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Ann Thorac Surg 2005;80:530-536
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Antimicrobial Drug Resistance in Salmonella-Infected Aortic Aneurysms

Ron-Bin Hsu, MD a , * , Fang-Yue Lin, MD a , Robert J. Chen, MD, MPH a , Po-Ren Hsueh, MD b , Shoei-Shen Wang, MD a

a Department of Surgery, National Taiwan University Hospital, National Taiwan University College of Medicine, Taipei, Taiwan, Republic of China
b Department of Internal Medicine, National Taiwan University Hospital, National Taiwan University College of Medicine, Taipei, Taiwan, Republic of China

Accepted for publication February 15, 2005.

* Address reprint requests to Dr Hsu, National Taiwan University Hospital, No. 7, Chung-Shan S. Rd. Taipei, Taiwan 100, R.O.C. (Email: ronbin{at}ha.mc.ntu.edu.tw).


   Abstract
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Introduction
 Patients and Methods
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 Comment
 The Society of Thoracic...
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BACKGROUND: Salmonella infection of the aorta and adjacent arteries is rare, but life-threatening. There is an increasing number of infections caused by antimicrobial drug resistant Salmonella. This study sought to assess the association between antimicrobial drug resistance and clinical outcomes of patients with Salmonella-infected aortic aneurysm.

METHODS: Data were collected by retrospective chart review. Between October 1995 and October 2004, 34 patients with Salmonella-infected aortic aneurysm were included. Aneurysm-related deaths were defined as hospital deaths and late deaths due to prosthetic graft infection. Analysis was performed using the {chi}2 test, Fisher’s exact test, and Mann-Whitney test.

RESULTS: Nineteen patients had a suprarenal and 15 patients had an infrarenal aortic infection. The most common responsible pathogen was group C Salmonella (47%). Ciprofloxacin-resistant Salmonella infection occurred since March 2001 and the rate increased from 0 per 15 in the years before March 2001 to 5 per 19 in the years after March 2001 (p = 0.005 by Fisher’s exact test). Among the 26 patients who had combined medical and surgical therapy, 4 died in the hospital and 4 died of late prosthetic graft infection 3 to 6 months after operation, whereas 4 of the 8 who had medical therapy alone died of aneurysm rupture during hospitalization. The actuarial survival rates by the Kaplan-Meier method were 64% at 6 months, 61% at 1 year, and 56% at 5 years. The risk factors for aneurysm-related death were old age (78.5 ± 9.7 years vs 63.5 ± 11.4 years; p < 0.001) and ciprofloxacin-resistant Salmonella infection (4 of 5 vs 8 of 29; p = 0.042).

CONCLUSIONS: There was an increased mortality associated with ciprofloxacin resistance in infected aortic aneurysms with Salmonella. With an increasing incidence of ciprofloxacin resistant Salmonella, third generation cephalosporin is the antibiotic of choice for Salmonella-infected aneurysm.


   Introduction
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Salmonella infection of the aorta and adjacent arteries is rare, but life threatening [1, 2]. The mortality rate is extremely high without surgical treatment. Previous studies, including case reports and comprehensive literature review [1, 2], reported mortality rates of 25%–50% even when early surgery was performed. It has been suggested that surgery should be done once the diagnosis is made [3]. Of particular concern is the increasing number of infections caused by antimicrobial drug resistant Salmonella. Whether antimicrobial drug resistance contributes to enhanced illness or death in patients with infected aortic aneurysm is unclear. Previous studies [4–7] have shown that infected aortic aneurysm with Salmonella is common in Taiwan. This study sought to assess the association of antimicrobial drug resistance and the clinical outcomes of infected aortic aneurysms caused by Salmonella.


   Patients and Methods
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Setting
The National Taiwan University Hospital (Taipei, Taiwan) is a 2,000-bed tertiary care hospital. It serves an urban population of two million people as both a first-line and tertiary facility. It serves also as a referral center for other hospitals in a country with a population of 22 million people.

Patients
Information was collected retrospectively on all patients with nontyphoid Salmonella bacteremia and infected aortic aneurysms that occurred between October 1995 and October 2004. Data on age, sex, medical comorbidities, operation, location of aortic infection, clinical outcome, and antimicrobial drug resistance were recorded.

