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Laboratory-Based Surveillance of Paratyphoid Fever in the United States: Travel and Antimicrobial Resistance

  1. Sundeep K. Gupta,
  2. Felicita Medalla,
  3. Michael W. Omondi,
  4. Jean M. Whichard,
  5. Patricia I. Fields,
  6. Peter Gerner-Smidt,
  7. Nehal J. Patel,
  8. Kara L. F. Cooper,
  9. Tom M. Chiller, and
  10. Eric D. Mintz
  1. Division of Foodborne, Bacterial, and Mycotic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia
  1. Reprints or correspondence: Dr. Sundeep K. Gupta, 2190 Kampala Place, Dulles, VA 20189 (scg7{at}ug.cdc.gov).
 
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Abstract

Background. The incidence of paratyphoid fever, including paratyphoid fever caused by antimicrobial-resistant strains, is increasing globally. However, the epidemiologic and laboratory characteristics of paratyphoid fever in the United States have never been studied.

Methods. We attempted to interview all patients who had been infected with laboratory-confirmed Salmonella serotypes Paratyphi A, Paratyphi B, or Paratyphi C in the United States with specimens collected from 1 April 2005 through 31 March 2006. At the Centers for Disease Control and Prevention (CDC), isolates underwent serotype confirmation, antimicrobial susceptibility testing, and pulsed-field gel electrophoresis typing.

Results. Of 149 patients infected with Salmonella Paratyphi A, we obtained epidemiologic information for 89 (60%); 55 (62%) of 86 were hospitalized. Eighty-five patients (96%) reported having travel internationally, and 80 (90%) had traveled to South Asia. Of the 146 isolates received at the CDC, 127 (87%) were nalidixic acid resistant; nalidixic acid resistance was associated with travel to South Asia (odds ratio, 17.0; 95% confidence interval, 3.8–75.9). All nalidixic acid–resistant isolates showed decreased susceptibility to ciprofloxacin (minimum inhibitory concentration, ⩾0.12 µg/mL). Of 49 patients infected with Salmonella Paratyphi B, only 12 (24%) were confirmed to have Paratyphi B when tested at the CDC. Four (67%) of 6 patients were hospitalized, and 5 (83%) reported travel (4 to the Andean region of South America). One case of Salmonella Paratyphi C infection was reported in a traveler to West Africa with a urinary tract infection.

Conclusions. Physicians should be aware of the increasing incidence of infection due to Salmonella Paratyphi A and treatment options given its widespread antimicrobial resistance. A paratyphoid fever vaccine is urgently needed. Continued surveillance for paratyphoid fever will help guide future prevention and treatment recommendations.

Paratyphoid fever is caused by Salmonella enterica serotypes Paratyphi A, Paratyphi B, or Paratyphi C. Like the other type of enteric fever, typhoid fever, paratyphoid fever is rare in the United States. However, an estimated 5,400,000 cases of paratyphoid fever occurred globally in 2000 [1]. In industrialized countries, paratyphoid fever is known to occur most often among international travelers [2], whereas in the United States, the epidemiology of paratyphoid fever has never been described.

Paratyphoid fever was previously considered to occur less frequently and be a more benign disease than typhoid fever. However, during the past 4 decades, both the incidence of Salmonella Paratyphi A infection and its relative frequency among enteric fever cases have increased in the United States (figure 1) and in China [3], India [4], Nepal [5], Pakistan [6], and Thailand [7]. In some parts of China [3], the incidence of paratyphoid fever has surpassed that of typhoid fever.

Figure 1
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Figure 1

Incidence of infection due to Salmonella serotypes Typhi and Paratyphi A, 1968–2005, National Salmonella Surveillance System

Recent studies have established that illnesses caused by Salmonella Paratyphi A and Salmonella Typhi are clinically indistinguishable [5, 8]. Salmonella Paratyphi A infection causes systemic complications in 10%–15% of cases, such as meningitis [9], endocarditis [10], hepatic abscess [11], osteomyelitis and psoas abscess [12], gallbladder cancer [13], and pancytopenia [14]. Three percent of invasive Salmonella infections in the United States are caused by Salmonella Paratyphi A [15].

