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BMC Infectious Diseases

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Salmonella enterica subspecies arizonae infection of adult patients in Southern Taiwan: a case series in a non-endemic area and literature review

  • Yi-Chien Lee1,
  • Miao-Chiu Hung2,
  • Sheng-Che Hung3, 4,
  • Hung-Ping Wang1,
  • Hui-Ling Cho5,
  • Mei-Chu Lai6 and
  • Jann-Tay Wang7Email author
BMC Infectious DiseasesBMC series – open, inclusive and trusted201616:746

https://doi.org/10.1186/s12879-016-2083-0

Received: 2 April 2016

Accepted: 1 December 2016

Published: 9 December 2016

Abstract

Background

The majority of Salmonella arizonae human infections have been reported in southwestern United States, where rattlesnake-based products are commonly used to treat illness; however, little is known in non-endemic areas. We reviewed and analyzed the clinical manifestations and treatment outcomes in adult patients with S. arizonae infection at our institution.

Method

A retrospective study was conducted at a regional teaching hospital in southern Taiwan from July 2007 to June 2014. All adult patients diagnosed with S. arizonae infections and treated for at least three days at Chia-Yi Christian Hospital were included. Patients were followed till discharge.

Results

A total of 18 patients with S. arizonae infections (median age: 63.5 years) were enrolled for analysis, of whom two thirds were male. The three leading underlying diseases were diabetes mellitus, peptic ulcer disease and malignancy. Ten patients had bacteraemia and the most common infection focus was the lower respiratory tract. Most of the patients (72.2%) received third-generation cephalosporins as definitive therapy. In contrast, ampicillin-based regimens (accounting for 45.2%) were the major treatment modalities in previous reports. The crude in-hospital mortality was 5.6%, which was much lower than what was previously reported (22.7%).

Conclusions

Though uncommon, there were cases of S. arizonae infections in Taiwan. Patients receiving third-generation cephalosporins treatment had better prognosis compared with those treated with ampicillin-based regimen.

Keywords

Salmonella arizonae Peptic ulcer diseaseProton pump inhibitorsThird generation cephalosporinsAmpicillin

Background

Salmonellae are Gram-negative, non-spore-forming, facultatively anaerobic bacilli belonging to the family of Enterobacteriaceae, which usually cause food-borne diseases. Salmonella arizonae, one of the less common members of Salmonellae, has the distinguishing biochemical characteristics of the ability to ferment lactose, utilize malonate, liquefy gelatin, and inhibition by the presence of potassium cyanide [1]. It was first reported in diseased reptiles in 1939 by Caldwell and Ryerson, and was named Salmonella dar-es-salaam at that time [2]. It has also been subsequently named Arizona hinshawii, S. arizonae, S. cholerasuis subsp. arizonae and finally reclassified as S. enterica subsp. arizonae in 1983 (S. arizonae was used throughout this manuscript) [3].

It was initially considered to be pathogenic only in reptiles, especially in snakes, with as many as 78.8% of them harboring the organism [4]. It was occasionally responsible for severe outbreaks in turkeys and sheep [4]. The first case of human infection by S. arizonae, presented with gastroenteritis, was recognized in 1944 [5]. Thereafter, S. arizonae was noted to be able to cause a spectrum of human diseases, including gastroenteritis, bacteraemia, vascular infection, bone and joint infection, and central nervous system infection [1, 4, 622]. Most of these infections have a good prognosis without any complications. However, severe human infection caused by S. arizonae has been documented in children below 7 years of age [23], immunocompromised adults, (e.g., autoimmune diseases under steroid therapy [1, 8, 10, 11, 14, 24, 25], malignancy [7, 13, 14, 21, 2629], human immunodeficiency virus (HIV) infection [1, 15, 17, 19, 30, 31], organ transplantation [11, 32]), or even in immunocompetent populations [18].

