A comprehensive review of disseminated Salmonella arizona infection with an illustrative case presentation.

Abstract: Salmonella arizona is known to cause infection in reptiles and other animals. Disseminated human infection is rare, except in the setting of a deficient immune system. The following is a unique account of disseminated infection including pericardial involvement. Unusual features include nonreptile vector transmission and eastern seaboard (rather than southwestern) locale. A comprehensive literature review of disseminated S arizona infections is presented describing the types of infection, sources of exposure, underlying conditions, locale, treatments, and outcomes.

Key Words: Salmonella arizona, pericarditis, rattlesnake 

Introduction

Salmonella arizona is an uncommon human pathogen. Over the last 50 years, approximately 50 case reports and case series have appeared in the literature. Serious human infections have been reported in hosts with impaired immune systems caused by conditions such as collagen vascular diseases requiring immunosuppressive therapy, (1-8) malignancy, (4,9-16) organ transplantation, (6,15) human immunodeficiency virus (HIV) infection, (1,5,17-20) and a young age (16,21-28) (< 7 years old). The majority of cases cited originated from the southwestern United States, primarily in California, (1-6,11-12,15,17,29-31) Arizona, (24,32) and Texas. (2,3,7-9,13,14,19) This geographic region corresponds to a large Latino population known to use folk remedies for a variety of illnesses. In particular, rattlesnake meat, (2,13,18,24) capsules (1,4,5,9-12,14,19,32,33), and powders (3,20) have been linked to infection with S arizona, although other animals or animal products have been implicated, including reptiles, poultry, sheep, rats, dogs, and cats. (34-38) This organism has caused disease in virtually every tissue in the human body and is often difficult to eradicate. Since serious infection has not been documented in a healthy human adult, isolation of S arizona should prompt evaluation of the immune status in apparently healthy individuals.

We present a case of pericardial infection associated with disseminated S arizona infection. Recognition of this unusual infection led to the diagnosis of HIV infection, and prolonged treatment resulted in a full recovery without recurrence.

Illustrative case

A previously healthy, 47-year-old black female presented to the emergency department complaining of progressive dyspnea of 1 week's duration. The patient reported worsening dyspnea on exertion that progressed to frank shortness of breath at rest over the course of 2 days, as well as diaphoresis and new onset pedal edema. She reported no chest pain or similar symptoms in the past. A review of systems revealed complaints of watery diarrhea without melena for 2 weeks before this admission and an approximate 40-pound unintentional weight loss during the preceding 3 months. She reported no fever, nausea, vomiting, dysuria, headache, or dizziness. Furthermore, she reported no previous surgery or travel outside of her hometown in Virginia during the preceding 10 years.

Vital signs included a blood pressure of 114/62 mm Hg, heart rate of 125/min, respiratory rate of 28 breaths/min, rectal temperature of 101.0[degrees]F, and a pulse oximetry of 70% on room air, and 99% while breathing 100% [O.sub.2] by nonrebreather mask. In general, she was a morbidly obese (body mass index = 49.7 kg/[m.sup.2]) female in moderate respiratory distress. Her oropharynx was normal, and mild, clear rhinorrhea was noted. Moderate jugular venous distension was present, and no carotid bruits were heard. She was using accessory muscles of respiration, and the lung examination revealed bilateral crackles in the lower halves of her lung zones with dullness to percussion at the bases. Her cardiovascular examination was significant for tachycardia with a regular rhythm, a prominent [S.sub.2], and a faint systolic ejection murmur at the lower left sternal border, but no rubs or gallops. Her abdomen was protuberant and soft, with normal bowel sounds and a reducible periumbilical hernia without tenderness or distension. A rectal examination showed Hemoccult negative brown stool and normal sphincter tone. Her lower extremities had bilateral pitting edema up to her thighs with faintly palpable peripheral pulses. Skin examination revealed an absence of rashes, tattoos, or areas of skin breakdown. Her neurologic examination was unremarkable.

