Antimicrobial Resistance for Neisseria gonorrhoeae in the United States, 1988 to 2003: The Spread of Fluoroquinolone Resistance

  1. Susan A. Wang, MD, MPH;
  2. Alesia B. Harvey, BS;
  3. Susan M. Conner, MPH;
  4. Akbar A. Zaidi, PhD;
  5. Joan S. Knapp, PhD;
  6. William L.H. Whittington, PhD;
  7. Carlos del Rio, MD;
  8. Franklyn N. Judson, MD; and
  9. King K. Holmes, MD, PhD
  1. From the Centers for Disease Control and Prevention, Emory University School of Medicine, and Emory Center for AIDS Research, Atlanta, Georgia; Medtronic, Memphis, Tennessee; University of Washington, Seattle, Washington; and University of Colorado School of Medicine, Denver, Colorado.

    Abstract

    Background: Over the past 60 years, Neisseria gonorrhoeae has acquired clinically significant resistance to sulfonamides, tetracyclines, penicillins, and ciprofloxacin.

    Objective: To determine U.S. trends in the prevalence of antimicrobial resistance of N. gonorrhoeae from 1988 to 2003.

    Design: 16-year, multisite, sentinel surveillance for gonococcal isolate susceptibility through the Gonococcal Isolate Surveillance Project (GISP).

    Setting: Sexually transmitted disease clinics in 37 cities.

    Patients: Male patients with a total of 82 064 episodes of urethral gonorrhea.

    Measurements: Primary outcome measures included percentage of gonococcal isolates resistant to antimicrobials used to treat gonorrhea, percentage of patients treated with specific antimicrobials for gonorrhea, and trends of these measures over time.

    Results: The median age of patients was 26 years, and 74.1% of patients were African American. The proportion of men treated with penicillins for gonorrhea declined from 39.5% in 1988 to 0% in 1994, while the proportion of those receiving fluoroquinolone treatment increased from 0% in 1988 to 42.0% in 2003. Penicillin resistance peaked at 19.6% in 1991, then declined to 6.5% in 2003. Tetracycline resistance peaked at 25.8% in 1997 and declined to 14.4% in 2003. The first fluoroquinolone-resistant isolate was found in 1991. Nationally, 0.4% of isolates were fluoroquinolone-resistant in 1999 and were identified in 39% of GISP cities. By 2003, 4.1% of isolates were fluoroquinolone-resistant and were identified in 70% of GISP cities. Isolates with decreased susceptibility to ceftriaxone, cefixime, azithromycin, and spectinomycin remained rare. In 2001, 3 multidrug-resistant isolates with decreased susceptibility to cefixime were identified.

    Limitation: Sentinel surveillance may not fully reflect trends for all patients with gonorrhea in the United States.

    Conclusions: Prevalence of penicillin resistance has declined in the years since gonorrhea treatment with penicillin was discontinued. Fluoroquinolone-resistant N. gonorrhoeae infections continue to increase at a time when fluoroquinolone use has increased. Ongoing nationwide and local antimicrobial susceptibility monitoring is crucial to ensure appropriate treatment of gonorrhea.

    Article and Author Information

    • Acknowledgments: The authors thank Laura Doyle, Josephine Ehret, Connie Lenderman, James Thomas, and Karen Winterscheid for antimicrobial susceptibility testing and specimen handling. They acknowledge the substantial contributions of the sexually transmitted disease clinics and the local laboratories that participated in the Gonococcal Isolate Surveillance Project during 1988 to 2003. They also thank Maya Sternberg for providing additional statistical input and Gary W. Procop and Hillard S. Weinstock for project support.

    • Grant Support: The Gonococcal Isolate Surveillance Project is funded by the Centers for Disease Control and Prevention, U.S. Department of Health and Human Services.

    • Potential Financial Conflicts of Interest:Grants received: W.L.H. Whittington (Centers for Disease Control and Prevention, National Institute of Allergy and Infectious Diseases).

    • Requests for Single Reprints: Susan A. Wang, MD, MPH, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Mail Stop G-37, 1600 Clifton Road, Atlanta, GA 30333; e-mail, sjw8{at}cdc.gov.

    • Current Author Addresses: Dr. Wang: National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Mail Stop G-37, 1600 Clifton Road, Atlanta, GA 30333.

    • Ms. Harvey and Dr. Zaidi: National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Mail Stop E-63, 1600 Clifton Road, Atlanta, GA 30333.

    • Ms. Conner: Medtronic, 2600 Sofamor Danek Drive, A.3.040, Memphis, TN 38132.

    • Dr. Knapp: National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Mail Stop A-12, 1600 Clifton Road, Atlanta, GA 30333.

    • Dr. Whittington: Department of Medicine, R/T Room 627 (Box 359742), Harborview Medical Center, 300 Ninth Avenue, Seattle, WA 98104.

    • Dr. del Rio: Department of Medicine, Grady Memorial Hospital, 69 Jesse Hill Jr. Drive, Atlanta, GA 30303.

    • Dr. Judson: Departments of Medicine and Preventive Medicine, University of Colorado Health Sciences Center, 2200 East 9th Avenue, Box B-119, Denver, CO 80262.

    • Dr. Holmes: Center for AIDS and STD, University of Washington, Box 359931, 325 Ninth Avenue, Seattle, WA 98104.

    • Author Contributions: Conception and design: S.A. Wang, J.S. Knapp, F.N. Judson.

    • Analysis and interpretation of the data: S.A. Wang, A.A. Zaidi, J.S. Knapp, W.L.H. Whittington, F.N. Judson, K.K. Holmes.

    • Drafting of the article: S.A. Wang, A.A. Zaidi, C. del Rio, K.K. Holmes.

    • Critical revision of the article for important intellectual content: S.A. Wang, A.A. Zaidi, J.S. Knapp, W.L.H. Whittington, C. del Rio, F.N. Judson, K.K. Holmes.

    • Final approval of the article: S.A. Wang, S.M. Conner, A.A. Zaidi, J.S. Knapp, W.L.H. Whittington, C. del Rio, F.N. Judson, K.K. Holmes.

    • Provision of study materials or patients: W.L.H. Whittington, C. del Rio, F.N. Judson.

    • Statistical expertise: S.A. Wang, A.A. Zaidi.

    • Obtaining of funding: S.A. Wang.

    • Administrative, technical, or logistic support: S.A. Wang, A.B. Harvey, S.M. Conner, F.N. Judson.

    • Collection and assembly of data: S.A. Wang, A.B. Harvey, S.M. Conner, W.L.H. Whittington, F.N. Judson.

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