ORIGINAL ARTICLE BACTERIOLOGY

Osteomyelitis due to Salmonella enterica subsp. arizonae: the price of

exotic pets

S. Kolker1, T. Itsekzon1, A. M. Yinnon1,2 and T. Lachish2

1) Division of Internal Medicine, and 2) Infectious Disease Unit and Shaare Zedek Medical Centre, Affiliated with the Hebrew University Hadassah Medical
School, Jerusalem, Israel

Abstract

We describe a 31-year-old immunocompromised patient who developed sepsis and osteomyelitis due to Salmonella enterica subsp. arizo-
nae secondary to exposure to iguana and snakes kept as pets at her home, and review all 23 previously published cases of bone and
joint infections due to this organism, for a total of nine children and 15 adults. Eleven of the adults were female (73%), compared with
three (33%) of the children (p <0.01). Significant underlying illnesses were present in all 15 adults and in five children (55%, p <0.05); 10
(77%) of the adults were immunosuppressed, compared with one child only (17%) (p <0.05). In ten of the adults the knee was infected
(67%), compared with one child only (11%, p <0.01). Antibiotic therapy was prolonged in both adults and children, and in most cases
consisted of 4–6 weeks of parenteral treatment. Complete cure and survival was attained in 11 of 15 adults (73%) and all nine children
(NS). Optimal antibiotic treatment probably consists of ceftriaxone or a fluoroquinolone, if the organism is susceptible.

Keywords: Exotic animals, osteomyelitis, Salmonella, Salmonella enterica subsp. arizonae, zoonosis
Original Submission: 16 January 2011; Revised Submission: 9 March 2011; Accepted: 10 March 2011
Editor: G. Greub
Article published online: 4 April 2011
Clin Microbiol Infect 2012; 18: 167–170
10.1111/j.1469-0691.2011.03533.x
Corresponding author: A. M. Yinnon, Division of Internal
Medicine, Shaare Zedek Medical Centre, P.O. Box 3235,
Jerusalem 91031, Israel
E-mail: yinnon@szmc.org.il
Introduction
Infections due to Salmonella enterica subsp. arizonae are
uncommon in humans. Most described cases occurred in the
southwestern USA and, in particular, in immunocompro-
mised hosts [1,2]. These bacteria are usually transmitted to
man after direct or indirect contact with reptiles or con-
sumption of snake products. We report the first case of
infection due to this organism in Israel, in an immunocom-
promised woman with osteomyelitis of the tibia, and review
all 23 previously reported cases of ostearticular infections
due to this organism.
Patient Presentation
The patient was a 32-year-old married woman, who was
referred to the emergency room because of 40.5C fever and
extreme fatigue, which started 1 day before admission. Six
weeks earlier, she had started to complain of pain in her left
knee and proximal tibia. A computed tomography scan
revealed chronic sclerosis in the proximal left tibia and an
inflammatory reaction in the soft tissues of the left shin. A
magnetic resonance imaging scan suggested avascular necrosis
in the proximal femoral medial condyle, an extensive infarct
in the medulla of the proximal tibia with bony oedema and
oedema of the surrounding soft tissues. The patient was diag-
nosed with avascular necrosis and instructed to avoid weight
bearing on her left leg. The pain increased during the days
before her admission, and the knee became swollen.
The patient’s past medical history was significant for pem-
phigus vulgaris, which was diagnosed 1 year earlier based on
buccal lesions. For the last 10 months she had been on oral
corticosteroid treatment and mycophenolate mofetil (Cell-
cept). She had also received a course of intravenous gammo-
globulin. For the last several months her disease was in
complete remission.
The physical examination revealed lack of obvious distress.
The blood pressure was 100/69 mmHg, the pulse 125/min
and the temperature 39.5C; oxygen saturation was 94% at
room air. The left knee and pretibial area were swollen, red,