Admission laboratory data revealed the following: blood urea nitrogen, 43 mg/dL; creatinine, 5.1 mg/dL; glucose, 201 mg/dL; albumin, 2.1 g/dL; aspartate aminotransferase, 69 U/L; international normalization ratio, 1.1; partial thromboplastin time (PTT), 36 seconds; creatine kinase, 641 U/L; creatine kinase-muscle/brain fraction, 4.7 [micro]g/L; troponin I, 2.9 [micro]g/L; erythrocyte sedimentation rate, 71 mm/h; and white blood cell count, 10.1 X [10.sup.6]/mL (75% PMNs). An arterial blood gas revealed a pH of 7.41, pC[O.sub.2] of 34 mm Hg, p[O.sub.2] of 43 mm Hg, and 79% saturation while breathing room air. The electrocardiogram showed sinus tachycardia at 131/min, normal QRS axis, normal intervals, low voltage, and nonspecific ST-T wave changes. Her chest radiograph revealed low lung volumes, a large cardiac silhouette suggesting global chamber enlargement and/or pericardial effusion, mild interstitial edema, and no alveolar infiltrate.

In the emergency department, blood and urine cultures were obtained, and she was given imipenem and levofloxacin as empiric antibiotic treatment. She was admitted to the medical intensive care unit, where a bedside transthoracic echocardiogram showed a left ventricular ejection fraction of 71%, moderate tricuspid regurgitation, moderate pulmonary hypertension, and no evidence of pericardial effusion. Because of the patient's size, a computed tomography scan for pulmonary embolism was deferred and a pulmonary angiogram was performed, which showed multiple bilateral subsegmental basilar emboli. At this point, she was started on unfractionated heparin infusion for treatment of pulmonary embolism. Approximately 6 hours after intravenous heparin therapy was started, the patient had worsening shortness of breath. Physical examination at this time revealed a three-component friction rub heard across the precordium. The heparin infusion was stopped, and an emergent echocardiogram showed a large pericardial effusion with severe right ventricular dysfunction (PTT at this time was 46 seconds). A bedside pericardiocentesis by subxiphoid approach under electrocardiographic and echocardiographic guidance was performed, and approximately 700 mL of bloody, nonclotting fluid was drained and sent for culture.

The following morning, her admission blood cultures were reported as growing Gram-negative bacilli. Empiric antibiotics were changed to ceftazidime and levofloxacin. The following day, the Gram-negative rod was identified as Salmonella arizona (subgroup III, group Y, serotype 48:G, Z51:-), which was sensitive to both ceftazidime and levofloxacin. The same species of bacteria was later isolated from the pericardial fluid, stool, and urine. Because of the known association between this type of disseminated infection and an underlying cell-mediated immunity defect, we pursued evaluation of possible causes. Subsequent serologic testing was negative for antinuclear antibodies and rheumatoid factor. Testing for HIV by enzyme-linked immunosorbent assay returned positive and was confirmed by Western blot for HIV type 1. Later, the patient's absolute CD4 count and HIV viral load returned as 12 mL (normal, 600 to 1500/mL) and 6.97 X [10.sup.5] copies/mL, respectively.

Our patient had multiple medical problems and complications coincident to her hospitalization, including renal failure requiring hemodialysis, shock requiring vasopressive therapy with phenylephrine and norepinephrine, incarcerated periumbilical hernia requiring surgical abdominal herniorrhaphy, and a central line-associated, methicillin-resistant Staphylococcus aureus bacteremia. Her antibiotic coverage for S arizona was changed to ciprofloxacin and ceftriaxone, and she completed a 4-week course.