Cold-blooded animals are the usual habitats of S. arizonae, especially in reptiles or rattlesnake-based products. Other animals, including poultry, rats, and dogs [6, 9, 17], have also been involved in human infection by S. arizonae. According to previously published articles [1, 10, 13, 14, 16, 2529, 31], the geographic distributions of S. arizonae human infections are mainly located in south-western United States, where the use of rattlesnake-associated products to treat a wide variety of illnesses is popular among Mexican-Americans populations. Around 20 pediatric patients below 18 years of age suffering from S. arizonae infection have been reported in the literature [9, 17, 21, 23]. Little is known about S. arizonae infection of adult patients in Asian countries, including Taiwan. The aim of this study was to analyze all adult patients with S. arizonae infection at a regional teaching hospital in southern Taiwan and to perform a literature review on similar patients.

Methods

From July 2007 to June 2014, all adult patients (≥18 years) diagnosed with S. arizonae infection and treated for at least 3 days at Chia-Yi Christian Hospital (CYCH, a regional teaching hospital with a capacity of 1000 beds in southern Taiwan) were retrospectively enrolled. S. arizonae infection was defined as positive cultures of any kind of clinical specimens, including blood, pleural effusion, ascites, urine, sputum, stool, pus and bone, for S. arizonae plus the presence of signs of systemic or local infection. All types of specimens were collected, transported, and processed according to the suggestion described previously [33], and then inoculated into the corresponding culture media for subsequent incubation [34]. The blood culture system at CYCH was Bactec FX system (Becton, Dickinson and Co. [BD], Franklin Lakes, NJ). All bone tissues were collected by bone biopsy or surgical procedures. Potential pathogens were identified by Vitek version 2.0 (bio Merieux Suisse S.A., Geneva, Switzerland), and Salmonella isolates were confirmed by serologic testing (DifcoTM Antiserum Solutions). The culture-positive cases were identified by reviewing microbiology records at CYCH.

A standardized case report form was used to collect the demographics, clinical and laboratory data and treatment outcomes. Patients who used H2-receptor antagonists or proton pump inhibitors within one month prior to admission were defined as having peptic ulcer disease. Leukocytosis was defined as white blood cell counts exceeding 10 K/μl and thrombocytopenia was defined as platelet count below 150 K/μl. The infection foci of non-bacteraemic patients and patients with secondary bacteraemia were determined if there was a presence of clinical symptoms or signs of infection and isolation of S. arizonae from related clinical specimens. Bacteraemia without an obvious infection source or related to intravascular catheter infection or vascular lesions was classified as primary bacteraemia.

The antimicrobial susceptibilities to chloramphenicol, ciprofloxacin, trimethoprim/sulfamethoxazole, ampicillin and ceftriaxone were determined using the disk diffusion method according to the recommendation of the Clinical and Laboratory Standards Institute (CLSI) [35]. The results were also interpreted using the criteria suggested by CLSI [36]. Antimicrobial agents given before the susceptibility results were defined as empirical therapy, whereas definitive therapy was defined as effective antibiotic therapy prescribed according to the results of final blood cultures and susceptibility testing. The study was approved by the ethics review boards of the hospital [Chia-Yi Christian Hospital-Institutional Review Board (CYCH-IRB) No. 104035, 06/30/2015]. The IRB waived informed consent due to the retrospective study design and the research posing no more than minimal risk.

Continuous variables were described as medians with interquartile ranges (IQR) and categorical variables were described as percentage.

Results

A total of 485 adult patients with Salmonella species infection were identified during this seven-year period, and only 4.7% (23/485) of those patients suffered from S. arizonae infection. Five among them were excluded because they received treatment for less than 3 days at CYCH and did not follow-up subsequently. For the five eliminated patients, the median age was 65 years (IQR, 60–72 years). Four of them had primary bacteraemia and one had pneumonia. The demographics, clinical features, laboratory data and treatment outcome of the enrolled 18 patients are showed in Table 1. Of these 18 patients, the median age was 63.5 years, ranging from 27 to 81 years, with 12 men and six women. All patients lived in Chiayi City, except one, who lived in Yunlin County. All patients had various underlying diseases, including endocrine diseases in 12 (66.7%; diabetes mellitus in ten, and another diseases in two), peptic ulcer disease in eight (44.4%), malignancy in eight (34.8%; hepatocellular carcinoma in four, lung cancer in three, and colon cancer in one), hypertension in seven (38.9%), liver cirrhosis in six (33.3%), chronic viral hepatitis in six (33.3%; hepatitis B virus in five, and hepatitis C virus in two), chronic kidney disease in three (16.7%), autoimmune diseases in one, and acquired immunodeficiency syndrome in one (5.6%).
Table 1

