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Risk of Recurrent Nontyphoid Salmonella Bacteremia in HIV-Infected Patients in the Era of Highly Active Antiretroviral Therapy and an Increasing Trend of Fluoroquinolone Resistance

  1. Chien-Ching Hung1,
  2. Min-Nan Hung5,
  3. Po-Ren Hsueh2,
  4. Sui-Yuan Chang3,
  5. Mao-Yuan Chen1,
  6. Szu-Min Hsieh1,
  7. Wang-Huei Sheng1,
  8. Hsin-Yun Sun1,
  9. Yu-Tsung Huang1,
  10. Yi-Chun Lo1,
  11. Chin-Fu Hsiao4,6, and
  12. Shan-Chwen Chang1
  1. 1Department of Internal Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine, Taiwan
  2. 2Department of Laboratory Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine, Taiwan
  3. 3Department of Clinical Laboratory Sciences and Medical Biotechnology, National Taiwan University College of Medicine, Taiwan
  4. 4National Taipei College of Nursing, Taipei, Taiwan
  5. 5Centers for Diseases Control, Taipei, Taiwan
  6. 6Division of Biostatistics and Bioinformatics, National Health Research Institutes, Zhunan Town, Taiwan
  1. Reprints or correspondence: Dr. Chien-Ching Hung, Dept. of Internal Medicine, National Taiwan University Hospital, 7 Chung-Shan South Rd., Taipei, Taiwan (hcc0401{at}ntu.edu.tw).
 
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Abstract

Background. Risk of recurrent nontyphoid Salmonella (NTS) bacteremia and trends of antimicrobial resistance of NTS remain unknown in human immunodeficiency virus (HIV)-infected patients receiving highly active antiretroviral therapy (HAART).

Methods. Ninety-three patients who received a diagnosis of NTS bacteremia from June 1994 through June 2006 were prospectively followed up. Incidence of recurrent NTS bacteremia was compared between the pre-HAART era (June 1994–March 1997) and the HAART era (April 1997–June 2006). Prevalence of antimicrobial resistance was compared among the NTS isolates obtained in the pre-HAART era, the early HAART era (April 1997–June 2002), and the late HAART era (July 2002–June 2006).

Results. Compared with patients enrolled in the pre-HAART era, patients who received HAART had an incidence of recurrent NTS bacteremia that was significantly reduced by 96%; the incidence of recurrent NTS bacteremia was 2.56 cases per 100 person-years in the HAART era, compared with 70.56 cases per 100 person-years in the pre-HAART era (rate ratio, 0.036; 95% confidence interval, 0.012–0.114; P < .001). In the HAART era, the incidence of recurrent NTS bacteremia did not increase among patients receiving fluoroquinolone prophylaxis for ⩽30 days (1.69 cases per 100 person-years), compared with among patients receiving fluoroquinolones for >30 days (3.95 cases per 100 person-years), with a rate ratio of 0.43 (95% confidence interval, 0.07–2.58). Although resistance to ampicillin, cotrimoxazole, and chloramphenicol decreased, the proportion of NTS isolates resistant to fluoroquinolones increased from 0% in the pre-HAART era to 6.2% in the early HAART era and 34.2% in the late HAART era (P = .002).

Conclusions. The risk of recurrent NTS bacteremia decreased significantly in the HAART era, although NTS isolates obtained from HIV-infected patients were increasingly resistant to fluoroquinolones.

Nontyphoid Salmonella (NTS) is the leading etiology of community- acquired bacteremia in patients with HIV infection in developed or developing countries [1,2,3,4,5,6,7,8–9]. The incidence of NTS bacteremia was found to be 20- to 100-fold higher among HIV-infected patients than among HIV-uninfected patients [10, 11]. In HIV-infected patients, NTS bacteremia tends to occur in patients with low CD4 lymphocyte counts and is associated with a high mortality rate in patients without access to appropriate antimicrobial therapy [1, 2, 6, 7, 12].

Before the introduction of HAART in 1996, recurrences of NTS bacteremia had been well described in HIV-infected patients despite appropriate antimicrobial therapy [12,13,14,15–16]. Indeed, recurrent NTS bacteremia is one of the several AIDS-defining opportunistic infectious diseases that are caused by bacteria [17]. In the pre-HAART era, as many as 43% of the patients with NTS bacteremia had a recurrent episode, and multiple recurrences were not uncommon [12]. The risk of recurrent NTS bacteremia may be related to the geographic prevalence of NTS infection, invasiveness of the infecting strains, the type and duration of antibiotic therapy prescribed for NTS bacteremia, the immune status of the patients, and receipt of antiretroviral therapy [12, 16, 18, 19].