Management
The diagnosis and management of Salmonella infection of the aorta were described previously [7]. Clinically, infected aortic aneurysm was usually preceded by infected aorta. Infected aorta was diagnosed with clinical evidence of infection (fever and leukocytosis) and periaortic soft tissue infiltration demonstrated by an imaging study with either computed tomography or magnetic resonance imaging. Imaging studies were considered in those patients with age greater than 50 years and localized pain. Once the diagnosis of aortic infection was made, a third generation cephalosporin, ceftriaxone, was commenced. In patients who had a good response to antibiotic treatment (no fever, declining white cell count, and C-reactive protein), surgical intervention was considered 4 to 6 weeks later. Early surgical intervention was performed only for uncontrolled infection (persistent fever or septic shock) or the presence of aortic rupture (shock or large saccular aneurysm formation on imaging studies). The surgical techniques included wide debridement of necrotic tissue and aortic wall, copious saline irrigation, and in situ repair with a Dacron graft. For patients with proximal descending thoracic aneurysm immediately distal to left subclavian artery, cardiopulmonary bypass was instituted through the femoral artery and femoral vein. Proximal aortic anastomosis was performed under deep hypothermic circulatory arrest. Once proximal anastomosis was completed, cardiopulmonary bypass was reinstituted with cannulation of the prosthetic graft and simultaneous perfusion of both graft cannula (upper body) and femoral artery (lower body). Distal aortic anastomosis was done without speed. For patients with distal thoracic and abdominal aneurysm, aortic anastomosis was performed with a simple clamp-and-sew method. For patients with suprarenal abdominal aneurysm involving visceral arteries, the visceral arteries were reimplanted directly to the graft as an island pedicle. The infected aorta was irrigated with copious saline. The infected aneurysm wall was partially removed. No bacteriologic analysis was utilized to determine an acceptable resection margin. Extraanatomic reconstruction was not employed. Antibiotics were administered intravenously in-hospital and continued for at least 6 weeks after the operation, or until the clinical and laboratory parameters returned to normal.

Bacteriology and Susceptibility Testing
Blood or tissue cultures were repeated to identify the causative microorganism and isolates of Salmonella were initially identified by biochemical tests. Serogrouping was determined by agglutination testing with the use of antisera specific to the O antigen. Serotypes were not determined routinely. Antimicrobial drug susceptibility testing of the bacterial isolates was performed by the disk diffusion method as described by the National Committee for Clinical Laboratory Standards [8]. For this report, we presented susceptibility data for ampicillin, chloramphenicol, ciprofloxacin, sulfamethoxazole-trimethoprim, and cefotaxime (one of third generation cephalosporin).

Statistical Analysis
Aneurysm-related deaths were defined as hospital deaths and late deaths due to prosthetic graft infection. Analysis was performed using the {chi}2 test, Fisher’s exact test, and Mann-Whitney test. Data were compared between two time periods; before March 2001 and after March 2001. Risk factors included age, sex, operation, hypertension, diabetes mellitus, serum creatinine, corticosteroid use, location of aortic infection (suprarenal or infrarenal), and antimicrobial drug resistance.


   Results
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Patients
Between 1995 and 2004, there were 269 adult patients admitted because of nontyphoid Salmonella bacteremia and 34 patients developed aortic infection. Patient characteristics were listed in Table 1. Nineteen patients had a suprarenal aortic infection (2 ascending aorta, 1 aortic arch, 4 proximal descending thoracic aorta, 4 distal descending thoracic aorta, and 8 suprarenal abdominal aorta) and 15 patients had an infrarenal infection (14 infrarenal abdominal aorta and 1 iliac artery). There were 28 men and 6 women with a median age of 70.5 years (range, 35 to 88). The medical comorbidities included the following: hypertension 15, diabetes mellitus 10, coronary artery disease 4, chronic lung disease 3, old stroke 4, hemodialysis for renal failure 2, idiopathic thrombocytopenic purpura 2, and pure red cell aplasia, liver cirrhosis with hepatocellular carcinoma, chronic alcoholism, hydrocephalus, and bladder carcinoma each in one patient. In 30 of 34 patients, the diagnosis of infected aneurysm was made on admission because of initial presentation of fever and localized pain. Four patients were diagnosed to have infected aneurysm 14 days to 4 months after a positive blood culture.