After a prolonged, complicated hospitalization, she recovered without long-term sequelae and is currently receiving highly active antiretroviral therapy (HAART). Her absolute CD4 count has increased above 300/mL after initiation of HAART therapy, and her HIV viral load is undetectable. At follow-up 18 months after initial presentation, she had no recurrence of infection with S arizona or other opportunistic infections. Interestingly, our patient reported no ingestion of alternative medicines, contact with reptiles, or travel to the southwestern United States. She did, however, describe close contact with approximately 15 chickens that she raised as pets, an association previously reported by others (31) as a possible source of exposure. She said that she had never used recreational drugs, had not received blood products by transfusion, and did not have tattoos. She said that she had no unprotected sexual activity in the 5 years before this admission, and her mode of contraction of HIV remains uncertain.

Discussion and Literature Review

A review of the English language literature available was performed with the use of MEDLINE (National Library of Medicine, Bethesda, MD) to search for publications containing S arizona or Arizona hinshawii, as well as review of the citations listed as references from results of the search. Features of the reported cases, including age, race, sex, type of infection, exposure, underlying immunocompromise, treatment, recurrence, outcome, and locale, are displayed in Table 1.

Salmonella arizona is a facultative anaerobic Gram-negative bacillus of the family Enterobacteriaceae, which has the ability to ferment lactulose and liquefy gelatin; its growth is inhibited by cyante. (1) This bacteria was first isolated from diseased reptiles in Arizona in 1939 (40) and was called "Salmonella. dar-es-saalam variety from Arizona," later Arizona hinshawii, and finally reclassified as Salmonella arizona in 1983. Not long after its discovery, a human case of gastroenteritis caused by S arizona was identified. (41) Since that time, S arizona infection has been documented in a myriad of animals including reptiles, fowl, ducks, rats, dogs, and cats. (35) Additional outbreaks of gastroenteritis have been linked to contaminated dairy and egg products. (34,36,37)

Serious human infections were very rare until multiple cases were identified in the 1980s, associated with widespread use of rattlesnake meat, capsules, and powders in the Latino communities in the southwestern United States as a form of alternative medicinal therapy. (1,2,9-11,17,33) Users of rattlesnake products believed that these preparations were beneficial for many illnesses including arthritis, diabetes mellitus, cancers, and HIV infection. (33,42) Into the 1990s, sporadic cases of disseminated S arizona infection were identified (3-5,12-14,18-20) until the California Public Health Department was instrumental in banning the sale of these preparations in the United States (43) (Table 2).

Infection has been documented in individuals ranging from 8 weeks to 87 years of age. Blacks and whites have been infected, although the majority of cases have occurred in Hispanics in the southwestern United States, probably related to the use of rattlesnake products. Although from one to nine cases per year of S arizona have been reported to the Virginia Department of Health [personal correspondence, Department of Epidemiology, Virginia Department of Health, Richmond, VA] since 1990, isolation from stool was the norm, and none were known to cause serious or disseminated infection.

The portal of entry for the bacteria into a human host is postulated to be the gastrointestinal tract as a result of eating a product that contains the bacteria. Salmonella then is thought to disseminate through the blood and lymphatics, (44) although this has not been evaluated with certainty. The time interval from exposure to development of overt clinical manifestation of infection appears to be variable. In a case series reported by Kraus, the mean time from exposure to infection was 3 months, (45) though Cortes documented a case in which the last known exposure to rattlesnake meat was up to 6 years earlier. (13) Thus, it is possible that colonization occurs for extended periods before the onset of illness.

Common to adults with serious S arizona infection is an impaired cell-mediated immune response. Multiple comorbid conditions have been documented including rheumatoid arthritis (3-5,45) and systemic lupus erythematosus on corticosteroid therapy, (1-27,28) malignancy, (4,9-14) HIV infection, (1,5,17-20) status posttransplantation, (6,15) and others cited in Table 3. Of the cases reviewed in which S arizona caused serious infection in individuals with connective tissue diseases and usual interstitial pneumonia, concomitant corticosteroid therapy was universal, suggesting the infection was a complication of therapeutic immunomodulation, rather than of the condition itself.

