1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Antimicrobial Resistance in

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • PDF
    248.63 Kb
  • HTML
    73.76 Kb
  • XML
    80.03 Kb
  • Authors: Steeve Giguère1, Londa J. Berghaus2, Jennifer M. Willingham-Lane3
  • Editors: Frank Møller Aarestrup4, Stefan Schwarz5, Jianzhong Shen6, Lina Cavaco7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Large Animal Medicine, College of Veterinary Medicine, University of Georgia, Athens, GA 30605; 2: Department of Large Animal Medicine, College of Veterinary Medicine, University of Georgia, Athens, GA 30605; 3: Department of Large Animal Medicine, College of Veterinary Medicine, University of Georgia, Athens, GA 30605; 4: Technical University of Denmark, Lyngby, Denmark; 5: Friedrich-Loeffler-Institut, Neustadt, Germany; 6: China Agricultural University, Beijing, China; 7: Technical University of Denmark, Lyngby, Denmark
    • Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.ARBA-0004-2016
  • Received 09 December 2016 Accepted 27 September 2017 Published 19 October 2017
  • Steeve Giguère, [email protected]
image of Antimicrobial Resistance in <span class="jp-italic">Rhodococcus equi</span>
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Antimicrobial Resistance in , Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/5/5/ARBA-0004-2016-1.gif /docserver/preview/fulltext/microbiolspec/5/5/ARBA-0004-2016-2.gif

  • Abstract:

    Pneumonia caused by remains an important cause of disease and death in foals. The combination of a macrolide (erythromycin, azithromycin, or clarithromycin) with rifampin has been the recommended treatment for foals with clinical signs of infection caused by since the early 1980s with, until recently, only rare reports of resistance. Resistance to macrolides and rifampin in isolates of cultured from horses is increasing, with isolates resistant to all macrolides and rifampin now being cultured from up to 40% of infected foals at some farms. This text reviews the available data regarding antimicrobial resistance in , with emphasis on the molecular mechanisms of the recent emergence of resistance to macrolides and rifampin in equine isolates of .

  • Citation: Giguère S, Berghaus L, Willingham-Lane J. 2017. Antimicrobial Resistance in . Microbiol Spectrum 5(5):ARBA-0004-2016. doi:10.1128/microbiolspec.ARBA-0004-2016.