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  		Table 1. Patient Characteristics
 
Bacteriology and Susceptibility Testing
All patients had a positive blood or tissue culture of Salmonella. Results of the Salmonella serogroups and antimicrobial drug susceptibility testing are shown in Table 2. The most common responsible pathogen was group C Salmonella in 16 patients (47%) followed by group D Salmonella in 11 patients (32%), and group B Salmonella in 7 patients (21%). Serotype determination was performed in 5 patients (Table 2).


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  		Table 2. Salmonella Serogroups and Antimicrobial Drug Resistance
 
For all 34 Salmonella isolated, 22 (65%) were ampicillin resistant, 21 (62%) were chloramphenicol resistant, 5 (15%) were ciprofloxacin resistant, 14 (41%) were sulfamethoxazole-trimethoprim resistant, and none was cefotaxime resistant (Table 2). Ciprofloxacin-resistant Salmonella infection was found since March, 2001 and the rate of ciprofloxacin resistance increased from 0/15 in the years before March 2001 to 5/19 in the years after March 2001 (p = 0.005 by Fisher’s exact test). The rate of antimicrobial drug resistance in the years before March 2001 and in the years after March 2001 did not change with ampicillin (73% vs 58%), chloramphenicol (73% vs 53%), sulfamethoxazole-trimethoprim (40% vs 47%), and cefotaxime (0% vs 0%).

Clinical Outcome
Of all 34 patients, 8 declined operation because of advanced age or severe medical comorbidities. Four patients died of aortic rupture 11 to 17 days after the diagnosis. A 76-year-old man with diabetes mellitus, coronary artery disease, and chronic renal insufficiency had suprarenal aortic infection. He did not have surgery because of effective antibiotic treatment (no fever, declining white cell count, and C-reactive protein) and a small saccular aneurysm 3 cm in size on imaging studies. He had oral ciprofloxacin for 6 months and has been well until the present. Follow-up imaging study one year after discharge showed a small saccular aneurysm with no interval change. Another 35-year-old woman had a 5-cm saccular aneurysm over suprarenal abdominal aorta. Operation was declined because of bleeding tendency due to Evan’s syndrome (idiopathic thrombocytopenia and hemolytic anemia). She was still well at present. Follow-up imaging study 7 years after discharge showed a heavily calcified fusiform aneurysm with no interval change.

Twenty-six patients were treated with a combination of medical therapy and surgery. Four patients died in the hospital. An 85-year-old man died of uncontrolled bleeding during operation and 3 patients died of overwhelming sepsis 17 days, 44 days, and 67 days after operation. Twenty-two operated patients were discharged and 4 patients died of late prosthetic graft infection 3 months, 3 months, 4 months, and 6 months after operation. An 81-year-old female patient died of organ failure 11 months after operation. A 72-year-old male patient died of hepatocellular carcinoma 14 months after operation.

Risk Factor Analysis
Collectively, the 8 hospital deaths (4 in operated and 4 in nonoperated patients) and 4 late prosthetic graft infections were considered as aneurysm-related deaths. Although statistically insignificant, the mortality rate of infected aortic aneurysm slightly increased from 20% (3 of 15) in the years before March 2001 to 47% (9 of 19) in the years after March 2001. The risk factors for aneurysm-related deaths were old age and ciprofloxacin-resistant Salmonella infection (Table 3). The actuarial survival rates by the Kaplan-Meier method were 64% at 6 months, 61% at 1 year, and 56% at 5 years.


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  		Table 3. Risk Factors for Aneurysm-Related Death by the Fisher’s Exact Test and the Mann-Whitney U Test
 

   Comment
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Nontyphoid Salmonella
Although Salmonella typhi and Salmonella paratyphi infect only humans, nontyphoid Salmonella are widespread, particularly in chickens and pigs. In humans, nontyphoid Salmonella infection is usually associated with contaminated foods [9]. Salmonella infection may manifest in five different clinical forms, including an asymptomatic chronic carrier state, gastroenteritis, enteric fever, bacteremia, and extraintestinal complications, of which infected aortic aneurysm is the most serious [10]. The major risk factors for nontyphoid salmonellosis and bacteremia were certain immunocompromised conditions including extreme age, alteration of the endogenous bowel flora of the intestine, diabetes, malignancy, autoimmune disorders, reticuloendothelial blockade, acquired human immunodeficiency virus infection, and therapeutic immunodeficiency [9]. The occurrence of primary bacteremia is ominous and should prompt clinicians to consider whether an immunodeficiency is present. Salmonella species are associated with about 35% of all infected aortic aneurysms [11]. However, the published literature contains only sporadic case reports of Salmonella-infected aortic aneurysms [1–5], usually with few patients. Clinical results have been poor because of the limited clinical experience in any one center. In Taiwan, where Salmonella infection is particularly prevalent, infected aortic aneurysm with Salmonella is more common than in other areas of the world [7, 12]. Because of this high incidence, it is reasonable to consider screening all adult patients with nontyphoid Salmonella bacteremia, especially the elderly and the immunocompromised, for infected aneurysm.