Mortality among patients with enteric fever has been as high as 40% [16]. The use of antimicrobials, beginning in 1948 with the introduction of chloramphenicol, has substantially reduced mortality to <1% [5, 17]. However, the emergence of antimicrobial resistance is concerning and threatens to increase treatment failure, relapse, and death due to enteric fever [18]. Salmonella Paratyphi A multidrug resistance [19], nalidixic acid resistance [20], and ceftriaxone resistance [5] have been recently reported in India and Nepal. Nalidixic acid resistance is a marker for decreased susceptibility to ciprofloxacin. Among Salmonella Paratyphi A isolates, nalidixic acid resistance is increasing and has become predominant in areas of endemicity [6]. Unlike typhoid fever, no vaccine is available that provides specific protection against paratyphoid fever.

Globally, Salmonella Paratyphi A is the most frequently described of the 3 serotypes. Little is known about serotypes Paratyphi B and Paratyphi C. Differentiation of serotype Paratyphi B from serotype Paratyphi B var. L(+) tartrate(+) (formerly serotype Java) requires special laboratory testing that is often not performed. This is important because serotype Paratyphi B var. L(+) tartrate(+) causes a typical Salmonella gastroenteritis instead of enteric fever [21].

Unlike typhoid fever, paratyphoid fever is not a nationally notifiable disease in the United States; instead, the 3 serotypes are included in national reporting of all non-Typhi Salmonella infection. Because paratyphoid fever cases comprise <1% of cases caused by all non-Typhi Salmonella serotypes [22], incidence data specific for paratyphoid fever are not generally published. Also, unlike for typhoid fever, clinical and travel information is not routinely collected. In the absence of paratyphoid fever surveillance, clinicians are unable to base treatment decisions on incidence and resistance patterns. To understand the epidemiologic and laboratory characteristics of paratyphoid fever in the United States, the Division of Foodborne, Bacterial, and Mycotic Diseases of the Centers for Disease Control and Prevention (CDC), in collaboration with state and local health departments, conducted laboratory-based paratyphoid fever surveillance during a 1-year period.

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Methods

All 50 US state health departments along with the Houston, Los Angeles, and New York City metropolitan health departments agreed to participate in the study. In California, however, interviews were only conducted in Los Angeles county and the 3 counties participating in the Foodborne Diseases Active Surveillance Network, San Francisco, Alameda, and Contra Costa counties, together representing 36% of the population of California. The District of Columbia and US territories were not included. State and local public health laboratories were asked to immediately report new cases of culture-confirmed paratyphoid fever to health department epidemiologists. A standard questionnaire was then administered by telephone or in person by state or local health department officials. For patients aged <18 years, a parent or guardian was interviewed. The questionnaire elicited demographic, epidemiologic, and clinical information, including country of birth, country of residence, travel history, onset date, symptoms, hospitalization, and antimicrobial treatment received. Completed questionnaires were reviewed and entered into a database at the CDC.

A case was defined as an acute illness compatible with paratyphoid fever with laboratory-confirmed Salmonella serotype Paratyphi A, Paratyphi B, or Paratyphi C isolated from a specimen collected from 1 April 2005 through 31 March 2006. Both US residents and nonresidents were defined by self-reported country of residence. A travel-associated case was defined as paratyphoid fever in a person who reported being outside the United States at any time during the 30 days before illness onset.