References

1. Arlotti M, Zoboli G, Moscatelli GL, Magnani G, Maserati R, Borghi V, Andreoni M, Libanore M, Bonazzi L, Piscina A, Ciammarughi R. 1996. Rhodococcus equi infection in HIV-positive subjects: a retrospective analysis of 24 cases. Scand J Infect Dis 28:463–467 http://dx.doi.org/10.3109/00365549609037941. [PubMed]
2. Donisi A, Suardi MG, Casari S, Longo M, Cadeo GP, Carosi G. 1996. Rhodococcus equi infection in HIV-infected patients. AIDS 10:359–362 http://dx.doi.org/10.1097/00002030-199604000-00002. [PubMed]
3. Yamshchikov AV, Schuetz A, Lyon GM. 2010. Rhodococcus equi infection. Lancet Infect Dis 10:350–359 http://dx.doi.org/10.1016/S1473-3099(10)70068-2. [PubMed]
4. Giguère S, Cohen ND, Chaffin MK, Hines SA, Hondalus MK, Prescott JF, Slovis NM. 2011. Rhodococcus equi: clinical manifestations, virulence, and immunity. J Vet Intern Med 25:1221–1230 http://dx.doi.org/10.1111/j.1939-1676.2011.00804.x. [PubMed]
5. Reuss SM, Chaffin MK, Cohen ND. 2009. Extrapulmonary disorders associated with Rhodococcus equi infection in foals: 150 cases (1987-2007). J Am Vet Med Assoc 235:855–863 http://dx.doi.org/10.2460/javma.235.7.855. [PubMed]
6. Zink MC, Yager JA, Smart NL. 1986. Corynebacterium equi infections in horses, 1958-1984: a review of 131 cases. Can Vet J 27:213–217. [PubMed]
7. Slovis NM, McCracken JL, Mundy G. 2005. How to use thoracic ultrasound to screen foals for Rhodococcus equi at affected farms. Proc Am Assoc Equine Pract 51:274–278.
8. Venner M, Kerth R, Klug E. 2007. Evaluation of tulathromycin in the treatment of pulmonary abscesses in foals. Vet J 174:418–421 http://dx.doi.org/10.1016/j.tvjl.2006.08.016. [PubMed]
9. Komijn RE, Wisselink HJ, Rijsman VM, Stockhofe-Zurwieden N, Bakker D, van Zijderveld FG, Eger T, Wagenaar JA, Putirulan FF, Urlings BA. 2007. Granulomatous lesions in lymph nodes of slaughter pigs bacteriologically negative for Mycobacterium avium subsp. avium and positive for Rhodococcus equi. Vet Microbiol 120:352–357 http://dx.doi.org/10.1016/j.vetmic.2006.10.031. [PubMed]
10. Madarame H, Yaegashi R, Fukunaga N, Matsukuma M, Mutoh K, Morisawa N, Sasaki Y, Tsubaki S, Hasegawa Y, Takai S. 1998. Pathogenicity of Rhodococcus equi strains possessing virulence-associated 15- to 17-kDa and 20-kDa antigens: experimental and natural cases in pigs. J Comp Pathol 119:397–405 http://dx.doi.org/10.1016/S0021-9975(98)80034-0. [PubMed]
11. Takai S, Fukunaga N, Ochiai S, Sakai T, Sasaki Y, Tsubaki S. 1996. Isolation of virulent and intermediately virulent Rhodococcus equi from soil and sand on parks and yards in Japan. J Vet Med Sci 58:669–672 http://dx.doi.org/10.1292/jvms.58.669. [PubMed]
12. Flynn O, Quigley F, Costello E, O’Grady D, Gogarty A, Mc Guirk J, Takai S. 2001. Virulence-associated protein characterisation of Rhodococcus equi isolated from bovine lymph nodes. Vet Microbiol 78:221–228 http://dx.doi.org/10.1016/S0378-1135(00)00297-2.
13. Hong CB, Donahue JM. 1995. Rhodococcus equi-associated necrotizing lymphadenitis in a llama. J Comp Pathol 113:85–88 http://dx.doi.org/10.1016/S0021-9975(05)80073-8.
14. Kinne J, Madarame H, Takai S, Jose S, Wernery U. 2011. Disseminated Rhodococcus equi infection in dromedary camels ( Camelus dromedarius). Vet Microbiol 149:269–272 http://dx.doi.org/10.1016/j.vetmic.2010.09.037. [PubMed]
15. Tkachuk-Saad O, Lusis P, Welsh RD, Prescott JF. 1998. Rhodococcus equi infections in goats. Vet Rec 143:311–312 http://dx.doi.org/10.1136/vr.143.11.311. [PubMed]
16. Bryan LK, Clark SD, Diaz-Delgado J, Lawhon SD, Edwards JF. 2016. Rhodococcus equi infections in dogs. Vet Pathol. [PubMed]
17. Takai S, Martens RJ, Julian A, Garcia Ribeiro M, Rodrigues de Farias M, Sasaki Y, Inuzuka K, Kakuda T, Tsubaki S, Prescott JF. 2003. Virulence of Rhodococcus equi isolated from cats and dogs. J Clin Microbiol 41:4468–4470 http://dx.doi.org/10.1128/JCM.41.9.4468-4470.2003. [PubMed]
18. Riesenberg A, Kaspar H, Feßler AT, Werckenthin C, Schwarz S. 2016.Susceptibility testing of Rhodococcus equi: an interlaboratory test. Vet Microbiol 194:30–35 http://dx.doi.org/10.1016/j.vetmic.2015.11.029. [PubMed]
19. Riesenberg A, Feßler AT, Frömke C, Kadlec K, Klarmann D, Kreienbrock L, Werckenthin C, Schwarz S. 2013. Harmonization of antimicrobial susceptibility testing by broth microdilution for Rhodococcus equi of animal origin. J Antimicrob Chemother 68:2173–2175 http://dx.doi.org/10.1093/jac/dkt134. [PubMed]
20. Berghaus LJ, Giguère S, Guldbech K, Warner E, Ugorji U, Berghaus RD. 2015. Comparison of Etest, disk diffusion, and broth macrodilution for in vitro susceptibility testing of Rhodococcus equi. J Clin Microbiol 53:314–318 http://dx.doi.org/10.1128/JCM.02673-14. [PubMed]