Many case reports and small case series [1–3] have emphasized the importance of surgical resection of infected aortic aneurysms with Salmonella. Survival appears to be improved among patients who receive combined medical and surgical therapy. Soravia-Dunand and colleagues [1] reviewed 140 cases and reported that early surgical intervention increased survival. The mortality rate was 40% in patients who had combined medical and surgical treatment and 96% in patients who had antibiotics alone. In our previous study [7], we reported an improved survival rate both in patients with medical treatment alone and in patients with combined medical and surgical treatment. A high index of suspicion and early diagnosis, avoidance of unnecessary immediate surgical resection, and more effective antibiotic therapy are most important. In this study, we further confirmed that the prognosis was not dismissal in medically treated patients and only 4 of 8 patients died of infection. The mortality rate in patients with combined medical and surgical treatment was 31%. Late prosthetic graft infection could occur as late as 6 months after operation.

Antimicrobial Resistance
Antimicrobial resistant nontyphoid Salmonella is increasingly common and appears with variable geographical incidence. In Taiwan, more than 40% of clinical isolates of nontyphoid Salmonella species were resistant to multiple antimicrobials [13]. It prompted us to investigate the association between antimicrobial drug resistance and clinical outcomes of patients with infected aortic aneurysm caused by Salmonella. The result of in vitro antimicrobial drug resistance in this study was that 65% of isolates were ampicillin resistant, 62% of isolates were chloramphenicol resistant, 15% of isolates were ciprofloxacin resistant, 44% of isolates were sulfamethoxazole-trimethoprim resistant, and no isolates were cefotaxime resistant. Third generation cephalosporin was the antibiotic of choice for Salmonella-infected aneurysm. Ciprofloxacin resistance has been observed in Salmonella enterica serotype choleraesuis since 2000, and in 2001 60% of Salmonella enterica serotype choleraesuis isolates were resistant to ciprofloxacin [14]. Antimicrobial drug resistant nontyphoid Salmonella have become an issue of worldwide concern [15, 16]. Between January 2000 and December 2003, 130 adult patients were admitted to our hospital with nontyphoid Salmonella bacteremia. The most common responsible pathogens were group D Salmonella (45%) and group C Salmonella (28%). The incidence of ciprofloxacin resistance significantly increased from 5/66 (8%) in the years 2000–2001 to 20/88 (23%) in the years 2002–2003 (p = 0.014 by Fisher’s exact test). Because of increasing rates of antimicrobial drug resistance in Salmonella worldwide, extended-spectrum cephalosporins, especially ceftriaxone, are frequently used to treat invasive salmonellosis. Thus, third generation cephalosporins are now the only reliable antibiotics to treat infected aortic aneurysms. Unfortunately, since the early 1990s, ceftriaxone-resistant Salmonella have been noted in many countries in addition to Taiwan [17, 18]. It could become an emerging threat. Antimicrobial drug resistant Salmonella can spread from animal to humans. Although all of Salmonella isolates in this study were sensitive to third generation cephalosporin, continued surveillance is needed to prevent the further spread of antimicrobial-resistant Salmonella [14, 19, 20].