After the introduction of HAART, the incidences of several major AIDS-related opportunistic infections and the mortality rate have decreased, and primary and secondary prophylaxis against several opportunistic infections can be safely discontinued in patients responding to HAART [20]. Similarly, the risk of bacteremia and associated mortality decrease with standard clinical management and the introduction of HAART [8, 9, 21, 22]. As for NTS bacteremia, clinical studies to assess the optimal duration of secondary prophylaxis for NTS bacteremia in HIV-infected patients are lacking, although long-term secondary prophylaxis with ciprofloxacin has been recommended by the Department of Health and Human Services guidelines [23]. However, the recommendation does not take into consideration the increasing trends of NTS isolates with reduced susceptibility or resistance to fluoroquinolones and other antibiotics worldwide [24,25,26,27–28]. With such increasing trends, prescription of orally bioavailable antibiotics as secondary prophylaxis will become problematic in this population at high risk for recurrent NTS bacteremia.

In this study, we aimed to compare the incidence of recurrent NTS bacteremia before and after the introduction of HAART and to assess the trends of fluoroquinolone resistance of NTS isolates in HIV-infected patients in Taiwan.

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Methods

Setting. All HIV-infected patients with NTS bacteremia diagnosed at the National Taiwan University Hospital from June 1994 through June 2006 were identified from the database of our prospective observational cohort study [29]. A standardized case record form was used to collect clinical and microbiological data for the patients with NTS bacteremia. During the 12-year study period, 1397 HIV-infected patients were consecutively enrolled in the cohort study. Most of the patients were in the late stage of HIV infection, with a median CD4 cell count of 96 cells/mL (range, 0–1202 cells/mL); 62.4% of the patients had a baseline CD4 cell count <200 cells/mL.

During the study period, standard treatment of NTS bacteremia was therapy with ceftriaxone or other third-generation cephalosporins for 7–14 days, followed by ciprofloxacin administered at 500 mg twice daily or other newer fluoroquinolones as secondary prophylaxis. Although secondary prophylaxis with fluoroquinolones for NTS bacteremia was not discontinued in the pre-HAART era, the duration of fluoroquinolone prophylaxis in patients receiving HAART was at the discretion of treating physicians. HAART, introduced into Taiwan in April 1997, was defined as the combination of at least 3 antiretroviral agents containing protease inhibitors or nonnucleoside reverse-transcriptase inhibitors and nucleoside reverse-transcriptase inhibitors. Antimicrobial prophylaxis against AIDS-related opportunistic infections and initiation of HAART were prescribed by following the guidelines, with the exception of rifabutin for prophylaxis against Mycobacterium avium complex because of concerns over the emergence of rifamycin-resistant Mycobacterium tuberculosis.

Laboratory investigations. Isolation of Salmonella species from blood samples was performed according to standard methods. Isolates of Salmonella serogroups B and C were further identified to the serotype level, according to the Kauffman and White scheme, by using somatic and flagellar antigens (Denka Seiken) and also by conventional methods and the Phoenix System (panel type, NMIC/ID4; Becton Dickson).

Disk diffusion susceptibility tests on the NTS isolates and interpretation of the results were performed by following the guidelines provided by the Clinical and Laboratory Standards Institute (formerly NCCLS) [30]. MICs of ampicillin, chloramphenicol, trimethoprim-sulfamethoxazole (cotrimoxazole), ceftriaxone, and ciprofloxacin were determined using the agar dilution method according to the Clinical and Laboratory Standards Institute guidelines [31].

Genotyping of the isolates from the patients with recurrent NTS bacteremia was determined by the pulsotypes generated by PFGE. The DNA extraction and purification were also performed as described previously [32]. In brief, the DNA was digested by the restriction enzymes SpeI, XbaI, and BlnI, and the restriction fragments were separated in a CHEF DRIII unit (Bio-Rad). Interpretation of the PFGE profiles was in accordance with the description by Tenover et al. [33]. Isolates belonging to the similar pulsotypes (within 6-band differences) by each of the 3 restriction enzymes were defined as the same genotypes. Isolates with identical pulsosubtypes (no band differences) by the 3 restriction enzymes were defined as the same genosubtypes (i.e., clones).