Salmonella arizona has been isolated from a variety of biological fluids and tissue, including blood, urine, stool, and others (Table 4). To the best of our knowledge, our case represents the first documented infection in which S arizona was isolated from pericardial fluid reported in the English language literature. The hemorrhagic nature of the pericardial fluid raises the question regarding whether primary infection was present initially with subsequent hemorrhage related to systemic anticoagulation or whether bleeding into the pericardial space was the sole source of bacteria. Confounding issues include renal failure and recent non-Q-wave myocardial infarction. Uremia has been associated with hemorrhagic pericarditis in the presence of anticoagulation with heparin (46); however, our patient's blood urea nitrogen was only 43 mg/dL; thus, frank uremia was not present. Also, as reviewed by Figueras, (47) anticoagulation with unfractionated heparin after myocardial infarction has not been shown to increase the incidence of hemorrhagic pericardial effusions. In a large review of complications of anticoagulation including major bleeding and death, hemorrhagic pericardial effusion was not listed as a complication of anticoagulation with intravenous unfractionated heparin therapy. (48) Moreover, in prior cases described in the literature, when other serous fluids including pleural (15) and peritoneal (12,14,30) fluid were involved, the samples were not noted to be hemorrhagic. Although our patient reported no chest pain on presentation, suppurative pericarditis may present silently, with tamponade as the initial manifestation of infection, and, as in our patient, overshadowed by concomitant systemic illness. (49) Furthermore, infectious pericarditis is usually the result of bacteremia. (50) For these reasons, we believe the hemorrhagic pericarditis was a direct result of disseminated infection with S arizona, while acknowledging that this is not proven.

How S arizona has been able to invade virtually all parts of the human body has been under investigation. Noskin (18) proposed a defect in cell-mediated immunity, as seen with HIV infection, as instrumental in pathogenesis. Salmonella strains are able to invade epithelial cells and macrophages. (44) In the macrophages, the bacteria proliferate and cause cell destruction with subsequent further dissemination of organisms. (49) Libby (51) determined that the virulence associated with S arizona was related to genes in the spv locus on the chromosome of this and other Salmonella species. The spv locus genes encode an ADP ribosyltransferase that is able to modify and destabilize the infected cells due to actin destabilization, therefore, enhancing the organism's growth. (44)

There has not been a uniform therapy for this type of infection. As documented in several of the case reports, this organism appears to be susceptible to commonly prescribed antibiotics. However, due to the critical nature of illness in these patients and their underlying immunocompromise, prolonged courses of therapy have been used. Moreover, recurrence of infection has been documented after apparent clearance of the organism demonstrated by negative cultures. (1-3,7,8,13,14,17,20,26,52) Although incomplete treatment is a possible explanation, reexposure has also been noted, especially when medicinal rattlesnake preparations are causative. (1,2) According to Jacobson, (17) standards of therapy for salmonellosis include ampicillin, trimethoprim/sulfamethoxazole, and chloramphenicol, although other [beta]-lactams, fluoroquinolones, aminoglycosides, and vancomycin in various combinations have also been used with apparent efficacy. Our patient responded to a combination of prolonged therapy (4 weeks) with antibiotics in combination with improved immune status as a result of HAART therapy.

Conclusions

Several important pieces of information can be gleaned from our case and review of the literature regarding S arizona infection. First, disseminated S arizona infection can be found outside of the typical geographic region and may not be associated with typical animal vectors such as snakes and reptiles. Second, the manifestations are protean, including infection of serosal surfaces. Third, the isolation of this organism from blood, tissue, or normally sterile body fluids should prompt an evaluation for underlying immunocompromise, since this is almost universal among patients with invasive disease. In 1987, the Centers for Disease Control and Prevention's National Center for HIV, STD and TB Prevention classified recurrent Salmonella infection as an AIDS indicator. (53) Fourth, although the organism tends to be susceptible to many antibiotics, patients who have serious infections with S arizona require prolonged therapy because of the high risk for recurrence. Finally, a detailed history of exposures to nonmainstream medicinal therapies is important, and education is paramount as reinfection is a real possibility.