Demographics and clinical data of 18 patients with S. arizonae infections in our case series

Age by years (median, range)

63.5 (27–81)

Male to female ratio

12 : 6

Underlying diseases (No., %)

 Diabetes mellitus

10 (55.6)

 Hypothyroidism

2 (11.1)

 Peptic ulcer diseases

8 (44.4)

 Hepatocellular carcinoma

4 (22.2)

 Lung cancer

3 (16.7)

 Colon cancer

1 (5.6)

 Multiple myeloma

1 (5.6)

 Hypertension

7 (38.9)

 Liver cirrohosis

6 (33.3)

 Hepatitis B

5 (27.8)

 Hepatitis C

2 (11.1)

 Chronic kidney diseases

3 (16.7)

 Systemic lupus erythematosus

1 (5.6)

 AIDS

1 (5.6)

Symptoms (No., %)

 Fever

9 (50.0)

 Abdominal discomfort

7 (38.9)

 Dyspnea

7 (38.9)

Laboratory data (No., %)

 WBC > 10000/μl

10 (55.6)

 CRP > 10 mg/dL

8/17 (47.1)

 ALT > 44 U/L

8/17 (47.1)

 Creatinine > 1.3 mg/dl

7/17 (41.2)

Site of bacterial isolation (No., %)

 Blood

10 (55.6)

 Bone

2 (11.1)

 Abscess

2 (11.1)

 Pleural effusion

2 (11.1)

 Sputum

1 (5.6)

 Stool

1 (5.6)

 Ascites

1 (5.6)

 Urine

1 (5.6)

Clinical presentations (No., %)

 Lower respiratory tract infection

4 (22.2)

 Bone and joint infection

3 (16.7)

 Gastrointestinal tract infection

3 (16.7)

 Intra-abdominal infection/peritonitis

3 (16.7)

 Soft tissue infection

2 (11.1)

 Mycotic aneurysm

2 (11.1)

 Urinary tract infection

1 (5.6)

Definite antibiotic treatment (No., %)

 3rd generation cephalosporins

13 (72.2)

 Fluoroquinolones

3 (16.7)

 Piperacillin/tazobactam

1 (5.6)

 TMP/SMX

1 (5.6)

Intensive care unit stay (No., %)

9 (50.0)

Length of hospitalization, days (mean ± standard deviation)

19.7 ± 13.7

In-hospital mortality (No., %)

1 (5.6)

AIDS acquired immunodeficiency syndrome, WBC white blood cell, CRP C-reactive protein, ALT alanine aminotransferase, TMP/SM trimethoprim/sulfamethoxazole

Nine patients (50.0%) had fever as their first presentations. The other initial presentations included abdominal discomfort (7/18, 38.9%), dyspnoea (7/18, 38.9%), cough (3/18, 16.7%), diarrhea (3/18, 16.7%), change in consciousness (2/18, 11.1%), and arthralgia (2/18, 11.1%). The median initial body temperature was 37.2 °C (IQR, 36.1–38.3) and 14 patients (77.8%) had initial heart rates above 90 beats per minute. Hypotension (systolic blood pressure < 90 mmHg) occurred in three patients. Leucocytosis was noted in ten patients (55.6%), and nine (50.0%) patients had thrombocytopenia. Seventeen patients had neutrophilia and eight patients (47.1%, one missing data) had elevated C-reactive protein levels of up to more than 10 mg/dL. For liver function tests, 11 patients (64.7%) had elevated aspartate or alanine transaminase values (AST > 38 U/L or ALT > 44 U/L). Impaired renal function at presentation, defined as serum creatinine > 1.3 mg/dl, was noted in 41.2% (7/17, one missing data) of patients. Initial serum albumin level was available in 13 patients only and 11 of them (84.6%) had hypoalbuminemia (albumin < 3 g/dL). Hyponatremia (sodium < 135 mmol/L) was found in 82.4% of patients (14/17, one missing data), and only four patients (23.5%, one missing data) had hypokalaemia (potassium < 3.5 mmol/L). Serum glucose level at presentation was only available in 13 patients, and five (38.5%) of them had elevated levels of ≥ 200 mg/dL.

