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

Susan A. Wang, MD, MPH; Alesia B. Harvey, BS; Susan M. Conner, MPH; Akbar A. Zaidi, PhD; Joan S. Knapp, PhD; William L.H. Whittington, PhD; Carlos del Rio, MD; Franklyn N. Judson, MD; and King K. Holmes, MD, PhD
[+] Article and Author Information

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.


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@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.


Ann Intern Med. 2007;147(2):81-88. doi:10.7326/0003-4819-147-2-200707170-00006
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From 1988 to 2003, GISP collected 82 064 isolates from men with urethral gonorrhea who attended sexually transmitted disease clinics in 37 cities (range, 21 to 30 cities per year). A median of 5088 isolates were collected each year (range, 4544 to 6552 isolates per year) (Table 1). Clinics in 16 cities participated for all 16 years and contributed 53 593 (65.3%) of the isolates. When we restricted analyses to these clinics, demographic or antimicrobial resistance trends were not affected.

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Figure 1.
Gonorrhea treatment for Gonococcal Isolate Surveillance Project patients, 1988 to 2003.

*“Other” for 2003 (3.2%) includes no therapy (1.8%) and macrolide (0.6%), levofloxacin (0.4%), and other (0.4%) therapy. †“Other cephalosporins” for 2003 (4.6%) include cefpodoxime, 200 mg (4.0%); cefpodoxime, 400 mg (0.5%); and ceftizoxime (0.1%). ‡Marketing of cefixime tablets in the United States was discontinued in October 2002.

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Figure 2.
Percentage of Gonococcal Isolate Surveillance Project isolates with resistance or intermediate resistance to ciprofloxacin, 1990 to 2003.
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Figure 3.
Penicillin resistance (top) and tetracycline resistance (bottom) among Gonococcal Isolate Surveillance Project isolates, 1988 to 2003.

PPNG = penicillinase-producing N. gonorrhoeae (β-lactamase–positive; tetracycline MIC <16.0 µg/mL); TRNG = plasmid-mediated, tetracycline-resistant N. gonorrhoeae (β-lactamase–negative; tetracycline MIC ≥16.0 µg/mL); PPNG-TRNG = N. gonorrhoeae with plasmid-mediated resistance to both penicillin and tetracycline (β-lactamase–positive; tetracycline MIC ≥16.0 µg/mL); PenR = chromosomally mediated, penicillin-resistant N. gonorrhoeae (β-lactamase–negative; penicillin MIC ≥2.0 µg/mL; tetracycline MIC <2.0 µg/mL); TetR = chromosomally mediated, tetracycline-resistant N. gonorrhoeae (β-lactamase–negative; penicillin MIC <2.0 µg/mL; tetracycline MIC, 2.0 to 8.0 µg/mL); CMRNG = N. gonorrhoeae with chromosomally mediated resistance to penicillin and tetracycline (β-lactamase–negative; penicillin MIC ≥2.0 µg/mL; tetracycline MIC, 2.0 to 8.0 µg/mL); MIC = minimum inhibitory concentration.

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Comments

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What about the DNA?
Posted on July 16, 2007
Daniel G. Arkfeld
USC Keck School of Medicine
Conflict of Interest: None Declared

It is with great interest that I reviewed the article "Antimicrobial Resistance for Neisseria gonorrhoeae in the United States, 1988 to 2003: The Spread of Fluoroquinolone Resistance" by Wang et al which summarizes the growing issue of resistance in treating STD's. However, I was surprised to see the high incidence of gonorrhoeae in 74.1% of African American male patients. This may lead to a false racial bias about the incidence of GC in the United States. I question the validity of this number due to the lack of DNA testing of urine samples which is the preferred method in many private practices and clinics. This test is more expensive(cpt code 87591) with a cost of $69.00 for the N. gonorrhoeae test alone. The urine DNA testing is also routinely done for C. trachomatis at an additional cost of $69.00. Patients undergoing the DNA urine tests thus would need $138.00 plus the costs of the office visit and subsequent medicines which often are given empirically due to lack of followup. Thus, patients receiving such care would usually be insured and possibly of more varied ethnicity. Additional studies of all socioeconomic classes is warranted.