Acknowledgments

The authors thank Dr. Richard Wenzel for his careful scrutiny and assistance with editing.

References

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Never confuse a single defeat with a final defeat.
--F. Scott Fitzgerald

Jeffrey B. Hoag, MD, MS, and Curtis N. Sessler, MD

From the Department of Internal Medicine, Division of Pulmonary and Critical Care Medicine, Johns Hopkins University Medical Center, Baltimore, MD; and the Department of Internal Medicine, Division of Pulmonary and Critical Care Medicine, Virginia Commonwealth University, Medical College of Virginia Hospitals, Richmond, VA.

Reprint requests to Curtis N. Sessler, MD, Department of Internal Medicine, Division of Pulmonary and Critical Care Medicine, Virginia Commonwealth University, Medical College of Virginia Hospitals, Box 980050, Richmond, VA 23298-0050. E-mail: [e-mail]

Accepted April 1, 2005.

RELATED ARTICLE: Key Points

* Disseminated Salmonella arizona infection should prompt investigation into underlying immunocompromise.

* Although most cases in the literature have occurred in the southwestern United States, eastern seaboard infections occur.

* Recurrence after adequate antibiotic therapy is common, thus requiring prolonged antibiotic therapy and vigilance in removing possible sources of exposure.

Table 1. Composite data from case reports or series of Salmonella
arizona infection from 1952 to 2004a

                      Age, race,     Type of             Exposure
Reference             sex            infection

Current 2002          47 yr, B, F    Pericarditis, UTI,  Chickens?
                                       bacteremia
Nowinski 2000 (21)     7 mo, F       Arthritis           Pet iguana
Buck 1997 (22)         3 mo, M       Gastroenteritis     Pet snake
Sanyal 1997 (23)       5 yr, M       Gastroenteritis     Pet snake
Kelly 1995 (24)        6 yr, H       Gastroenteritis     Meat
Sharma 1993 (14)      69 yr, H, M    Peritonitis         Capsules
Cortes 1992 (13)      60 yr, H, M    Bacteremia          Meat
Waterman 1990 (5)     H              Pneumonia, UTI      Capsules
                      H              Perirectal abscess  Capsules
                      H              Perirectal abscess  Capsules
                      H              Gastroenteritis     Capsules
Cone 1990 (4)         71 yr, H, F    Bacteremia          "Folk remedy"
                      72 yr, H, M    Bacteremia          Capsules
Caravalho 1990 (3)    55 yr, H, F    Endophthalmitis     Powder
Woolf 1990 (12)       28 yr, F       Peritonitis         Capsules
Babu 1990 (20)        25 yr, H, M    Bacteremia          Powder
Casner 1990 (19)      30 yr, H, M    Bacteremia          Capsules
Noskin 1990 (18)      57 yr, H, M    Bacteremia          Meat
Bhatt 1989 (2)        27 yr, H, F    Bacteremia,         Meat
                                       gastroenteritis
Fleischman 1989 (11)  38 yr, H, M    Bacteremia          Capsules
Jakobson 1989 (17)    49 yr, W, F    Bacteremia          Unknown
Riley 1988 (1)        19 yr, H, F    Bacteremia          Capsules
                      25 yr, H, M    Gastroenteritis     Capsules
                      51 yr, H, M    Bacteremia          Capsules
Croop 1984 (39)                      Osteomyelitis       Pet snake
Marzouk 1983 (10)     63 yr, H, M    Bacteremia          Capsules
Quismorio 1993 (6)    31 yr, H, M    Arthritis           Unknown
                      41 yr, A, M    Arthritis, UTI,     Unknown
                                       abscess
                      48 yr, H, F    Arthritis,          Unknown
                                       bacteremia
Fainstein 1982 (9)    66 yr, H, M    Bacteremia          Capsules
McIntyre 1981 (32)    73 yr, H, M    Arthritis, UTI,     Capsules
                                       aortitis
Petru 1981 (31)       53 yr, M       Bacteremia          Hens at home
Ichord 1980 (25)       8 wk, W, F    Bacteremia,         Pet turtle,
                                       meningitis        milk
Lindsay 1980 (30)     69 yr, F       Peritonitis,        Unknown
                                       bacteremia
Ogden 1979 (26)        2 yr, B, M    Osteomyelitis       Unknown
                       1 yr, B, M    Osteomyelitis       Unknown
Keren 1976 (51)       53 yr, B, M    Disseminated        Unknown
Johnson 1976 (15)     29 yr, H, F    Bacteremia,         Raw milk
                                       gastroenteritis,
                                       empyema,
                                       pneumonia
                      54 yr, W, M    Gastroenteritis     Unknown
                      54 yr, W, M    Pneumonia           Unknown
Smilack 1975 (7)      23 yr, B, F    Osteomyelitis,      Unknown
                                       arthritis
Hruby 1973 (27)        2.5 yr, B, F  Bacteremia          Unknown
Guckian 1967 (8)      52 yr, B, F    Arthritis, UTI      Unknown
Krag 1959 (29)        87 yr, W, F    Abscess             Unknown
                      63 yr, W, F    Osteomyelitis,      Unknown
                                       arthritis
Fisher 1953 (16)       2 yr, B, M    Osteomyelitis,      Raw milk
                                       bacteremia
Butt 1952 (28)         7 yr, B, F    Otitis media        Unknown