Blood cultures were obtained in all 18 patients, and bacteraemia was identified in ten (55.6%), including primary bacteraemia in two, both with mycotic aneurysm and secondary bacteraemia in eight. The most common infection foci of patients with secondary bacteraemia and non-bacteraemic clinical syndromes were lower respiratory tract (4/18, 22.2%), followed by bone and joint (n = 3, 16.7%), gastrointestinal tract (n = 3, 16.7%), intra-abdominal infection or peritonitis (n = 3, 16.7%), soft tissue (n = 2, 11.1%), and urinary tract (n = 1, 5.6%). In-vitro susceptibility testing revealed that all isolates were susceptible to all of the five tested antimicrobials, i.e. no strains had decreased susceptibility to ciprofloxacin according to the 2013 CLSI guidelines. Seven patients received effective empirical antibiotics. The definite therapy included third-generation cephalosporins in 13 (72.2%) of 18 patients, of which three patients received combined therapy (oral co-trimoxazole in two and ciprofloxacin in one), fluoroquinolone in three (16.7%), piperacillin/tazobactam in one (5.6%), and oral co-trimoxazole in one (5.6%). The median duration of treatment with parenteral antibiotics was 12 days, ranging from 5 to 62 days. Of the 18 patients, the median hospital stay was 14 days, ranging from 6 to 62 days. Nine (50.0%) patients were admitted to the intensive care unit during their hospitalization. 17 patients recovered from this infection successfully after completion of the treatment course, and one patient died. Overall, the crude in-hospital mortality rate was 5.6% (1/18).

Discussion

Our present study demonstrates that S. arizonae infection is uncommon among adult patients with a crude in-hospital mortality rate of 5.6%. To the best of our knowledge, this is the largest case series reporting adult patients infected by S. arizonae. Based on a thorough search in PubMed, there were 27 studies reporting and discussing patients with S. arizonae infection from 1959 to the writing of the present manuscript. Clinical characteristics of these 44 reported patients, including age, gender, underlying diseases, type of infection, antibiotic therapy, exposure and treatment outcome, are displayed in Table 2.
Table 2

Characteristics, clinical diseases and outcome of 44 human infections with S. arizonae reported in the literature (1959–2012)

Reference

Age

Gender

Underlying Diseases

Type of Infection

Antibiotic Treatment

Exposure

Outcome

Krag 1959 [20]

63

F

idiopathic thrombocytopenic purpura

knee septic arthritis

achromycin

unknown

death

Guckian 1967 [24]

52

F

SLE, DM

knee septic arthritis/gastroenteritis/UTI

cephalothin/ampicillin/chloramphenicol

unknown

recover

Andrews 1970 [6]

21

M

none

gastroenteritis

ampicillin/chloramphenicol

dog

recover

Smilack 1975 [8]

23

F

SLE

knee/shoulder arthritis/tibial abscess

ampicillin/cephalothin

unknown

recover

Arora 1976 [18]

30

M

none

bacteraemia

chloramphenicol

unknown

recover

Keren 1976 [12]

53

M

alcoholism

osteomyelitis/gastroenteritis

ampicillin/aminoglycoside

unknown

recover

Johnson 1976 [32]

29

M

Hodgkin’s disease

bacteraemia/gastroenteritis/UTI

ampicillin

raw milk

death

Johnson 1976 [32]

54

M

post heart transplant

bacteraemia/gastroenteritis

cephalothin/gentamicin

unknown

death

Johnson 1976 [32]

54

F

mental retardation

gastroenteritis/pneumonia/empyema

ampicillin

unknown

recover

Petru 1981 [22]

53

M

DM/interstitial pneumonitis

bacteraemia/mycotic aneurysm

ampicillin/gentamicin

NA

recover

Lindsay 1981 [40]

69

F

cirrhosis

bacteraemia/peritonitis

cephalosporin/aminoglycoside/chloramphenicol

unknown

death

Fainstein 1982 [13]

66

M

leukaemia

bacteraemia

ticarcillin/aminoglycoside

rattlesnake capsule

death

Mcintyre 1982 [16]

73

M

DM/HTN

septic arthritis/aortic aneurysm/UTI

ampicillin

rattlesnake capsule

recover

CDC 1983 [7]

63

F

gallbaldder adenocarcinoma

bacteraemia

?