State and metropolitan public health laboratories sent all Salmonella Paratyphi A, Paratyphi B, and Paratyphi C isolates received from clinical laboratories to the National Antimicrobial Resistance Monitoring System laboratory at the CDC. Isolates that appeared to be from the same patient were identified using the first 3 letters of the patient's last name, county and state of residence, month and year of birth or age, and sex. If >1 isolate was received for the same patient, the following criteria were applied sequentially to decide which specimen to include: the pathogen was isolated from a blood specimen, an earlier specimen collection date, a lower state isolate number (suggestive of an earlier isolation date), and finally a lower CDC isolate number. Inability to ferment tartrate was confirmed at the CDC for isolates submitted as serotype Paratyphi B using Jordan's tartrate test [23]. For isolates that had a negative Jordan's tartrate result after 72 h of incubation at 37°C, other tests were performed to identify tartrate fermentation [24] by the National Salmonella Reference Laboratory. Isolates that were able to ferment tartrate as determined by 1 or more of these methods were excluded from the study.

Antimicrobial susceptibility testing was performed using the broth microdilution method according to Clinical and Laboratory Standards Institute standards, and where available, resistance was defined using Clinical and Laboratory Standards Institute breakpoints. The MIC values were determined for the following 14 antimicrobial agents: amikacin, ampicillin, amoxicillin-clavulanic acid, ceftriaxone, chloramphenicol, ciprofloxacin, trimethoprim-sulfamethoxazole, sulfisoxazole, cefoxitin, gentamicin, kanamycin, nalidixic acid, streptomycin, and tetracycline. Isolates resistant to ampicillin, chloramphenicol, sulfisoxazole, and trimethoprim-sulfamethoxazole were defined as multidrug resistant. Isolates that exhibited susceptible or intermediate MIC values with all 14 antimicrobial agents tested were classified as susceptible.

PFGE testing using the XbaI restriction enzyme was performed either by the submitting state public health laboratory or by the PulseNet Methods Development and Validation Laboratory at the CDC according to the PulseNet standardized protocol [25]. When epidemiologically unrelated isolates had indistinguishable XbaI patterns, PFGE testing using a second DNA restriction enzyme (BlnI) was performed.

Interview and laboratory data were linked at the CDC using the first 3 letters of the patient's last name, onset date, county and state of residence, month and year of birth, and sex. This study was determined by the CDC Institutional Review Board to be exempt from review. Informed consent was obtained from all respondents.

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Results

During the 1-year study period, 149 patients were confirmed to have Salmonella Paratyphi A infection, 12 had Salmonella Paratyphi B infection, and 1 had Salmonella Paratyphi C infection, compared with 378 patients infected with Salmonella Typhi in the same period (National Salmonella Surveillance System), indicating that 30% of enteric fever cases were paratyphoid fever.

Salmonella Paratyphi A

The 149 patients infected with Salmonella Paratyphi A were identified through 28 state and metropolitan health departments (table 1). Eighteen (12%) of the 149 patients were from nonparticipating counties in California. We obtained epidemiologic information for 89 patients (60%), antimicrobial susceptibility results for 146 patients (98%), and PFGE results for 137 patients (92%); all 3 types of data were available for 88 patients (59%).

Epidemiology results. The median age of 138 patients was 26 years (range, 1–67 years); 59 (49%) of 121 patients were male. Seventy-eight (91%) of 86 patients reported that they were US residents, 55 (71%) of whom were born outside the United States. Infection rates peaked during the late summer and late spring (figure 2). Eight (12%) of 66 patients had received antimicrobials in the 6 weeks before illness onset. This is the same as the proportion of the general population reporting receiving antimicrobials in the previous 30 days [26].

Figure 2
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Figure 2

Seasonality of Salmonella Paratyphi A infection, by month of specimen collection, United States, 1 April 2005–31 March 2006 (n=145)

Almost all patients reported experiencing a fever, and headache, anorexia, diarrhea, and abdominal pain were each reported by approximately one-half of patients (table 2). Fifty-five (64%) of 86 patients were hospitalized for a median of 5 days (range, 1–14 days); no fatalities were reported.

Table 1
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Table 1

Patients with Salmonella serotype Paratyphi A by state, United States, 1 April 2005–31 March 2006 (n=149).