                      Age, race,     Underlying
Reference             sex            condition               Antibiotic

Current 2002          47 yr, B, F    HIV/AIDS (CD4 12)       Cep, Q
Nowinski 2000 (21)     7 mo, F       Young age               Cep
Buck 1997 (22)         3 mo, M       Young age               Sal
Sanyal 1997 (23)       5 yr, M       Netherton syndrome      Q
Kelly 1995 (24)        6 yr, H       Young age               Cep
Sharma 1993 (14)      69 yr, H, M    Metastatic AdenoCa      Cep, AG
Cortes 1992 (13)      60 yr, H, M    Right Neck Mass         AZ, Q
Waterman 1990 (5)     H              HIV/AIDS
                      H              RA, Dermatitis
                      H
                      H
Cone 1990 (4)         71 yr, H, F    RA, corticosteroids     Cep, Chl
                      72 yr, H, M    Metastatic melanoma     V, AZ
Caravalho 1990 (3)    55 yr, H, F    Rheumaroid arthritis    Cep, AG
Woolf 1990 (12)       28 yr, F       Pregnant, AdenoCa       AMP
Babu 1990 (20)        25 yr, H, M    HIV/AIDS                Q
Casner 1990 (19)      30 yr, H, M    HIV/AIDS                SMX-
                                                               TMP
Noskin 1990 (18)      57 yr, H, M    HIV (CD4 300)           AMP, AG
Bhatt 1989 (2)        27 yr, H, F    SLE, corticosteroids    AMP
Fleischman 1989 (11)  38 yr, H, M    Gastric cancer          AMP
Jakobson 1989 (17)    49 yr, W, F    HIV/AIDS                Q
Riley 1988 (1)        19 yr, H, F    SLE, corticosteroids    AMP
                      25 yr, H, M    HIV                     AMP
                      51 yr, H, M    CHF, Afib, dilated
                                       CM
Croop 1984 (39)
Marzouk 1983 (10)     63 yr, H, M    AdenoCa
Quismorio 1993 (6)    31 yr, H, M    SLE, corticosteroids    AMP
                      41 yr, A, M    Renal transplant        AMP, Cep
                      48 yr, H, F    W. Macroglob            AMP
Fainstein 1982 (9)    66 yr, H, M    Leukemia                TIC, AG
McIntyre 1981 (32)    73 yr, H, M    DM, HTN                 AMP
Petru 1981 (31)       53 yr, M       UIP on corticosteroids  AMP, AG
Ichord 1980 (25)       8 wk, W, F    Young age               AMP, Chl
Lindsay 1980 (30)     69 yr, F       Alcoholic, cirrhosis    Cep, AG,
                                                               Chl
Ogden 1979 (26)        2 yr, B, M    SSA                     Chl
                       1 yr, B, M    SSA                     Chl
Keren 1976 (51)       53 yr, B, M    Alcohol abuse           AMP, AG
Johnson 1976 (15)     29 yr, H, F    Hodgkin disease         Cep, AG,
                                                               AMP
                      54 yr, W, M    Heart transplant
                      54 yr, W, M    Mental retardation      Cep, AMP
Smilack 1975 (7)      23 yr, B, F    Sickle cell trait,      AMP
                                       SLE
Hruby 1973 (27)        2.5 yr, B, F  SSA                     AMP, AG
Guckian 1967 (8)      52 yr, B, F    SLE                     Cep, AMP
Krag 1959 (29)        87 yr, W, F    DM, nursing home        PCN
                      63 yr, W, F    ATP, splenectomy
Fisher 1953 (16)       2 yr, B, M    Letterer-Siwe           Strept
Butt 1952 (28)         7 yr, B, F    SSA