Rattlesnake capsule

recover

Quismorio 1983 [11]

31

F

SLE

septic arthritis

ampicillin

unknown

death

Quismorio 1983 [11]

41

M

HBV, post renal transplant

septic arthritis/kidney abscess

ampicillin

unknown

death

Quismorio 1983 [11]

48

F

Waldenstrom macroglobulinemia

septic arthritis/gastroenteritis/UTI

ampicillin

unknown

death

Riley 1988 [1]

19

F

SLE

bacteraemia

ampicillin

rattlesnake capsule

recover

Riley 1988 [1]

25

M

AIDS

adenitis/empyema

TMP/SMX

rattlesnake capsule

recover

Riley 1988 [1]

51

M

HTN/DCM/CHF/atrial fibrillation

pleurisy

nil

rattlesnake capsule

recover

Bhatt 1989 [10]

27

F

SLE

bacteraemia/gastroenteritis/peritonitis/

meningitis

ampicillin

rattlesnake meat

death

Fleischman 1989 [28]

38

M

gastric carcinoma

bacteraemia/empyema

ampicillin

rattlesnake capsule

recover

Jacobson 1989 [19]

49

F

AIDS

bacteraemia

ciprofloxacin

unknown

recover

Cone 1990 [14]

71

F

RA

bacteraemia/arthritis/gastroenteritis

ceftriaxone/chloramphenicol

folk remedy

recover

Cone 1990 [14]

72

M

metastatic melanoma

bacteraemia

aztreonam

rattlesnake capsule

recover

Casner 1990 [31]

30

M

AIDS/Kaposi’s sarcoma

bacteraemia/UTI

Baktar

rattlesnake capsule

recover

Caravalho1990 [25]

55

F

RA

endophthalmitis

cephalosporin

powder

recover

Woolf 1990 [27]

28

F

adenocarcinoma

peritonitis

ampicillin

capsule

death

Babu 1990 [30]

25

M

AIDS/Kaposi’s sarcoma

bacteraemia/gastroenteritis/UTI

ciprofloxacin

rattlesnake powder

recover

Noskin 1990 [15]

57

M

AIDS

bacteraemia

ampicillin

rattlesnake meat

recover

Kraus 1991 [21]

49

F

SLE

cholecystitis/bacteraemia

cephalothin/amikacin

rattlesanke capsule

recover

Kraus 1991 [21]

27

M

dermatomyositis

hip septic arthritis

ciprofloxacin

rattlesnake capsule

recover

Kraus 1991 [21]

34

F

SLE

knee septic arthritis

ciprofloxacin

rattlesnake capsule

recover

Kraus 1991 [21]

36

F

SLE

knee/shoulder septic arthritis/sepsis

ampicillin

rattlesnake capsule

recover

Kraus 1991 [21]

29

F

SLE

knee/shoulder septic arthritis/bacteraemia/UTI

ampicillin/amikacin

rattlesnake capsule

recover

Kraus 1991 [21]

24

F

leukaemia

bacteraemia

ciprofloxacin

unknown

recover

Kraus 1991 [21]

61

F

Primary biliary cirrhosis

vertebral osteomyelitis/UTI

ampicillin/amikacin

unknown

recover

Kraus 1991 [21]

25

F

SLE

UTI

TMP/SMX

NA

recover

Kraus 1991 [21]

70

M

DM, ALS

bacteraemia

TMP/SMX

rattlesnake capsule

recover

Sharma 1992 [29]

69

M

gastric cancer

peritonitis

cefotaxime/gentamicin

rattlesnake pills

recover

Cortes 1992 [26]

60

M

metastatic carcinoma

bacteraemia/pneumonia

aztreonam

rattlesnake meat

recover

Hoag 2005 [17]