Plasma HIV RNA load was quantified using the Cobas Amplicor HIV-1 Monitor test (Cobas Amplicor, version 1.5; Roche Diagnostics) with a lower detection limit of 400 copies/mL, and CD4 cell count was determined using FACFlow (BD FACS Calibur; Becton Dickinson). The CD4 cell counts and HIV RNA load were monitored every 3–4 months.

Statistical analysis. All statistical analyses were performed using SAS statistical software, version 8.1 (SAS Institute). Categorical variables were compared using χ2 or Fisher's exact test, whereas noncategorical variables were compared using the Wilcoxon rank sum test. The χ2 test was used to test the trends of resistance to ampicillin, chloramphenicol, cotrimoxazole, ceftriaxone, and ciprofloxacin of NTS strains that were isolated from June 1994 through March 1997 (the pre-HAART era), from April 1997 through June 2002 (the early HAART era), and from July 2002 through June 2006 (the late HAART era). In cases of recurrence, only the antibiotic-susceptibility results of the first isolates were analyzed. The incidence rate of recurrent NTS bacteremia was calculated as number of episodes per 100 person-years of observation. Exact 95% CIs for incidence rates were calculated on the basis of the Poisson distribution. The follow-up duration of the patients enrolled in the pre-HAART era was from the date when NTS bacteremia was first diagnosed to the date of last clinic contact, date of death, or 30 September 1997, whichever occurred first, whereas that of the patients enrolled in the HAART era was the date of last clinic contact, date of death, or 31 December 2006, whichever occurred first. The generalized estimating equations were used to assess the association between duration of fluoroquinolone therapy and NTS recurrences [34].

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Results

Prevalence of NTS bacteremia and incidence rate of recurrent NTS bacteremia. During the 12-year study period, 93 (6.7%) of 1397 HIV-infected patients developed 105 episodes of NTS bacteremia, including 16 (9.1%) of 175 patients in the pre-HAART era and 77 (6.3%) of 1222 patients in the HAART era (P = .22). The clinical and demographic characteristics of the 93 patients with NTS bacteremia are shown in table 1. In the pre-HAART era, 4 (25%) of 16 patients had recurrent NTS bacteremia, compared with 3 (3.9%) of 77 patients in the HAART era (OR, 8.222; 95% CI, 1.633–41.4; P = .03).

In the pre-HAART era, 16 patients whose median CD4 cell count at NTS bacteremia diagnosis was 8 cells/µL (range, 1–144 cells/µL) developed 23 episodes of NTS bacteremia: 2 patients with 3 episodes each, 3 patients with 2 episodes each, and 11 patients with 1 episode each. The median interval between 2 episodes of NTS bacteremia among the patients with recurrences was 45.5 days (range, 18–136 days). None of the patients with recurrent NTS bacteremia interrupted secondary prophylaxis with ciprofloxacin and/or cotrimoxazole. As of 30 September 1997, 12 deaths and 2 losses to follow-up had occurred. The total observation duration was 9.92 person-years in the pre-HAART era, and the incidence rate of recurrent NTS bacteremia was 70.56 cases per 100 person-years (95% CI, 28.27–145.4 cases per 100 person-years).

In the HAART era, 77 patients whose median CD4 cell count was 20 cells/µL (range, 0–431 cells/µL) developed 82 episodes of NTS bacteremia. One patient with primary CNS lymphoma who was receiving cytoreductive chemotherapy containing steroids developed 1 recurrent episode. Each of 2 other patients who did not adhere to HAART and antibiotic therapy developed 2 recurrent episodes. The median interval between 2 episodes of NTS bacteremia of each patient with recurrences was 59 days (range, 15–543 days). Genotyping results confirmed that all of the recurrent episodes in each case patient were caused by strains with PFGE patterns identical to those of the first isolate (figure 1). The total observation duration was 195.12 person-years, and therefore, the incidence rate of NTS relapse was 2.56 cases per 100 person-years (95% CI, 0.83–5.98 cases per 100 person-years). Compared with the incidence rate for patients enrolled in the pre-HAART era, patients enrolled in the HAART era had a statistically significant reduced risk of recurrent NTS bacteremia, with a rate ratio of 0.036 (95% CI, 0.011–0.114; P < .001).