                      Age, race,
Reference             sex            Rec  O  St

Current 2002          47 yr, B, F    N    S  VA
Nowinski 2000 (21)     7 mo, F       N    S  OH
Buck 1997 (22)         3 mo, M       N    S  UK
Sanyal 1997 (23)       5 yr, M       N    S
Kelly 1995 (24)        6 yr, H       N    S  AZ
Sharma 1993 (14)      69 yr, H, M    Y    S  TX
Cortes 1992 (13)      60 yr, H, M    Y    S  TX
Waterman 1990 (5)     H                      CA
                      H                      CA
                      H                      CA
                      H                      CA
Cone 1990 (4)         71 yr, H, F    N    S  CA
                      72 yr, H, M    N    S  CA
Caravalho 1990 (3)    55 yr, H, F    Y    S  TX
Woolf 1990 (12)       28 yr, F       N    D  CA
Babu 1990 (20)        25 yr, H, M    Y    S  IL
Casner 1990 (19)      30 yr, H, M    N    S  TX
Noskin 1990 (18)      57 yr, H, M    N    S  IL
Bhatt 1989 (2)        27 yr, H, F    Y    S  TX
Fleischman 1989 (11)  38 yr, H, M    N    S  CA
Jakobson 1989 (17)    49 yr, W, F    Y    S  CA
Riley 1988 (1)        19 yr, H, F    N    S  CA
                      25 yr, H, M    Y    S  CA
                      51 yr, H, M    N    S  CA
Croop 1984 (39)
Marzouk 1983 (10)     63 yr, H, M
Quismorio 1993 (6)    31 yr, H, M    N    D  CA
                      41 yr, A, M    Y    D  CA
                      48 yr, H, F    Y    D  CA
Fainstein 1982 (9)    66 yr, H, M    N    D  TX
McIntyre 1981 (32)    73 yr, H, M    N    S  AZ
Petru 1981 (31)       53 yr, M       N    S  CA
Ichord 1980 (25)       8 wk, W, F    N    S
Lindsay 1980 (30)     69 yr, F       N    D  CA
Ogden 1979 (26)        2 yr, B, M    N    S  H
                       1 yr, B, M    N    S  H
Keren 1976 (51)       53 yr, B, M    Y    S  MD
Johnson 1976 (15)     29 yr, H, F    N    D  CA
                      54 yr, W, M    N    D  CA
                      54 yr, W, M    N       CA
Smilack 1975 (7)      23 yr, B, F    Y    S  TX
Hruby 1973 (27)        2.5 yr, B, F  N    S  IL
Guckian 1967 (8)      52 yr, B, F    Y    S  TX
Krag 1959 (29)        87 yr, W, F         D  CA
                      63 yr, W, F
Fisher 1953 (16)       2 yr, B, M    N    D  VA
Butt 1952 (28)         7 yr, B, F    N    S  GA