21. Giguère S, Lee EA, Guldbech KM, Berghaus LJ. 2012. In vitro synergy, pharmacodynamics, and postantibiotic effect of 11 antimicrobial agents against Rhodococcus equi. Vet Microbiol 160:207–213 http://dx.doi.org/10.1016/j.vetmic.2012.05.031. [PubMed]
22. Nordmann P, Ronco E. 1992. In-vitro antimicrobial susceptibility of Rhodococcus equi. J Antimicrob Chemother 29:383–393 http://dx.doi.org/10.1093/jac/29.4.383. [PubMed]
23. Prescott JF, Nicholson VM. 1984. The effects of combinations of selected antibiotics on the growth of Corynebacterium equi. J Vet Pharmacol Ther 7:61–64 http://dx.doi.org/10.1111/j.1365-2885.1984.tb00880.x. [PubMed]
24. Blondeau JM. 2009. New concepts in antimicrobial susceptibility testing: the mutant prevention concentration and mutant selection window approach. Vet Dermatol 20:383–396 http://dx.doi.org/10.1111/j.1365-3164.2009.00856.x. [PubMed]
25. Berghaus LJ, Giguère S, Guldbech K. 2013. Mutant prevention concentration and mutant selection window for 10 antimicrobial agents against Rhodococcus equi. Vet Microbiol 166:670–675 http://dx.doi.org/10.1016/j.vetmic.2013.07.006. [PubMed]
26. Giguère S, Hondalus MK, Yager JA, Darrah P, Mosser DM, Prescott JF. 1999. Role of the 85-kilobase plasmid and plasmid-encoded virulence-associated protein A in intracellular survival and virulence of Rhodococcus equi. Infect Immun 67:3548–3557. [PubMed]
27. Berghaus LJ, Giguère S, Sturgill TL, Bade D, Malinski TJ, Huang R. 2012. Plasma pharmacokinetics, pulmonary distribution, and in vitro activity of gamithromycin in foals. J Vet Pharmacol Ther 35:59–66 http://dx.doi.org/10.1111/j.1365-2885.2011.01292.x. [PubMed]
28. Giguère S, Jacks S, Roberts GD, Hernandez J, Long MT, Ellis C. 2004. Retrospective comparison of azithromycin, clarithromycin, and erythromycin for the treatment of foals with Rhodococcus equi pneumonia. J Vet Intern Med 18:568–573 http://dx.doi.org/10.1111/j.1939-1676.2004.tb02587.x. [PubMed]
29. Giguère S, Cohen ND, Chaffin MK, Slovis NM, Hondalus MK, Hines SA, Prescott JF. 2011. Diagnosis, treatment, control, and prevention of infections caused by Rhodococcus equi in foals. J Vet Intern Med 25:1209–1220 http://dx.doi.org/10.1111/j.1939-1676.2011.00835.x. [PubMed]
30. Hillidge CJ. 1987. Use of erythromycin-rifampin combination in treatment of Rhodococcus equi pneumonia. Vet Microbiol 14:337–342 http://dx.doi.org/10.1016/0378-1135(87)90121-0. [PubMed]
31. Kenney DG, Robbins SC, Prescott JF, Kaushik A, Baird JD. 1994. Development of reactive arthritis and resistance to erythromycin and rifampin in a foal during treatment for Rhodococcus equi pneumonia. Equine Vet J 26:246–248 http://dx.doi.org/10.1111/j.2042-3306.1994.tb04379.x. [PubMed]
32. Fines M, Pronost S, Maillard K, Taouji S, Leclercq R. 2001. Characterization of mutations in the rpoB gene associated with rifampin resistance in Rhodococcus equi isolated from foals. J Clin Microbiol 39:2784–2787 http://dx.doi.org/10.1128/JCM.39.8.2784-2787.2001. [PubMed]
33. Takai S, Takeda K, Nakano Y, Karasawa T, Furugoori J, Sasaki Y, Tsubaki S, Higuchi T, Anzai T, Wada R, Kamada M. 1997. Emergence of rifampin-resistant Rhodococcus equi in an infected foal. J Clin Microbiol 35:1904–1908. [PubMed]
34. Giguère S, Lee E, Williams E, Cohen ND, Chaffin MK, Halbert N, Martens RJ, Franklin RP, Clark CC, Slovis NM. 2010. Determination of the prevalence of antimicrobial resistance to macrolide antimicrobials or rifampin in Rhodococcus equi isolates and treatment outcome in foals infected with antimicrobial-resistant isolates of R equi. J Am Vet Med Assoc 237:74–81 http://dx.doi.org/10.2460/javma.237.1.74. [PubMed]
35. Burton AJ, Giguère S, Sturgill TL, Berghaus LJ, Slovis NM, Whitman JL, Levering C, Kuskie KR, Cohen ND. 2013. Macrolide- and rifampin-resistant Rhodococcus equi on a horse breeding farm, Kentucky, USA. Emerg Infect Dis 19:282–285 http://dx.doi.org/10.3201/eid1902.121210. [PubMed]
36. Liu H, Wang Y, Yan J, Wang C, He H, Forbes BA. 2014. Appearance of multidrug-resistant virulent Rhodococcus equi clinical isolates obtained in China. J Clin Microbiol 52:703 http://dx.doi.org/10.1128/JCM.02925-13. [PubMed]
37. McNeil MM, Brown JM. 1992. Distribution and antimicrobial susceptibility of Rhodococcus equi from clinical specimens. Eur J Epidemiol 8:437–443 http://dx.doi.org/10.1007/BF00158580. [PubMed]
38. Roberts MC. 2004. Resistance to macrolide, lincosamide, streptogramin, ketolide, and oxazolidinone antibiotics. Mol Biotechnol 28:47–62 http://dx.doi.org/10.1385/MB:28:1:47. [PubMed]
39. Roberts MC. 2008. Update on macrolide-lincosamide-streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett 282:147–159 http://dx.doi.org/10.1111/j.1574-6968.2008.01145.x. [PubMed]
40. Franceschi F, Kanyo Z, Sherer EC, Sutcliffe J. 2004. Macrolide resistance from the ribosome perspective. Curr Drug Targets Infect Disord 4:177–191 http://dx.doi.org/10.2174/1568005043340740. [PubMed]
