Progress in the fight against multidrug-resistant bacteria? A review of U.S. food and drug administration-approved antibiotics, 2010-2015

Annals of Internal Medicine

Volumn 165, Issue 5, 2016, Pages 363-372

  Deak, Dalia ^a   Outterson, Kevin ^b   Powers, John H ^c   Kesselheim, Aaron S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON UNIVERSITY   (United States)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; AVIBACTAM PLUS CEFTAZIDIME; BEDAQUILINE; CEFTAROLINE; CEFTOLOZANE PLUS TAZOBACTAM; DALBAVANCIN; FIDAXOMICIN; ORITAVANCIN; TEDIZOLID; ANTIINFECTIVE AGENT;

ABDOMINAL INFECTION; ANTIBIOTIC RESISTANCE; BACTERIAL SKIN DISEASE; COMMUNITY ACQUIRED PNEUMONIA; DATA BASE; DRUG APPROVAL; DRUG COST; DRUG EFFICACY; DRUG INDUSTRY; FOOD AND DRUG ADMINISTRATION; HUMAN; KIDNEY FAILURE; MORTALITY; MULTIDRUG RESISTANCE; MULTIDRUG RESISTANT TUBERCULOSIS; POSTMARKETING SURVEILLANCE; PRIORITY JOURNAL; REVIEW; TREATMENT DURATION; TREATMENT OUTCOME; UNITED STATES; URINARY TRACT INFECTION; BACTERIAL INFECTIONS; CLINICAL TRIAL (TOPIC); ECONOMICS; OUTCOME ASSESSMENT; STANDARDS;

ANTI-BACTERIAL AGENTS; BACTERIAL INFECTIONS; CLINICAL TRIALS AS TOPIC; DRUG APPROVAL; DRUG COSTS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; HUMANS; PATIENT OUTCOME ASSESSMENT; PRODUCT SURVEILLANCE, POSTMARKETING; UNITED STATES; UNITED STATES FOOD AND DRUG ADMINISTRATION;

EID: 84985947120     PISSN: 00034819     EISSN: 15393704     Source Type: Journal    
DOI: 10.7326/M16-0291     Document Type: Review

References (61)