"Race: A, Asian; B, black; H, Hispanic; W, white. Type of infection:
UTI, urinary tract infection. Exposure: capsules, powder, and meat
refers to rattlesnake preparations. Underlying conditions: AdenoCa,
adenocarcinoma; ATP, autoimmune thrombocytopenia purpura; DM, diabetes
mellitus; HTN, hypertension; RA, rheumatoid arthritis; SLE, systemic
lupus erythematosus; SSA, sickle cell anemia; UIP, usual interstitial
pneumonia; W. Macroglob, Waldenstrom macroglobulinemia. Antibiotics: AG,
aminoglycoside; AMP, ampicillin; AZ, aztreonam; Cep, cephalosporin; Chl,
chloramphenicol; PCN, penicillin; Q, fluoroquinolone; Sal,
sulfasalazine; Strept, streptomycin; SMX-TMP, sulfamethoxazole-
trimethoprim; TIC, ticarcillin; V, vancomycin, Recurrence (Rec): Y, yes;
N, no or not documented. Outcome (O): S, survived; D, died. State or
country (St): AZ, Arizona; CA, California; GA, Georgia; H, Republic of
Haiti; IL, Illinois; MD, Maryland; OH, Ohio; TX, Texas; UK, United
Kingdom; VA, Virginia.

Table 2. Exposures cited as source of Salmonella arizona infection

Pet chickens or hens (31)
Pet iguanas (21)
Pet snakes (22-23,39)
Pet turtles (25,38)
Rattlesnake meat (2,13,18,24)
Rattlesnake capsules (1,4,5,9-12,14,19,32,33)
Rattlesnake powder (3,20)
Unpasteurized milk (15,16,24,25,36)
Egg powder (37)
"Folk remedy" from Mexico (4)
Unknown (6-8,15,17,26-30,52)

Table 3. Underlying medical conditions of patients infected with
Salmonella arizona

Human immunodeficiency virus (2,13,17-19,23, current)
Neoplastic diseases
  Adenocarcinoma (10-12,14)
  Carcinoma (13)
  Melanoma (4)
  Leukemia (9)
  Letterer-Siwe disease (16)
Connective tissue diseases
  Rheumatoid arthritis (3-5)
  Systemic lupus erythematosus (1,2,6-8)
Dermatologic diseases
  Netherton syndrome (23)
Hematologic diseases
  Sickle cell anemia (7,26-28)
  Autoimmune thrombocytopenia purpura, splenectomy (29)
  Waldenstrom macroglobulinemia (6)
Posttransplant, on immunosuppressive medication
  Kidney transplant (6)
  Heart transplant (15)
Other conditions
  Usual interstitial pneumonia (31)
  Cardiac disease (CHF, dilated cardiomyopathy, atrial fibrillation) (1)
  Diabetes mellitus (29,32)
  Alcoholism, cirrhosis (30,52)
  Young age (< 7 yr) (16,21-28)

Table 4. Infection caused by Salmonella arizona and source of bacterial
culture (a)

Type of infection       Source of culture

Abscess, hematoma and   Tissue (5,6,29,32)
  aorta
Adenitis                Lymph node (1)
Bacteremia, septicemia  Blood (1,2,4,9-11,13,15-20,25,30,31,52, current)
Empyema, pleural        Pleural fluid (15)
  effusion
Endophthalmitis         Vitreous fluid (3)
Gastroenteritis         Stool (1,5,15,22-24,41, current)
Meningitis              Cerebrospinal fluid (25)
Osteomyelitis           Bone (7,16,26,27,29,39)
Otitis media            Ear drainage (28)
Pericarditis            Pericardial fluid (current)
Peritonitis             Peritoneal fluid (12,14,30)
Pneumonia               Sputum (5,15)
Septic arthritis        Synovial fluid (6,8,21,32)
UTI, pyelonephritis     Urine (5,8,32, current)

(a) UTI, urinary tract infection.