Conflict of Interest:

None declared

ANTIBIOTIC CYCLING: A NOVEL STRATEGY TO DECREASE ANTIMICROBIAL RESISTANCE FOR Neisseria gonorrhoeae
Posted on July 30, 2007
Shailendra Kapoor
University of Illinois at Chicago, Chicago, IL
Conflict of Interest: None Declared

The article by Wang et al was highly interesting and provided conclusive evidence that Gonococcal resistance to fluoroquinolones is on the rise. (1) Given the ever increasing menace of sexually transmitted infections, especially gonorrhea, new strategies are needed to overcome this situation.

One plausible method might be "antibiotic cycling". (2) This is a strategy in which antibiotics from different antibiotic classes are alternated periodically over a set period of time ultimately returning to the original antibiotic. (3) This in a way prevents the development of resistance. For instance in one recent 2 year study antibiotic cycling was shown to significantly decrease the incidence of gram positive coccal infections. (4) In this study fluoroquinolones as well as cephalosporins were used in rotation with other antibiotics such as imipenems. In the context of gonorrhea, this would mean restricting the use of fluoroquinolones for a certain time period and instead using another alternative such as penicillins or cephalosporins for that duration. Antibiotic cycling has been shown to work in other situations (5) and applying it for the long term management of gonorrhea seems a reasonable strategy.

REFERENCES

1. Wang SA, Harvey AB, Conner SM, Zaidi AA, Knapp JS, Whittington WL, et al. Antimicrobial resistance for Neisseria gonorrhoeae in the United States, 1988 to 2003: the spread of fluoroquinolone resistance. Ann Intern Med. 2007;147(2):81-8.

2. Masterton RG. Antibiotic cycling: more than it might seem? J Antimicrob Chemother. 2005;55(1):1-5.

3. Pujol M, Gudiol F. Evidence for antibiotic cycling in control of resistance. Curr Opin Infect Dis. 2001;14(6):711-5.

4. Raymond DP, Pelletier SJ, Crabtree TD, Gleason TG, Hamm LL, Pruett TL, et al. Impact of a rotating empiric antibiotic schedule on infectious mortality in an intensive care unit. Crit Care Med. 2001;29(6):1101-8.

5. Dominguez EA, Smith TL, Reed E, Sanders CC, Sanders WE,Jr. A pilot study of antibiotic cycling in a hematology-oncology unit. Infect Control Hosp Epidemiol. 2000;21(1 Suppl):S4-8.

Conflict of Interest:

None declared

Higher gonorrhea rates among African Americans than among whites in the United States
Posted on October 15, 2007
Susan A. Wang
Centers for Disease Control & Prevention
Conflict of Interest: None Declared

Dear Dr. Arkfeld,

Thank you for your letter.

As noted in the Results section reviewing the demographic characteristics of GISP patients, African American men were underrepresented in GISP compared with their proportion among nationally reported male patients with gonorrhea: during 1988-2003, 74.1% of GISP patients were African American while during that same time period, 83.0% of male patients reported through the national notifiable disease reporting system to have gonorrhea in the United States were African American [1]. Reporting of gonorrhea cases occurs as a result of healthcare provider and/or laboratory reporting of gonorrhea cases to local health departments which, in turn, report these results to the Centers for Disease Control and Prevention. In 2005, the gonorrhea rate among African Americans was 18 times greater than the rate for whites [2]; in years prior to 2005, the difference in gonorrhea rates between the two groups was larger (see Figure 17 [3]).

It is possible that persons who are symptomatically treated for gonorrhea without laboratory confirmation may be less likely to get reported to health departments but persons who undergo laboratory testing, such as nucleic acid amplification diagnostic tests, and have positive gonococcal test results are likely to get reported due to health department reporting requirements for laboratories.

Sincerely,

Susan A. Wang, MD, MPH

National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention

Centers for Disease Control & Prevention

References

1. Wang SA, Harvey AB, Conner SM, et al. Antimicrobial resistance for Neisseria gonorrheoae in the United States, 1988 to 2003: the spread of fluoroquinolone resistance. Ann Intern Med 2007;147:81-88.

2. http://www.cdc.gov/std/stats/gonorrhea.htm

3. Centers for Disease Control and Prevention, Figure 17. Gonorrhea "” Rates by race/ethnicity: United States, 1996"“2005. http://www.cdc.gov/std/stats/figures/fig17.htm

Conflict of Interest:

None declared

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