1. U.S. Department of Commerce and Labor. Mortality Statistics, 1900 to 1904. Washington, DC: US Gov Pr Office; 1906.
2. Centers for Disease Control and Prevention (CDC). Control of infectious diseases. MMWR Morb Mortal Wkly Rep. 1999;48:621-9. [PMID: 10458535].
3. Laxminarayan R, Matsoso P, Pant S, Brower C, Røttingen JA, Klugman K, et al. Access to effective antimicrobials: A worldwide challenge. Lancet. 2016;387:168-75. [PMID: 26603918] doi:10.1016/S0140-6736(15)00474-2.
4. Armstrong GL, Conn LA, Pinner RW. Trends in infectious disease mortality in the United States during the 20th century. JAMA. 1999; 281:61-6. [PMID: 9892452].
5. Roberts RR, Hota B, Ahmad I, Scott RD 2nd, Foster SD, Abbasi F, et al. Hospital and societal costs of antimicrobial-resistant infections in a Chicago teaching hospital: implications for antibiotic stewardship. Clin Infect Dis. 2009;49:1175-84. [PMID: 19739972] doi:10.1086/605630.
6. Centers for Disease Control and Prevention. Antibiotic Resistance Threats in the United States, 2013. Atlanta, GA: Centers for Disease Control and Prevention; 2013.
7. World Health Organization. Antimicrobial Resistance: Global Report on Surveillance. Geneva: World Health Organization; 2014.
8. Morel CM, Mossialos E. Stoking the antibiotic pipeline. BMJ. 2010; 340:c2115. [PMID: 20483950] doi:10.1136/bmj.c2115.
9. Spellberg B, Powers JH, Brass EP, Miller LG, Edwards JE Jr. Trends in antimicrobial drug development: implications for the future. Clin Infect Dis. 2004;38:1279-86. [PMID: 15127341].
10. Projan SJ. Why is Big Pharma getting out of antibacterial drug discovery? Curr Opin Microbiol. 2003;6:427-30. [PMID: 14572532].
11. Coates A, Hu Y, Bax R, Page C. The future challenges facing the development of new antimicrobial drugs. Nat Rev Drug Discov. 2002;1:895-910. [PMID: 12415249].
12. Norrby SR, Nord CE, Finch R; European Society of Clinical Microbiology and Infectious Diseases. Lack of development of new antimicrobial drugs: A potential serious threat to public health. Lancet Infect Dis. 2005;5:115-9. [PMID: 15680781].
13. Outterson K, Powers JH, Seoane-Vazquez E, Rodriguez- Monguio R, Kesselheim AS. Approval and withdrawal of new antibiotics and other antiinfectives in the U.S., 1980-2009. J Law Med Ethics. 2013;41:688-96. [PMID: 24088160] doi:10.1111/jlme.12079.
14. Lewis K. Platforms for antibiotic discovery. Nat Rev Drug Discov. 2013;12:371-87. [PMID: 23629505] doi:10.1038/nrd3975.
15. So AD, Gupta N, Brahmachari SK, Chopra I, Munos B, Nathan C, et al. Towards new business models for R&D for novel antibiotics. Drug Resist Updat. 2011;14:88-94. [PMID: 21439891] doi:10.1016/j.drup.2011.01.006.
16. Outterson K, Powers JH, Daniel GW, McClellan MB. Repairing the broken market for antibiotic innovation. Health Aff (Millwood). 2015;34:277-85. [PMID: 25646108] doi:10.1377/hlthaff.2014.1003.
17. The White House. National Strategy for Combating Antibiotic- Resistant Bacteria. Washington, DC: US Gov Pr Office; 2014.
18. Centers for Disease Control and Prevention. Antibiotic resistance solutions initiative 2015. 2015. Accessed at www.cdc.gov/drugresistance/solutions-initiative/index.html on 13 October 2015.
19. World Health Organization. WHO Global Strategy for Containment of Antimicrobial Resistance. Geneva: World Health Organization; 2001.
20. Infectious Diseases Society of America. The 10 x '20 Initiative: pursuing a global commitment to develop 10 new antibacterial drugs by 2020. Clin Infect Dis. 2010;50:1081-3. [PMID: 20214473] doi:10.1086/652237.
21. Clift C, Gopinathan U, Morel C, Outterson K, Røttingen J, So A, eds; Chatham House Working Group on New Antibiotic Business Models. Towards a New Global Business Model for Antibiotics: Delinking Revenues from Sales. London: The Royal Institute of International Affairs; 2015.
22. Food and Drug Administration Safety and Innovation Act of 2013, 3187 (2013).