Figure 1
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Figure 1

Genotyping of 12 isolates of nontyphoid Salmonella obtained from 7 patients in the HAART era, determined by the pulsotypes that are generated by PFGE. Identical PFGE patterns are shown for 3 patients with recurrent nontyphoid Salmonella bacteremia: patient 1, isolates 1 and 2; patient 2, isolates 3–5; and patient 3, isolates 6–8.

Serotypes and changes in the antimicrobial susceptibility of NTS isolates. Antimicrobial susceptibility by disk diffusion method of 13 available isolates obtained during the pre-HAART era and 70 isolates obtained during the HAART era are shown in table 2. There were no demographic or clinical differences between 83 patients with antimicrobial susceptibility test results and 10 patients without such results (data not shown). In the 3 study periods (i.e., the pre-HAART, early HAART, and late HAART eras), the number of NTS isolates that were resistant to ampicillin, cotrimoxazole, and chloramphenicol was decreasing, and all of the isolates remained susceptible to ceftriaxone in each of the 3 study periods (table 2 and Figure 2). In contrast, the prevalence of NTS isolates that were ciprofloxacin-resistant increased from 0% in the pre-HAART era to 6.2% in the early HAART era and 34.2% in the late HAART era (P = .002) (table 2 and Figure 2).

Figure 2
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Figure 2

Trends of antimicrobial resistance of nontyphoid Salmonella isolates to ampicillin, chloramphenicol, cotrimoxazole, ceftriaxone, and ciprofloxacin for 3 study periods: the pre-HAART era (June 1994–March 1997), the early HAART era (April 1997–June 2002), and the late HAART era (July 2002–June 2006).

Table 1
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Table 1

Characteristics of 93 nonhemophiliac HIV-infected patients aged ⩾15 years with nontyphoid Salmonella (NTS) bacteremia in the pre-HAART (June 1994–March 1997) and HAART (April 1997–June 2006) eras.

Table 2
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Table 2

Antimicrobial susceptibility of nontyphoid Salmonella isolates causing bacteremia determined using disc diffusion methods in the pre-HAART (June 1994–March 1997), early HAART (April 1997–June 2002), and late HAART (July 2002–June 2006) eras.

Of the 82 isolates (88.2%) that were serotyped, 23 were Salmonella enterica serotype Choleraesuis, 29 were S. enterica serotype Enteritidis, and 30 were S. enterica serotype Typhimurium. Fourteen isolates (63.9%) of S. Choleraesuis were ciprofloxacin resistant according to the disc diffusion method, compared with 1 isolate (3.4%) of S. Enteritidis and none of the S. Typhimurium isolates. Nine (60.0%) of the 15 ciprofloxacin-resistant isolates were also resistant to all other antibiotics tested, except ceftriaxone.

Seventy-two NTS isolates were available and had MICs determined. The MIC90 values of ampicillin, chloramphenicol, cotrimoxazole, and ceftriaxone remained largely unchanged throughout the 3 study periods (table 2). In contrast, the MIC90 of ciprofloxacin increased significantly, from 0.25 µg/mL in the pre-HAART era to 16 µg/mL in the late HAART era (table 2).

Incidence rate of recurrent NTS bacteremia and duration of secondary fluoroquinolone prophylaxis in the HAART era. As of 31 December 2006, 70 patients (90.9%) enrolled during the HAART era started HAART, and 30 deaths (39.0% of patients) and 6 losses to follow-up (7.8% of patients) occurred. The median interval between the first episode of NTS bacteremia and death was 160 days (range, 2–1558 days). Six (20%) of the 30 deaths in the HAART era occurred within 30 days after diagnosis of NTS bacteremia (median duration, 10 days; range, 2–26 days). Fifty-six patients received secondary prophylaxis with fluoroquinolones for a median duration of 22 days (range, 3–669 days): 35 (62.5%) for ⩽30 days and only 5 (8.9%) for>180 days. At discontinuation of fluoroquinolone therapy, the median CD4 cell count was 41 cells/µL (range, 1–588 cells/µL), and the median plasma HIV RNA load was 1440 copies/mL (range, <400 to >750,000 copies/mL). Of the 53 patients who survived >30 days after diagnosis of NTS bacteremia, duration of fluoroquinolone therapy was a median of 26 days (range, 7–669 days); 81.1% of the patients received fluoroquinolones for <90 days. After HAART, the median CD4 cell count increased from 20 cells/µL at baseline to 216 cells/µL (range, 0–985 cells/µL) at the end of follow-up (P < .001).