Risk Factors for Death
Because of the small case numbers in previous studies, risk factors for death in patients with Salmonella-infected aortic aneurysm are still unknown. In this study, we first demonstrated that risk factors for aneurysm-related death were old age and ciprofloxacin-resistant Salmonella infection. Antimicrobial drug resistance has two principal effects on the outcome of infections [21]. First, antimicrobial resistance may be associated with a change in the virulence of the strain. A second effect of antimicrobial resistance is the possible complication of the choice of treatment agents. There can be a poor response to treatment because of the empiric choice of an antimicrobial to which the organism is resistant. In this study, we used ceftriaxone in all infected patients. Thus, the increased mortality of ciprofloxacin-resistant Salmonella infection should result from an increased virulence of Salmonella. Several studies have addressed the relation between antimicrobial resistance and the virulence of nontyphoid Salmonella. In a report from the Centers for Disease Control and Prevention for nontyphoid salmonellosis, subjects with infection caused by antimicrobial-resistant organisms were significantly more likely to be hospitalized and be ill longer than those with antimicrobial susceptible infections [22]. In a matched control study, Helms and colleagues [23] reported an increased mortality associated with antimicrobial drug-resistant Salmonella enterica serotype Typhimurium. In their study, patients infected with strains resistant to ampicillin, chloramphenicol, streptomycin, sulfonamide, and tetracycline were 4.8 times more likely to die, whereas quinolone resistance was associated with a mortality rate 10.3 times higher than the general population. But the control group used in their study was a healthy population, rather than patients infected with antimicrobial susceptible Salmonella. Recently Martin and colleagues [24] reported an increased rate of hospitalization in patients with antimicrobial-resistant Salmonella enterica serotype Typhimurium infections, but the impact of antimicrobial resistance on the clinical outcomes (death) was not mentioned. Whether antimicrobial resistance increases the mortality of Salmonella-infected patients is not assessed in previous studies. Here, we demonstrated an increased mortality in patients with infected aortic aneurysm caused by ciprofloxacin-resistant Salmonella.

Study Limitation
The major limitations of this study are the lack of the Salmonella serotype determination and relatively small case number. No multivariate logistic regression analysis was performed because of our small case number. However, this study is one of the largest series of Salmonella-infected aortic aneurysms ever reported in the literature. This study also demonstrates the association between antimicrobial drug resistance and prognosis of infected aortic aneurysm.

Conclusions
There was an increased mortality associated with ciprofloxacin resistance in infected aortic aneurysms with Salmonella. With an increasing incidence of ciprofloxacin-resistant Salmonella, third generation cephalosporin is the antibiotic of choice for Salmonella-infected aneurysms. Close clinical follow-up is mandatory in every case of infected aortic aneurysm caused by ciprofloxacin-resistant Salmonella.


   The Society of Thoracic Surgeons: Forty-Second Annual Meeting
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Please mark your calendars for the Forty-Second Annual Meeting of The Society of Thoracic Surgeons, to be held in New Orleans, Louisiana, from January 30-February 1, 2006. The program will provide in-depth coverage of thoracic surgical topics selected to enhance and broaden the knowledge of cardiothoracic surgeons. Attendees will benefit from traditional Abstract Presentations, as well as Surgical Forums, Breakfast Sessions, Surgical Motion Pictures, and Town Hall Meetings on specific topics.

Advance registration forms, hotel reservation forms, and details regarding transportation arrangements, as well as the complete meeting program, will be mailed to Society members this fall. Also, complete meeting information will be available on the Society’s Web site at www.sts.org. Nonmembers who wish to receive information on the Annual Meeting may contact the Society’s secretary, Douglas E. Wood.

Abstracts for the meeting must be submitted elec-tronically. The electronic submission form may be accessed at www.sts.org. There is no charge for sub-mitting abstracts. The submission deadline is August 8, 2005 at 5:00 PM CDT. Please direct any questions regarding your submission to the Society’s headquar-ters.