41. Anastasi E, Giguère S, Berghaus LJ, Hondalus MK, Willingham-Lane JM, MacArthur I, Cohen ND, Roberts MC, Vazquez-Boland JA. 2015. Novel transferable erm(46) determinant responsible for emerging macrolide resistance in Rhodococcus equi.J Antimicrob Chemother 70:3184–3190. [PubMed]
42. Asoh N, Watanabe H, Fines-Guyon M, Watanabe K, Oishi K, Kositsakulchai W, Sanchai T, Kunsuikmengrai K, Kahintapong S, Khantawa B, Tharavichitkul P, Sirisanthana T, Nagatake T. 2003. Emergence of rifampin-resistant Rhodococcus equi with several types of mutations in the rpoB gene among AIDS patients in northern Thailand. J Clin Microbiol 41:2337–2340 http://dx.doi.org/10.1128/JCM.41.6.2337-2340.2003. [PubMed]
43. Riesenberg A, Feßler AT, Erol E, Prenger-Berninghoff E, Stamm I, Böse R, Heusinger A, Klarmann D, Werckenthin C, Schwarz S. 2014. MICs of 32 antimicrobial agents for Rhodococcus equi isolates of animal origin. J Antimicrob Chemother 69:1045–1049 http://dx.doi.org/10.1093/jac/dkt460. [PubMed]
44. Quan S, Venter H, Dabbs ER. 1997. Ribosylative inactivation of rifampin by Mycobacterium smegmatis is a principal contributor to its low susceptibility to this antibiotic. Antimicrob Agents Chemother 41:2456–2460. [PubMed]
45. Spanogiannopoulos P, Waglechner N, Koteva K, Wright GD. 2014. A rifamycin inactivating phosphotransferase family shared by environmental and pathogenic bacteria. Proc Natl Acad Sci USA 111:7102–7107 http://dx.doi.org/10.1073/pnas.1402358111. [PubMed]
46. Hoshino Y, Fujii S, Shinonaga H, Arai K, Saito F, Fukai T, Satoh H, Miyazaki Y, Ishikawa J. 2010. Monooxygenation of rifampicin catalyzed by the rox gene product of Nocardia farcinica: structure elucidation, gene identification and role in drug resistance. J Antibiot (Tokyo) 63:23–28 http://dx.doi.org/10.1038/ja.2009.116. [PubMed]
47. Andersen SJ, Quan S, Gowan B, Dabbs ER. 1997. Monooxygenase-like sequence of a Rhodococcus equi gene conferring increased resistance to rifampin by inactivating this antibiotic. Antimicrob Agents Chemother 41:218–221. [PubMed]
48. Vivrette S, Bostian A, Bermingham E, Papich MG. 2001. Quinolone induced arthropathy in neonatal foals. Proc. Am. Assoc. Equine Pract 47:376–377.
49. Jacks SS, Giguère S, Nguyen A. 2003. In vitro susceptibilities of Rhodococcus equi and other common equine pathogens to azithromycin, clarithromycin, and 20 other antimicrobials. Antimicrob Agents Chemother 47:1742–1745 http://dx.doi.org/10.1128/AAC.47.5.1742-1745.2003. [PubMed]
50. Giguère S. 2006. Antimicrobial drug use in horses, p 449–462. In Giguère S, Prescott JF, Baggot JD, Walker RD, Dowling PM (ed), Antimicrobial Therapy in Veterinary Medicine, 4th ed. Blackwell Publishing, Ames IA.
51. Gundelly P, Suzuki Y, Ribes JA, Thornton A. 2016. Differences in Rhodococcus equi infections based on immune status and antibiotic susceptibility of clinical isolates in a case series of 12 patients and cases in the literature. BioMed Res Int 2016:2737295 http://dx.doi.org/10.1155/2016/2737295. [PubMed]
52. Niwa H, Hobo S, Anzai T. 2006. A nucleotide mutation associated with fluoroquinolone resistance observed in gyrA of in vitro obtained Rhodococcus equi mutants. Vet Microbiol 115:264–268 http://dx.doi.org/10.1016/j.vetmic.2006.01.015. [PubMed]
53. Niwa H, Lasker BA. 2010. Mutant selection window and characterization of allelic diversity for ciprofloxacin-resistant mutants of Rhodococcus equi. Antimicrob Agents Chemother 54:3520–3523 http://dx.doi.org/10.1128/AAC.01670-09. [PubMed]
54. Gudeta DD, Moodley A, Bortolaia V, Guardabassi L. 2014. vanO, a new glycopeptide resistance operon in environmental Rhodococcus equi isolates. Antimicrob Agents Chemother 58:1768–1770 http://dx.doi.org/10.1128/AAC.01880-13. [PubMed]
55. Letek M, González P, Macarthur I, Rodríguez H, Freeman TC, Valero-Rello A, Blanco M, Buckley T, Cherevach I, Fahey R, Hapeshi A, Holdstock J, Leadon D, Navas J, Ocampo A, Quail MA, Sanders M, Scortti MM, Prescott JF, Fogarty U, Meijer WG, Parkhill J, Bentley SD, Vázquez-Boland JA. 2010. The genome of a pathogenic Rhodococcus: cooptive virulence underpinned by key gene acquisitions. PLoS Genet 6:e1001145 http://dx.doi.org/10.1371/journal.pgen.1001145. [PubMed]
56. Nordmann P, Nicolas MH, Gutmann L. 1993. Penicillin-binding proteins of Rhodococcus equi: potential role in resistance to imipenem. Antimicrob Agents Chemother 37:1406–1409 http://dx.doi.org/10.1128/AAC.37.7.1406. [PubMed]
57. Carlson KL, Kuskie KR, Chaffin KM, Libal MC, Giguère S, Lawhon SD, Cohen ND. 2010. Antimicrobial activity of tulathromycin and 14 other antimicrobials against virulent Rhodococcus equi in vitro. Vet Ther 11:E1–E9. [PubMed]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016
2017-10-19
2021-04-13