Table 2
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Table 2

Frequency of symptoms among patients with Salmonella Paratyphi A infection, United States, 1 April 2005–31 March 2006.

Of 89 patients, 85 (96%) traveled outside the United States in the 30 days before illness onset. Of the 79 patients who traveled to a single nonindustrialized country, 74 reported travel to South Asia (India, 57; Bangladesh, 13; and Pakistan, 4) (table 3). The 4 patients who reported no travel were born outside of the United States (3 were born in India, and 1 was born in Bangladesh). Sixty-five patients (76%) traveled to visit friends or relatives, and another 6 (7%) traveled to visit or immigrate to the United States. Among US residents who traveled, 15 (27%) of 55 reported visiting a health care professional before their trip for pretravel health advice, and 7 (12%) of 59 reported receiving a typhoid fever vaccine before traveling.

Table 3
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Table 3

Countries visited by patients with Salmonella Paratyphi A infection in the 30 days before illness onset, United States, 1 April 2005–31 March 2006 (n=79).

The incidence of infection due to Salmonella Paratyphi A among US residents traveling to India was >8 times that for Indonesia and >29 times that for Brazil (table 3).

Laboratory testing. Of 146 isolates received at the CDC, 121 (83%) were from blood specimens, 18 (12%) were from stool specimens, and 1 was from a urine sample. Seventeen isolates (12%) were susceptible to all antimicrobial agents, 2 (1%) were multidrug resistant, and 127 (87%) were nalidixic acid resistant. The 2 multidrug-resistant isolates were also resistant to streptomycin and tetracycline. Of the nalidixic acid–resistant isolates, 1 isolate was also resistant to trimethoprim-sulfamethoxazole, sulfisoxazole, and tetracycline; 1 was also resistant to amoxicillin clavulanate, cefoxitin, and tetracycline; and 1 was also resistant to ciprofloxacin. All 127 nalidixic acid–resistant isolates and 1 nalidixic acid–susceptible isolate had a ciprofloxacin MIC of ⩾0.12 µg/mL, suggesting a decreased susceptibility to ciprofloxacin [18]. All isolates were susceptible to ceftriaxone (MIC, ⩽5 µg/mL) and all aminoglycosides tested.

Multidrug-resistant Salmonella Paratyphi A. The 2 patients infected with multidrug-resistant Salmonella Paratyphi A were both Pakistan-born US residents who traveled to Pakistan to visit friends or relatives. Neither patient reported taking antimicrobials in the 6 weeks before illness onset.

Nalidixic acid–resistant Salmonella Paratyphi A. Seventy-five patients (59%) infected with nalidixic acid–resistant Salmonella Paratyphi A had epidemiologic information available. Seventy-two patients (96%) reported foreign travel. Forty-eight (64%) were hospitalized for a median duration of 5 days. Of 13 patients with nalidixic acid–susceptible isolates and epidemiologic information available, 7 (53%) were hospitalized for a median duration of 6 days.

Among 79 travelers to only 1 nonindustrialized country, a nalidixic acid–resistant strain was isolated from 0 of 1 traveler to Brazil, 0 of 2 travelers to Cambodia, 0 of 4 travelers to Pakistan, 1 of 2 travelers to Indonesia, 56 of 57 travelers to India, and all 13 travelers to Bangladesh. Three of 4 persons who denied travel were also found to have nalidixic acid–resistant isolates; all 3 were born in India. Travel to South Asia, especially India, was significantly associated with nalidixic acid–resistant Salmonella Paratyphi A infection (table 4). Travel information was not available for the 1 patient infected with a ciprofloxacin-resistant strain.

Table 4
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Table 4

Nalidixic acid resistance and selected characteristics of patients infected with Salmonella Paratyphi A, United States, 1 April 2005–31 March 2006.

Molecular subtyping. PFGE XbaI pattern results were available for 137 patients. Twenty-seven isolates with non-unique XbaI patterns did not have BlnI results available, leaving 110 isolates that could be uniquely categorized. Among these, 31 molecular subtypes (unique combinations of XbaI and BlnI patterns) were identified. Six subtypes (19%) accounted for 90 (82%) of these isolates.