47

F

AIDS

bacteraemia/pericarditis/gastroenteritis/UTI

ceftriaxone/ciproxin

pet chicken?

recover

Di Bella 2011 [4]

43

M

Hodgkin’s disease/

panhypoglobulinemia

gastroenteritis

ciprofloxacin

NA

recover

S. Kolker 2012 [9]

32

F

pemphigus

tibial abscess

ceftriaxone/ciproxin

iguana/snakes

recover

F female, M male, SLE systemic lupus erythematosus, DM diabetes mellitus, HTN hypertension, HBV hepatitis B, AIDS acquired immunodeficiency syndrome, DCM dilated cardiomyopathy, CHF congestive heart failure, RA rheumatoid arthritis, ALS amyotrophic lateral sclerosis, UTI urinary tract infection, TMP/SMX trimethoprim/sulfamethoxazole, NA not available

Patients in the present study were either elderly male or had various underlying conditions (Table 1) which would compromise their cell-mediated immunity. In the literature (Table 2), the most commonly reported comorbidities associated with S. arizonae infections were immunocompromised status, including connective tissue diseases under steroid therapy (40.9%), malignancy (27.3%) and acquired immunodeficiency syndrome (13.6%) [15, 17]. Our case series produced similar findings. Additionally, we identified three more associated host underlying conditions, including type 2 diabetes mellitus, liver cirrhosis, and peptic ulcer disease. Uncontrolled diabetes and liver cirrhosis have been shown to cause impairment of humoral- and cell-mediated immunity, which play important roles in clearing Salmonella [37]. Therefore, these two diseases would reasonably predispose to the development of S. arizonae infection. Moreover, patients with peptic ulcer diseases received acid suppressants to treat their diseases. Usage of acid suppressants would not only decrease the acidity of gastric juice, which in turn might result in intestinal bacterial overgrowth, facilitate bacterial translocation from the intestine and lead to infection via the gastro-intestinal route [38], but also reduce the gastric acid barrier with subsequent infection despite a lower inoculum of bacteria. Similar findings have been previously reported by Wu et al. [39].

A variety of clinical manifestations were displayed in our series, including enterocolitis, bacteraemia, vascular infection and localized infections. The rank order of infection syndromes in our reports was bacteraemia, intra-abdominal infection, and pulmonary infection. In contrast, bacteraemia [1, 7, 10, 1315, 1719, 21, 22, 26, 28, 3032], intra-abdominal infection [4, 6, 1012, 14, 17, 21, 24, 27, 29, 30, 32, 40] and bone or joint infection [8, 9, 11, 12, 14, 20, 21, 24] were the most common clinical manifestations in previously-reported patients (Table 2). Much fewer patients with bone and joint infection (16.7%) were noted in our present study. Interestingly, both of the two patients in our series diagnosed as S. arizonae related mycotic aneurysm with bacteraemia had a past history of hypertension. This is similar to the result by Wang JY et al., who demonstrated that hypertension was the major factor predisposing to S. choleraesuis mycotic aneurysm [41]. Importantly, our study is the first one to demonstrate that soft tissue could be the infection focus of S. arizonae, which was observed in two of our patients. Overall, the difference in clinical manifestations between our study and prior reports might be due to the small number of patients enrolled in every study. Therefore, further study is needed to clarify whether geographic variance or other factors were associated with the difference of clinical syndromes.

All S. arizonae isolates collected in the present study were susceptible to all five of the recommended anti-Salmonella agents, including chloramphenicol, ciprofloxacin, trimethoprim/sulfamethoxazole, ampicillin, and ceftriaxone. These five antimicrobial agents have the ability to penetrate host cells, which is crucial in killing intra-cellular pathogens, such as Salmonella. All of our patients received at least one of these five agents as their definite therapy, among which third-generation cephalosporins were prescribed for the majority of patients (72.2%, Table 1). Instead, ampicillin was usually chosen as the backbone of the treatment modality (45.2%) in previously published articles (Table 2). Although the difference was not statistically significant (p = 0.1 by chi-square test), the crude in-hospital mortality rate was only 5.6% in the present study, which was much lower than that (10/44, 22.7%) of the prior reports (Table 2). In particular, 6 of the 10 fatal patients in prior reports received ampicillin as their treatment against S. arizonae infection. Therefore, a third-generation cephalosporin could potentially be a better choice for treating S. arizonae infection compared to ampicillin. However, further investigation is needed.