Abstract:

Pneumonia caused by remains an important cause of disease and death in foals. The combination of a macrolide (erythromycin, azithromycin, or clarithromycin) with rifampin has been the recommended treatment for foals with clinical signs of infection caused by since the early 1980s with, until recently, only rare reports of resistance. Resistance to macrolides and rifampin in isolates of cultured from horses is increasing, with isolates resistant to all macrolides and rifampin now being cultured from up to 40% of infected foals at some farms. This text reviews the available data regarding antimicrobial resistance in , with emphasis on the molecular mechanisms of the recent emergence of resistance to macrolides and rifampin in equine isolates of .

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/5/5/ARBA-0004-2016.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016&mimeType=html&fmt=ahah

Tables

Antimicrobial Resistance in
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-1,properties={foaf_givenname=Steeve, foaf_name=Steeve Giguère, foaf_surname=Giguère, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-2,properties={foaf_givenname=Londa J., foaf_name=Londa J. Berghaus, foaf_surname=Berghaus, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-3,properties={foaf_givenname=Jennifer M., foaf_name=Jennifer M. Willingham-Lane, foaf_surname=Willingham-Lane, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016-aff3]]}]]
Citation: Giguère S, Berghaus L, Willingham-Lane J. 2017. Antimicrobial resistance in . microbiolspec 5(5): doi:10.1128/microbiolspec.ARBA-0004-2016
/content/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016.T1
TABLE 1
MIC data for isolates susceptible to macrolides and rifampin
Generic image for table

Click to view

TABLE 1

MIC data for isolates susceptible to macrolides and rifampin

Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.ARBA-0004-2016
/content/microbiolspec/10.1128/microbiolspec.ARBA-0004-2016.T2
TABLE 2
Mutations in the gene associated with rifampin resistance in
Generic image for table

Click to view

TABLE 2

Mutations in the gene associated with rifampin resistance in

Source: microbiolspec October 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.ARBA-0004-2016

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error