Travel-associated Antimicrobial Drug–Resistant Nontyphoidal Salmonellae, 2004–2009

Russell S. Barlow, Emilio E. DeBess

, Kevin L. Winthrop, Jodi A. Lapidus, Robert Vega, and Paul R. Cieslak

Author affiliations: Oregon Health Authority, Portland, Oregon USA (R.S. Barlow, E.E. DeBess, P.R. Cieslak); Oregon Health and Science University, Portland (R.S. Barlow, K.L. Winthrop, J.A. Lapidus); Oregon State Public Health Lab, Hillsboro, Oregon, USA (R. Vega)

Abstract

To evaluate trends in and risk factors for acquisition of antimicrobial-drug resistant nontyphoidal Salmonella infections, we searched Oregon surveillance data for 2004–2009 for all culture-confirmed cases of salmonellosis. We defined clinically important resistance (CIR) as decreased susceptibility to ampicillin, ceftriaxone, ciprofloxacin, gentamicin, or trimethoprim/sulfamethoxazole. Of 2,153 cases, 2,127 (99%) nontyphoidal Salmonellaisolates were obtained from a specific source (e.g., feces, urine, blood, or other normally sterile tissue) and had been tested for drug susceptibility. Among these, 347 (16%) isolates had CIR. The odds of acquiring CIR infection significantly increased each year. Hospitalization was more likely for patients with than without CIR infections. Among patients with isolates that had been tested, we analyzed data from 1,813 (84%) who were interviewed. Travel to eastern or Southeast Asia was associated with increased CIR. Isolates associated with outbreaks were less likely to have CIR. Future surveillance activities should evaluate resistance with respect to international travel.

Each year, nontyphoidal salmonellae (NTS) are responsible for >1 million infections in the United States and an estimated 98 million cases globally (1–4). Each year in the United States, infections result in an estimated 168,000 physician visits, 19,000 hospitalizations, and 380 deaths at a cost of $US 2.3 billion (1–3,5). Data suggest that 85.6% of NTS infections are foodborne and that the remaining infections occur by the fecal–oral route in human-to-human transmission and zoonotic transmission (2). For healthy persons, infections commonly result in self-limiting acute gastroenteritis that resolves without antimicrobial drug therapy. However, antimicrobial drugs can be life saving for immunologically vulnerable populations, such as infants, elderly persons, immunocompromised persons, and persons with invasive infection (6–8). The drugs most commonly prescribed in developing countries are ampicillin and chloramphenicol; those most commonly prescribed in the United States are trimethoprim/sulfamethoxazole, fluoroquinolones, and cephalosporins (9).

In the 1980s, studies demonstrated alarming increases in the prevalence of antimicrobial drug resistance among NTS infections (10,11). This increase was associated with indiscriminate use of antimicrobial drugs in animal husbandry and in humans (10–12). A retrospective study conducted during 1996–2001 associated antimicrobial drug resistance with increased disease severity, highlighting the risk to public health (13).

During the past decade, few population-level analyses have identified risk factors for acquiring a resistant NTS infection outside of outbreak clusters and retail meat supplies. A recently identified risk factor is international travel (14,15). Bacteriologic studies from Europe identified differences in resistance among Salmonella enterica serotypes Stanley, Concord, and Typhimurium isolated from patients with a history of international travel (16–20). However, these studies did not estimate the magnitude of or risk for antimicrobial drug–resistant NTS acquisition among international travelers. We hypothesized that international travel is a risk factor for acquisition of a resistant NTS infection. To test our hypothesis, we analyzed surveillance data from Oregon for 2004–2009 and quantified trends in antimicrobial drug resistance, investigated the relationship between resistance and case outcomes, and assessed whether international travel was associated with acquisition of NTS infections with clinically important resistance (CIR).