23. 21st Century Cures Act, 6 (2015).
24. Woodcock J. Three encouraging steps towards new antibiotics. FDA Voice Blog. 23 September 2014. Accessed at http://blogs.fda.gov/fdavoice/index.php/2014/09/three-encouraging-steps-towards-new-antibioticson 26 April 2016.
25. U.S. Food and Drug Administration. CDER new molecular entity (NME) & new BLA calendar year approvals as of December 31, 2010. 2010. Accessed at www.fda.gov/downloads/Drugs/DevelopmentApprovalProcess/HowDrugsareDevelopedandApproved/DrugandBiologicApprovalReports/UCM242677.pdf on 26 April 2016.
26. U.S. Food and Drug Administration. Novel new drugs summary 2012. 2013. Accessed at www.fda.gov/downloads/Drugs/DevelopmentApprovalProcess/DrugInnovation/UCM337830.pdf on 26 April 2016.
27. U.S. Food and Drug Administration. Novel new drugs 2011. 2012. Accessed at www.fda.gov/downloads/Drugs/DevelopmentApprovalProcess/DrugInnovation/ucm293663.pdf on 26 April 2016.
28. U.S. Food and Drug Administration. Novel new drugs 2014 summary. 2015. Accessed at www.fda.gov/downloads/Drugs/DevelopmentApprovalProcess/DrugInnovation/UCM430299.pdf on 26 April 2016.
29. U.S. Food and Drug Administration. Novel new drugs 2013 summary. 2014. Accessed at www.fda.gov/downloads/Drugs/DevelopmentApprovalProcess/DrugInnovation/UCM381803.pdf on 26 April 2016.
30. U.S. Food and Drug Administration. New Molecular Entity and New Therapeutic Biological Product Approvals for 2015. Silver Spring, MD: U.S. Food and Drug Administration; 2015. Accessed at www.fda.gov/Drugs/DevelopmentApprovalProcess/DrugInnovation/ucm430302.htm on 26 April 2016.
31. U.S. Food and Drug Administration. Postmarket requirements and commitments. 2013. Accessed at www.accessdata.fda.gov/scripts/cder/pmc on 26 April 2016.
32. U.S. Food and Drug Administration. Orange Book: Approved Drug Products with Therapeutic Equivalence Evaluations. 2013. Accessed at www.accessdata.fda.gov/scripts/cder/ob/default.cfm on 4 April 2016.
33. Red Book Online [online database]. Greenwood Village, CO: Truven Health Analytics. Accessed at http://sites.truvenhealth.com/redbook/index.html on 26 April 2016.
34. Rice LB. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE [Editorial]. J Infect Dis. 2008; 197:1079-81. [PMID: 18419525] doi:10.1086/533452.
35. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009;48:1-12. [PMID: 19035777] doi:10.1086/595011.
36. Prasad P, Sun J, Danner RL, Natanson C. Excess deaths associated with tigecycline after approval based on noninferiority trials. Clin Infect Dis. 2012;54:1699-709. [PMID: 22467668] doi:10.1093/cid/cis270.
37. U.S. Food and Drug Administration. Doribax (doripenem): drug safety communication-risk when used to treat pneumonia on ventilated patients. 2014. Accessed at www.fda.gov/Safety/MedWatch/SafetyInformation/SafetyAlertsforHumanMedicalProducts/ucm388328.htm on 4 April 2016.
38. Bassetti M, Merelli M, Temperoni C, Astilean A. New antibiotics for bad bugs: Where are we? Ann Clin Microbiol Antimicrob. 2013; 12:22. [PMID: 23984642] doi:10.1186/1476-0711-12-22.
39. Kotz J. Targeting tuberculosis. Nat Chem Biol. 2005. Accessed at www.nature.com/nchembio/journal/vaop/nprelaunch/full/nchembio002.html on 26 April 2016.
40. Wilcox MH, Corey GR, Talbot GH, Thye D, Friedland D, Baculik T; CANVAS 2 investigators. CANVAS 2: The second phase III, randomized, double-blind study evaluating ceftaroline fosamil for the treatment of patients with complicated skin and skin structure infections. J Antimicrob Chemother. 2010;65 Suppl 4:iv53-iv65. [PMID: 21115455] doi:10.1093/jac/dkq255.
41. Diacon AH, Pym A, Grobusch MP, de los Rios JM, Gotuzzo E, Vasilyeva I, et al; TMC207-C208 Study Group. Multidrug-resistant tuberculosis and culture conversion with bedaquiline. N Engl J Med. 2014;371:723-32. [PMID: 25140958] doi:10.1056/NEJMoa1313865.
