polysaccharide storage myopathy revealed inflammation, glycogenesis inhibition, hypoxia and mitochondrial dysfunctions. BMC Vet. Res. 5:29 [Google Scholar]
  80. Johlig L, Valberg SJ, Mickelson JR, Klukowska J, Reusser HR et al. 2011. Epidemiological and genetic study of exertional rhabdomyolysis in a Warmblood horse family in Switzerland. Equine Vet. J. 43:240–45 [Google Scholar]
  81. Ribeiro WP, Valberg SJ, Pagan JD, Gustavsson BE. 2004. The effect of varying dietary starch and fat content on serum creatine kinase activity and substrate availability in equine polysaccharide storage myopathy. J. Vet. Intern. Med. 18:887–94 [Google Scholar]
  82. Firshman AM, Valberg SJ, Bender JB, Finno CJ. 2003. Epidemiologic characteristics and management of polysaccharide storage myopathy in Quarter Horses. Am. J. Vet. Res. 64:1319–27 [Google Scholar]
  83. Borgia LA, Valberg SJ, McCue ME, Pagan JD, Roe CR. 2010. Effect of dietary fats with odd or even numbers of carbon atoms on metabolic response and muscle damage with exercise in Quarter Horse-type horses with type 1 polysaccharide storage myopathy. Am. J. Vet. Res. 71:326–36 [Google Scholar]
  84. Valentine BA, Van Saun RJ, Thompson KN, Hintz HF. 2001. Role of dietary carbohydrate and fat in horses with equine polysaccharide storage myopathy. J. Am. Vet. Med. Assoc. 219:1537–44 [Google Scholar]
  85. DiMauro S, Tsujino S, Shanske S, Rowland LP. 1995. Biochemistry and molecular genetics of human glycogenoses: an overview. Muscle Nerve 3:S10–17 [Google Scholar]
  86. DiMauro S, Lamperti C. 2001. Muscle glycogenoses. Muscle Nerve 24:984–99 [Google Scholar]
  87. DiMauro S, Garone C, Naini A. 2010. Metabolic myopathies. Curr. Rheumatol. Rep. 12:386–93 [Google Scholar]
  88. McCoy AM, Schaefer R, Petersen JL, Morrell PL, Slamka MA et al. 2014. Evidence of positive selection for a glycogen synthase (GYS1) mutation in domestic horse populations. J. Hered. 105:163–72 [Google Scholar]
  89. Valberg SJ, Ward TL, Rush B, Kinde H, Hiraragi H et al. 2001. Glycogen branching enzyme deficiency in Quarter Horse foals. J. Vet. Intern. Med. 15:572–80 [Google Scholar]
  90. Sponseller BT, Valberg SJ, Ward TL, Fales-Williams AJ, Mickelson JR. 2003. Muscular weakness and recumbency in a Quarter Horse colt due to glycogen branching enzyme deficiency. Equine Vet. Educ. 14:182–88 [Google Scholar]
  91. Ward TL, Valberg SJ, Lear TL, Guerin G, Milenkovic D et al. 2003. Genetic mapping of GBE1 and its association with glycogen storage disease IV in American Quarter Horses. Cytogenet. Genome Res. 102:201–6 [Google Scholar]
  92. Wagner ML, Valberg SJ, Ames EG, Bauer MM, Wiseman JA et al. 2006. Allele frequency and likely impact of the glycogen branching enzyme deficiency gene in Quarter Horse and Paint Horse populations. J. Vet. Intern. Med. 20:1207–11 [Google Scholar]
  93. Render JA, Common RS, Kennedy FA, Jones MZ, Fyfe JC. 1999. Amylopectinosis in fetal and neonatal Quarter Horses. Vet. Pathol. 36:157–60 [Google Scholar]
  94. De La Corte FD, Valberg SJ, Mickelson JR, Hower-Moritz M. 1999. Blood glucose clearance after feeding and exercise in polysaccharide storage myopathy. Equine Vet. J. Suppl. 30:324–28 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error