Salmonella Paratyphi B

Of 49 patients with reported cases of Salmonella Paratyphi B infection, 37 (76%) were found to have Salmonella Paratyphi B var. L(+) tartrate(+) at the CDC, leaving 12 patients with confirmed cases of Salmonella Paratyphi B infection from 8 states. Three cases were among siblings, and the 2 patients with later illness onset were excluded from analysis because their infections were likely secondary.

The median age of the 10 patients infected with Salmonella Paratyphi B was 20 years (range, 2–44 years); 4 (40%) were male (table 5). Five (50%) of the 10 isolates were from blood specimens. Of 6 patients interviewed, 5 (83%) reported experiencing fever, and all 6 had diarrhea. Four (67%) were hospitalized for a median of 5 days (range, 4–6 days); no fatalities occurred. Five patients (83%) reported having traveled internationally within 30 days of illness onset: 2 traveled to Bolivia, 1 to Peru, 1 to Bolivia and Peru, and 1 to Ethiopia. Nine isolates (90%) were susceptible to all antimicrobial agents, and 1 was resistant to nalidixic acid. Six distinct PFGE patterns using the XbaI enzyme were found; 1 pattern was seen in 4 isolates, 3 of which were linked to travel to South America.

Table 5
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Table 5

Epidemiologic and laboratory data for patients with primary Salmonella Paratyphi B (n=10).

Salmonella Paratyphi C

A 49-year-old man who had traveled to Mauritania and Senegal in the 30 days before illness onset represented the only case of illness due to Salmonella Paratyphi C. The patient reported symptoms of a urinary tract infection; he was not hospitalized. Salmonella Paratyphi C was isolated from a urine sample and was susceptible to all antimicrobial agents tested.

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Discussion

This is the first study, to our knowledge, of the epidemiology of paratyphoid fever in the United States. It confirms that paratyphoid fever is a severe illness that most often is caused by nalidixic acid–resistant Salmonella Paratyphi A. Paratyphoid fever, like typhoid fever, is usually acquired while traveling internationally. Infection with Salmonella Paratyphi A was associated with travel to South and Southeast Asia, and nalidixic acid–resistant infection was associated with travel to South Asia. Salmonella Paratyphi B infection appeared to be associated with travel to the Andean region of South America. One patient with Salmonella Paratyphi C infection traveled to Africa, consistent with reports of Salmonella Paratyphi C infection from different regions of Africa [27].

Most Salmonella Paratyphi A isolates in this study showed decreased susceptibility to ciprofloxacin. Decreased susceptibility to ciprofloxacin is common in isolates from South and Southeast Asia, and full ciprofloxacin resistance is also occasionally reported in isolates from patients with paratyphoid fever [28]. Decreased susceptibility to ciprofloxacin is associated with delayed defervescence, persistence of positive fecal culture results after antimicrobial therapy, clinical relapse, and the need for additional treatment [18].

Clinicians should be aware of nalidixic acid–resistant paratyphoid fever. Options for antimicrobial therapy include high-dose and prolonged treatment with fluoroquinolones, gatifloxacin or other higher-generation fluoroquinolones [29], ceftriaxone [30], or azithromycin [30] or the use of 2 agents in combination until antimicrobial susceptibility results are available; cefixime may be a less ideal choice [29]. Although multidrug resistance was infrequently seen in our study, it is commonly seen globally, and traditional antimicrobial agents, such as trimethoprim-sulfamethoxazole, are not recommended for treatment. Insufficient information is available regarding the effectiveness of extended-spectrum β-lactams, such as aztreonam and imipenem, in multidrug-resistant or nalidixic acid–resistant strains [30]. In developing countries, these options may be prohibitively expensive, and affordable and effective treatment options need to be developed.