Of the 15 patients with NTS isolates that were resistant to ampicillin, chloramphenicol, cotrimoxazole, and ciprofloxacin, 1 died of primary CNS lymphoma 10 days after NTS bacteremia was diagnosed; 4 received fluoroquinolones for tuberculosis (1 patient) and disseminated M. avium complex infection (3 patients); and 10 other patients, including 8 patients with S. Choleraesuis isolates, did not receive ciprofloxacin prophylaxis, although they continued to receive cotrimoxazole prophylaxis for pneumocystosis (at a trimethoprim dosage of 160 mg daily). However, there were no recurrences during HAART for a median observation duration of 745 days (range, 160–2337 days). With HAART, the CD4 cell count of the patients increased from a median of 62 cells/µL (range, 7–431 cells/µL) at diagnosis of NTS bacteremia to 344 cells/µL (range, 140–814 cells/µL) at the end of follow-up.

The incidence of recurrent NTS bacteremia in patients receiving fluoroquinolone prophylaxis for ⩽30 days, including those who did not receive fluoroquinolone prophylaxis, did not increase, compared with the incidence in patients receiving fluoroquinolones for >30 days. In the former group of patients, the incidence of recurrent NTS bacteremia was 1.69 cases per 100 person-years (95% CI, 0.19–6.09 cases per 100 person-years), while in the latter, the incidence was 3.95 cases per 100 person-years (95% CI, 0.79–11.45 cases per 100 person-years) (rate ratio, 0.43; 95% CI, 0.07–2.58; P = .61). By generalized estimating equations, we were not able to find an association between duration of ciprofloxacin use and the incidence of recurrent NTS bacteremia after adjustment for CD4 cell count and plasma HIV RNA load at discontinuation of fluoroquinolone prophylaxis (P = .11).

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Discussion

In this study, we found that the incidence of recurrent NTS bacteremia was significantly reduced by 96% among patients who achieved favorable immunological and virological responses after receiving HAART, compared with the incidence among patients enrolled in the pre-HAART era (table 1). Despite an increasing trend of fluoroquinolone-resistant NTS, a shorter duration of secondary prophylaxis did not appear to increase the risk of recurrent NTS bacteremia in patients receiving HAART.

The type of antibiotic therapy prescribed for NTS bacteremia and secondary prophylaxis may have been related to the risk of recurrences before HAART was introduced. In an African study, chloramphenicol failed to eradicate NTS bacteremia in 47% of the episodes [12]. After treatment with ampicillin or extended-spectrum cephalosporins for 2–3 weeks, recurrent NTS bacteremia continued to occur [13, 14]. Ciprofloxacin prophylaxis administered for 1–8 months was found to effectively prevent recurrent NTS bacteremia in 4 HIV-infected patients [15]. In this study, we found that 25% of the patients enrolled in the pre-HAART era developed recurrences while they were receiving 175 days of ciprofloxacin prophylaxis, after receiving ceftriaxone or ciprofloxacin as initial therapy for NTS bacteremia. It was not until the introduction of HAART that the incidence of recurrent NTS bacteremia significantly decreased, from 70.56 cases per 100 person-years to 2.56 cases per 100 person-years (table 1).

Recurrent NTS bacteremia has been found to occur mainly in patients with low CD4 cell counts. In this study, patients presenting with NTS bacteremia had depleted CD4 cell counts (median CD4 cell count, 8 cells/µL and 20 cells/µL in the pre-HAART and HAART eras, respectively) (table 1). They would have been at high risk for recurrences if their CD4 cell counts had remained low without antiretroviral therapy. After HAART, the median CD4 cell count increased from 20 cells/µL to 216 cells/µL, and >60% of the patients had achieved undetectable HIV RNA loads. Therefore, our study suggests that favorable immunological and virological responses contributed to a decreased risk of recurrent NTS bacteremia.