One patient in our study received piperacillin/tazobactam, which is not the recommended antibiotic as the definitive treatment against Salmonellae , and had a favorable outcome. Using piperacillin/tazobactam for Salmonella infection was rarely reported in previous articles. Bell SD demonstrated that minimal inhibitory concentration of piperacillin/tazobactam for S. arizonae isolated from this study was 4 μg/mL [4], implicating the bacterium susceptible to it in-vitro. Gerada et al. reported a liver transplant recipient with Salmonella related infectious aortitis and bacteraemia, who responded well to piperacillin/tazobactam treatment [42]. Thus, piperacillin/tazobactam might be considered as one of the therapeutic options for S. arizonae infection.

During the 1980s, S. arizonae infection became an important issue in public health due to the emergence of many severe infection cases, and its association with extensive use of rattlesnake-based products [10, 19, 28] mainly in areas with large Mexican-American populations in southwestern United States [1, 7, 13]. Approximately 70% of the 44 patients reported in previous studies (Table 2) mentioned a history of exposure to reptiles, especially snakes. Rattlesnake-based products are not common in Taiwan and we could not identify any specific animal contact history from the medical records of those patients. It is important to identify whether natural habitats of S. arizonae are present and whether S. arizonae infection is one of the zoonoses in Taiwan. Further studies are needed to identify the possible sources of this infection.

Conclusions

Our study showed that S. arizonae infection, although uncommon, is present in Taiwan, an area outside of typical endemic areas. In addition to previously reported risk factors, usage of acid suppressants, such as proton pump inhibitors and H2 blockers, might also predispose to S. arizonae infection. To treat S. arizonae infection, third-generation cephalosporins might be more effective than ampicillin.

Abbreviations

AIDS: 

Acquired immunodeficiency syndrome

ALS: 

Amyotrophic lateral sclerosis

ALT: 

Alanine aminotransferase

CHF: 

Congestive heart failure

CLSI: 

Clinical and laboratory standards institute

CRP: 

C-reactive protein

CYCH: 

Chia-Yi Christian hospital

DCM: 

Dilated cardiomyopathy

DM: 

Diabetes mellitus

F: 

Female

HBV: 

Hepatitis B

HTN: 

Hypertension

M: 

Male

NA: 

Not available

RA: 

Rheumatoid arthritis

SLE: 

Systemic lupus erythematosus

TMP/SMX: 

Trimethoprim/sulfamethoxazole

UTI: 

Urinary tract infection

WBC: 

White blood cell

Declarations

Acknowledgments

We would like to acknowledge Management Information System Engineer Mrs. Fang-ling Kao for acquisition and analysis of data.

Funding

There were no external or internal sources of specific funding for this paper.

Availability of data and materials

The datasets supporting the conclusions of this article would be obtained by contacting the author at cimedin7@yahoo.com.tw.

Authors’ contributions

YCL and JTW designed, executed, and supervised the study. YCL drafted the manuscript, and MCH and SCH helped writing of the article. SCH, HPW and MCL participated in collection, analysis and interpretation of the data. HLC carried out the literature review. YCL, MCH and JTW critically reviewed the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

The study was approved by the Institutional Review of Board of Chia-Yi Christian Hospital (CYCH-IRB No. 104035, 06/30/2015). The IRB waived both the informed consent due to the retrospective study design and the research posing no more than minimal risk.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Internal Medicine, Ditmanson Medical Foundation Chia-Yi Christian Hospital
(2)
Department of Pediatrics, Taipei Veterans General Hospital
(3)
Department of Radiology, Taipei Veterans General Hospital
(4)
School of Medicine, National Yang-Ming University
(5)
Department of Nursing, Ditmanson Medical Foundation Chia-Yi Christian Hospital
(6)
Department of Laboratory Medicine, Ditmanson Medical Foundation Chia-Yi Christian Hospital
(7)
Department of Internal Medicine, National Taiwan University Hospital

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© The Author(s). 2016

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