Our study confirmed the substantial heterogeneity of Salmonella Paratyphi A molecular subtypes [31]. PFGE testing can be useful in identifying and investigating outbreaks of paratyphoid fever [31].

The reasons for the emergence of paratyphoid fever in Asia are unknown and cannot be readily explained by improved diagnostic methods, typhoid fever vaccination, or the effect of improved water and sanitation systems. The emergence of nalidixic acid–resistant Salmonella Paratyphi A is not surprising, given the easy availability of fluoroquinolones without a prescription in developing countries. Compared with South Asia, few cases of paratyphoid fever were seen from Indonesia and none from China, although both are populous Asian countries with endemic paratyphoid fever that are frequently traveled to by US residents. This finding is consistent with studies in other industrialized countries [8, 32] and may reflect a lower incidence of paratyphoid fever in the areas of these countries visited by US residents compared with countries in South Asia [33].

Infection due to Salmonella Paratyphi A occurred most frequently in early spring and late summer. A similar pattern has been seen among travelers from both Japan and Sweden to South Asia [34, 35]. Although this corresponds to the high travel seasons, this pattern may also reflect the seasonal pattern seen among endemic cases of typhoid and paratyphoid fever in this region [36].

In the absence of an effective vaccine against Salmonella Paratyphi A, prevention of paratyphoid fever is extremely challenging. Most patients with paratyphoid fever were immigrants to the United States who were visiting friends or relatives. Individuals who visit friends or relatives are known to have high travel-related morbidity for a variety of health conditions [37]. As seen in this study, lack of pretravel health care is common in individuals who are visiting friends or relatives. Exposure to infectious agents may also be increased because of poor adherence to safe food and water consumption, longer duration of travel, and travel to high-risk areas within countries. For the prevention of paratyphoid fever, outreach efforts and effective health messages to the South Asian community are essential.

An effective vaccine against Salmonella Paratyphi A is urgently needed. The Ty21a live oral typhoid vaccine has recently been shown to protect against Salmonella Paratyphi B but not serotype Paratyphi A [38]. An effective paratyphoid fever vaccine would not only reduce infection but could also potentially reduce the chance of outbreaks. However, a vaccine should not be considered a substitute for safe food and water consumption by travelers and efforts to improve water and sanitation systems in countries where enteric fevers are endemic.

A high percentage of isolates reported as Salmonella Paratyphi B were found to have the ability to ferment tartrate, illustrating the technical difficulty in distinguishing the 2 biovars. The recent identification of molecular markers associated with the inability to ferment [39] should improve the ability to differentiate the 2 biovars in the future.

This study was primarily limited by the inability to obtain epidemiologic information. Substantial parts of California did not participate in the epidemiologic part of the investigation, and ∼40% of patients infected with Salmonella Paratyphi A or Salmonella Paratyphi B could not be interviewed. However, it seems unlikely that these data would substantially change our conclusions.

As a result of this study, the CDC's national typhoid fever case report form has been modified for use with paratyphoid fever cases. Use of this new form, along with antimicrobial susceptibility testing of all Salmonella Paratyphi A and C isolates, will begin in 2008. Consideration should be given to including paratyphoid fever as a specific nationally notifiable disease. National laboratory-based epidemiologic surveillance for paratyphoid fever, such as is currently performed for typhoid fever, is essential to monitor trends in country-specific incidence and resistance and to develop future prevention and treatment strategies.

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Acknowledgments

We thank state and local health departments and public health laboratories for their hard work in completing interview forms and sending isolates to the Centers for Disease Control and Prevention (CDC).

Financial support. This work was funded by the CDC and the US Food and Drug Administration Center for Veterinary Medicine.

Manuscript preparation. The CDC had a direct role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, and approval of the manuscript.

Potential conflicts of interest. All authors: no conflicts.

  • Received November 19, 2007.
  • Accepted January 14, 2008.
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  1. Clin Infect Dis. (2008) 46 (11): 1656-1663. doi: 10.1086/587894
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