In our study, we found a significant increase in ciprofloxacin-resistant NTS isolates obtained from HIV-infected patients. The increase may be related to the emergence of fluoroquinolone resistance in S. Choleraesuis in Taiwan [25, 32], immunosuppression, and prior use of antimicrobial agents [35]. In patients with and patients without HIV infection, antimicrobial-resistant NTS strains cause more cases of bacteremia and more hospitalizations than do strains that are pansusceptible [19, 35]. Despite drug resistance, recurrences did not develop in 10 of our patients who were infected with ciprofloxacin-resistant NTS and did not receive effective secondary prophylaxis. Similar to the studies of the discontinuation of primary or secondary prophylaxis for several opportunistic infections in the HAART era, we believe that significant increases in CD4 cell counts have conferred protection against recurrences in patients who did not receive fluoroquinolones as secondary prophylaxis.

The appropriate duration of fluoroquinolone prophylaxis for HIV-infected patients receiving HAART remains unknown, despite the recommendation for long-term secondary prophylaxis with ciprofloxacin by the Department of Health and Human Services guidelines [23]. Our preliminary analysis, performed in the absence of ciprofloxacin resistance, suggested that a 30-day course of ciprofloxacin prophylaxis appeared to be effective in preventing recurrent NTS bacteremia in patients receiving HAART [37]. In this study, which involved a larger sample size and a longer observation duration, we further demonstrated that the incidence of recurrent NTS bacteremia in patients receiving fluoroquinolones for ⩽30 days was similar to that in those receiving fluoroquinolones for >30 days in the era of HAART.

There are several limitations to our current study. First, this is not a randomized clinical trial, and the duration of ciprofloxacin prophylaxis was not predetermined before this observational study was started. In view of a low incidence of recurrent NTS bacteremia in the HAART era, a large study population is needed to determine the appropriate timing of discontinuation of ciprofloxacin prophylaxis after HAART. Second, a large proportion of patients in this study who survived NTS bacteremia received HAART with virological suppression. Our results may not be generalizable to patients who experience virological and immunological failure or to patients with limited access to HAART. Third, the number of NTS isolates that are resistant to fluoroquinolones remains small. More studies are needed to assess the impact of fluoroquinolone resistance on the selection of antimicrobial prophylaxis. Fourth, cotrimoxazole, with variable in vitro antimicrobial activities against NTS isolates, was prescribed for pneumocystosis prophylaxis in most (77.9%) of our patients who were enrolled in the HAART era when they discontinued ciprofloxacin prophylaxis. We were not able to completely exclude the possibility that cotrimaxazole, when administered at a prophylactic dose, may confer protection against recurrent NTS bacteremia. However, the effect of prevention, as shown in a previous study, may be negligible [18]. In our study, the MIC90 of cotrimoxazole was high (>128 µg/mL), and 25% of the patients who received cotrimoxazole prophylaxis in the pre-HAART era developed recurrences. Finally, S. Choleraesuis, for which higher prevalences of resistance to fluoroquinolones and to third-generation cephalosporins have been reported in Taiwan than in other industrialized countries [25, 32], accounted for 28.0% of the NTS isolates in this study. Therefore, our findings may not be generalizable to other countries where S. Choleraesuis is not the predominant NTS serotype, such as the United States and several European countries [24, 26,27–28, 35, 36]. However, concerns have been raised regarding the increasing prevalence of other NTS serotypes isolated from humans and from imported meat that are resistant to nalixidic acid and that exhibit reduced susceptibility to ciprofloxacin (MIC90, 0.125–2 mg/L) in several industrialized countries [27, 28]. Surveillance studies are needed to assess the trends of antibiotic resistance of NTS isolates in HIV-infected patients.

In conclusion, our findings suggest that the risk of recurrent NTS bacteremia decreased significantly in the HAART era, although the prevalence of fluoroquinolone resistance was increasing in Taiwan. If our findings are confirmed by other investigators, a shorter course of secondary ciprofloxacin prophylaxis can be recommended to prevent recurrences of NTS bacteremia in HIV-infected patients who continue to receive HAART with favorable responses.

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Acknowledgments

We thank Dr. Victor L. Yu (University of Pittsburgh, Pittsburgh, PA), for review of the manuscript.

Potential conflicts of interest. All authors: no conflicts.

  • Received January 28, 2007.
  • Accepted May 1, 2007.
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  1. Clin Infect Dis. (2007) 45 (5): e60-e67. doi: 10.1086/520681
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