Douglas E. Wood, MD

Secretary

The Society of Thoracic Surgeons

633 N. Saint Clair St, Suite 2320

Chicago, IL 60611-3658

Telephone: (312) 202-5800

Fax: (312) 202-5801

e-mail: mailto:sts{at}sts.org

website: www.sts.org


   References
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  1. Soravia-Dunand VA, Loo VG, Salit IE. Aortitis due to Salmonellareport of 10 cases and comprehensive review of the literature. Clin Infect Dis 1999;29:862-868.[Medline]
  2. Veraldi GF, de Manzoni G, Laterza E, et al. Extraintestinal infection by group C Salmonellaa case report and review of the literature. Hepatogastroenterology 2001;48:471-474.[Medline]
  3. Oskoui R, Davis WA, Gomes MN. Salmonella aortitis. A report of a successfully treated case with a comprehensive review of the literature Arch Intern Med 1993;153:517-525.[Abstract]
  4. Wang JH, Liu YC, Yen MY, et al. Mycotic aneurysm due to non-typhi salmonellareport of 16 cases. Clin Infect Dis 1996;23:743-747.[Medline]
  5. Chan P, Tsai CW, Huang JJ, Chuang YC, Hung JS. Salmonellosis and mycotic aneurysm of the aorta. A report of 10 cases J Infect 1995;30:129-133.[Medline]
  6. Hsu RB, Tsay YG, Wang SS, Chu SH. Surgical treatment for primary infected aneurysm of descending thoracic aorta, abdominal aorta and iliac arteries J Vasc Surg 2002;36:746-750.[Medline]
  7. Hsu RB, Chen RJ, Wang SS, Chu SH. Infected aortic aneurysmsclinical outcome and risk factor analysis. J Vasc Surg 2004;40:30-35.[Medline]
  8. National Committee for Clinical Laboratory Standards (NCCLS) Performance standard M2-A6. Wayne, PA: NCCLS; 1998.
  9. Hohmann EL. Nontyphoidal salmonellosis Clin Infect Dis 2001;32:263-269.[Medline]
  10. Cohen JI, Bartlett JA, Corey GR. Extra-intestinal manifestations of Salmonella infections Medicine 1987;66:349-388.[Medline]
  11. Moneta GL, Taylor Jr LM, Yeager RA, et al. Surgical treatment of infected aortic aneurysm Am J Surg 1998;175:396-399.[Medline]
  12. Hsu RB, Tsay YG, Chen RJ, Chu SH. Risk factors for primary bacteremia and endovascular infection in patients without acquired immunodeficiency syndrome who have nontyphoid salmonellosis Clin Infect Dis 2003;36:829-834.[Medline]
  13. Hsueh PR, Liu CY, Luh KT. Current status of antimicrobial resistance in Taiwan Emerg Infect Dis 2002;8:132-137.[Medline]
  14. Chiu CH, Wu TL, Su LH, et al. The emergence in Taiwan of fluoroquinolone resistance in Salmonella enterica serotype choleraesuis N Eng J Med 2002;346:413-419.[Abstract/Free Full Text]
  15. Parry CM. Antimicrobial drug resistance in Salmonella enterica Curr Opin Infect Dis 2003;16:467-472.[Medline]
  16. Threlfall EJ. Antimicrobial drug resistance in Salmonellaproblems and perspectives in food- and water-borne infections. FEMS Microbiol Rev 2002;26:141-148.[Medline]
  17. Yan JJ, Ko WC, Chiu CH, Tsai SH, Wu HM, Wu JJ. Emergence of ceftriaxone-resistant Salmonella isolates and rapid spread of plasmid-encoded CMY-2-like cephalosporinase, Taiwan Emerg Infect Dis 2003;9:323-328.[Medline]
  18. Gupta A, Fontana J, Crowe C, et al. Emergence of multidrug-resistant Salmonella enterica serotype Newport infections resistant to expanded-spectrum cephalosporins in the United States J Infect Dis 2003;188:1707-1716.[Medline]
  19. Anderson AD, Nelson JM, Rossiter S, Angulo FJ. Public health consequences of use of antimicrobial agents in food animals in the United States Microb Drug Resist 2003;9:373-379.[Medline]
  20. Glynn MK, Bopp C, Dewitt W, Dabney P, Mokhtar M, Angulo FJ. Emergence of multidrug-resistant Salmonella enterica serotype typhimurium DT104 infections in the United States N Engl J Med 1998;338:1333-1338.[Abstract/Free Full Text]
  21. Travers K, Barza M. Morbidity of infections caused by antimicrobial-resistant bacteria Clin Infect Dis 2002;34:S131-S134.
  22. Lee LA, Puhr ND, Maloney EK, Bean NH, Tauxe RV. Increase in antimicrobial-resistant Salmonella infections in the United States, 1989–1990 J Infect Dis 1994;170:128-134.[Medline]
  23. Helms M, Vastrup P, Gerner-Smidt P, Molbak K. Excess mortality associated with antimicrobial drug-resistant Salmonella typhimurium Emerg Infect Dis 2002;8:490-495.[Medline]
  24. Martin LJ, Fyfe M, Dore K, et al. Increased burden of illness associated with antimicrobial-resistant Salmonella enterica serotype typhimurium infections J Infect Dis 2004;189:377-384.[Medline]




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