42. International Conference on Harmonisation of Technical Requirements for Registration of Pharmaceuticals for Human Use. ICH harmonised tripartite guideline: choice of control group and related issues in clinical trials E10. 2000. Accessed at www.ich.org/fileadmin/Public-Web-Site/ICH-Products/Guidelines/Efficacy/E10/Step4/E10-Guideline.pdf on 26 April 2016.
43. U.S. Food and Drug Administration. Statistical Review, Ceftolozane/Tazobactam (Zerbaxa). Silver Spring, MD: U.S. Food and Drug Administration; 2014.
44. C.F.R. 314.500 (2015).
45. Cox E, Laessig K. FDA approval of bedaquiline-the benefit-risk balance for drug-resistant tuberculosis. N Engl J Med. 2014;371: 689-91. [PMID: 25140952] doi:10.1056/NEJMp1314385.
46. U.S. Food and Drug Administration. Medical Review: Dificid (Fidaxomicin). Silver Spring, MD: U.S. Food and Drug Administration; 2011.
47. Doshi P. Speeding new antibiotics to market: A fake fix? BMJ. 2015;350:1453. [PMID: 25814536] doi:10.1136/bmj.h1453.
48. Brigden G, Hewison C, Varaine F. New developments in the treatment of drug-resistant tuberculosis: clinical utility of bedaquiline and delamanid. Infect Drug Resist. 2015;8:367-78. [PMID: 26586956] doi:10.2147/IDR.S68351.
49. U.S. Government Accountability Office. Drug Safety: FDA Expedites Many Applications, but Data for Postapproval Oversight Need Improvement. Washington, DC: U.S. Government Accountability Office; 2015.
50. Prokocimer P, De Anda C, Fang E, Mehra P, Das A. Tedizolid phosphate vs linezolid for treatment of acute bacterial skin and skin structure infections: The ESTABLISH-1 randomized trial. JAMA. 2013; 309:559-69. [PMID: 23403680] doi:10.1001/jama.2013.241.
51. Corey GR, Good S, Jiang H, Moeck G, Wikler M, Green S, et al; SOLO II Investigators. Single-dose oritavancin versus 7-10 days of vancomycin in the treatment of gram-positive acute bacterial skin and skin structure infections: The SOLO II noninferiority study. Clin Infect Dis. 2015;60:254-62. [PMID: 25294250] doi:10.1093/cid/ciu778.
52. Boucher HW, Wilcox M, Talbot GH, Puttagunta S, Das AF, Dunne MW. Once-weekly dalbavancin versus daily conventional therapy for skin infection. N Engl J Med. 2014;370:2169-79. [PMID: 24897082] doi:10.1056/NEJMoa1310480.
53. U.S. Food and Drug Administration. Guidance on Providing Clinical Evidence of Effectiveness for Human Drugs and Biologics. Silver Spring, MD: U.S. Food and Drug Administration; 1998:4-5.
54. Actavis + Forest Laboratories. Forest Laboratories, Inc. reports fiscal year fourth quarter 2013 earnings per share of $0.17 including $0.08 per share of acquisition amortization [press release]. 23 April 2013. Accessed at http://investor.frx.com/press-release/corporate-news/forest-laboratories-inc-reports-fiscal-year-fourth-quarter-2013-earning on 13 October 2015.
55. Reichert JM. Trends in development and approval times for new therapeutics in the United States. Nat Rev Drug Discov. 2003;2:695- 702. [PMID: 12951576].
56. DiMasi JA, Hansen RW, Grabowski HG. The price of innovation: new estimates of drug development costs. J Health Econ. 2003;22: 151-85. [PMID: 12606142].
57. Rex JH, Goldberger M, Eisenstein BI, Harney C. The evolution of the regulatory framework for antibacterial agents. Ann N Y Acad Sci. 2014;1323:11-21. [PMID: 24797794] doi:10.1111/nyas.12441.
58. Alemayehu D, Quinn J, Cook J, Kunkel M, Knirsch CA. A paradigm shift in drug development for treatment of rare multidrugresistant gram-negative pathogens. Clin Infect Dis. 2012;55:562-7. [PMID: 22610933] doi:10.1093/cid/cis503.
59. Sertkaya A, Eyraud J, Birkenbach A, Franz C, Ackerley N, Overton V, et al. Analytical Framework for Examining the Value of Antibacterial Products. Washington, DC: U.S. Department of Health and Human Services; 2014.
60. U.S. Food and Drug Administration. Guidance for Industry: Expedited Programs for Serious Conditions-Drugs and Biologics. Silver Spring, MD: U.S. Food and Drug Administration; 2014.
61. The Orphan Drug Act of 1983 (1983).