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Clinical Microbiology and Infection ª2011 European Society of Clinical Microbiology and Infectious Diseases
168 Clinical Microbiology and Infection, Volume 18 Number 2, February 2012
hot and painful, without evidence of intra-articular fluid. The
laboratory tests showed a white blood count of 11 000/lL
with 87% polymorphonuclear cells; haemoglobin was 9.9 g/dL
and platelets 84 9000/mm3; alkaline phosphatase was 203 IU/
mL, GGT 753 IU/mL, albumin 2.8 g/dL, erythrocyte sedimen-
tation rate 90 mm/h and fibrinogen 1023 mg/dL. The trans-
thoracic echocardiogram was normal. An abdominal
ultrasound revealed a fatty liver, but was otherwise normal,
while an ultrasound of the knee did not reveal fluid.
Blood cultures were obtained and showed no growth, and
the patient was started on penicillin, clindamycin and amika-
cin. Because of lack of response to treatment, and ongoing
severe pain at the left pretibial area, it was decided to obtain
a bone biopsy of the involved area. Under local anaesthesia,
the skin and tibia were opened, and 70 mL of pus were
drained from the bone. The area was debrided and a drain
was left in place. After the procedure, immediate improve-
ment of pain and fever were observed. A Gram stain from
the pus revealed Gram-negative bacilli, which subsequently
were identified as Salmonella enterica subsp. arizonae. This led
to further questioning of the patient, regarding exposure to
animals, and it appeared that the patient’s husband kept
iguana, snakes and other reptiles at their home, although the
patient herself denied direct physical contact with these
animals. In vitro susceptibility testing revealed that the organ-
ism was susceptible to all tested antimicrobials, including
ampicillin, amoxycyllin-clavulanate, piperacillin-tazobactam,
all cephalosporins, ciprofloxacin, gentamicin and trimetho-
prim-sulfamethoxazole. The patient received 7 weeks of
intravenous ceftriaxone 2 g once daily, followed by oral
ciprofloxacin 750 mg twice daily. However, after several
days, local findings of infection relapsed and she required
one further operation to debride the infected tibia and
received another 6 weeks of intravenous ceftriaxone. In view
of this history and the fact that the patient continued to
receive her usual immunosuppressive therapy, we continued
with oral ciprofloxacin 750 mg twice daily for a full year and
she recovered without residual sequelae. The mentioned
pets were duly removed from the family’s home. Four years
later the patient’s pemphigus vulgaris remains in complete
remission with low-dose steroids and mycophenolate mofetil,
without relapse of osteomyelitis.
Discussion
Salmonella enterica subsp. arizonae is a facultative anaerobic
Gram-negative bacillus of the family Enterobactericeae, which
has the ability to ferment lactulose and liquefy gelatin. The
bacteria was first isolated from reptiles in Arizona in 1939
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Clinical Microbiology and Infection ª2011 European Society of Clinical Microbiology and Infectious Diseases, CMI, 18, 167–170
CMI
and was called Salmonella dar-es-salaam [3], to be subse-
quently reclassified as Arizona hinshawii, Salmonella arizonae,
Salmonella cholerasuis subsp. arizonae and finally Salmonella
enterica subsp. arizonae [4]. Less than 60 human cases and
case series have been published, and virtually all involve
immunocompromised adults or young children [1,5]. There-
fore, isolation of this organism from apparently healthy adults
should prompt evaluation of their immune status. Infection
usually involves bacteraemia, which may lead to involvement
of any organ, including meningitis, pericarditis, gastroenteritis,
pneumonia, urinary tract infection, abscesses, and bone and
joint involvement. The majority of the reported cases origi-
nate from the southwestern United States, primarily Califor-
nia, Arizona and Texas. These states harbour large numbers
of people of Latino descent, some of whom use folk reme-
dies, in particular rattlesnake meat, capsules and powders.
Only two cases have been reported from Europe. However,
in Israel one study from 1970 reported on 156 cultures with
S. enterica subsp. arizonae, of which 66 were from humans,
most of whom were children with gastroenteritis, and the
remainder from snakes [6].
The patient described in this report received immunosup-
pressive therapy for pemphigus vulgaris; she developed acute
osteomyelitis of the tibia and isolation of Salmonella enterica
subsp. arizonae led to further questioning, which revealed the
presence of reptiles at the family’s residence. Our case report
represents the 24th published case of osteoarticular infection
with Salmonella enterica subsp. Arizonae; nine of these cases
involved children (Table 1) [2,7–13] and 15 involved adult
patients (Table 2) [11,14–20]. Eleven of the adults were
female (73%), compared with three (33%) children (p <0.01).
The mean (±SD) age in the adult patients was 45 ± 16 years
(range 23–73), and in the children 5.3 ± 5.8 years (range
7 months to 14 years). Significant underlying illnesses were
present in all 15 adults and in five children (55%) (p <0.05); 10
(77%) of the adults were immunosuppressed, compared with
one child only (17%) (p <0.05). In ten of the adults the knee
was infected (67%), compared with one child only (11%)
(p <0.01). Other sites, in addition to an infected bone or
joint, were involved in eight adults (53%), compared with four
of the children (44%) (NS). Antibiotic therapy was prolonged
in both adults and children, and in most cases consisted of 4–
6 weeks of parenteral treatment. Relapse occurred in six
adults (43%) and none of the children (NS). Complete cure
and survival was attained in 11 adults (73%) and all children
(NS). Optimal antibiotic treatment probably consists of ceftri-
axone or a fluoroquinolone, provided the organism is suscep-
tible in vitro. Azithromycin is an appropriate alternative for
non-typhoidal Salmonella enterica; [21] however, there are no
data regarding its efficacy for osteomyelitis in humans.
CMI Kolker et al. Osteomyelitis due to Salmonella enterica subsp. arizonae 169

TABLE 1. Children with bone and/or joint infection due to Salmonella enterica subsp. arizonae

Type of bone/joint Other sites Antibiotic Other

Ref Sex/age Co-morbidity IS? infection of infection course treatment Relapse Outcome

7 M/2 y Histiocytosis X NA Disseminated osteomyelitis Sepsis gastro-enteritis 7M Radio-therapy No Recovery

8 F/2.5 y Sickle cell anaemia NA Disseminated osteomyelitis Sepsis 6W No Recovery
9 M/1 y Sickle cell anaemia No Osteomyelitis No NA No Recovery
9 M/2 y Sickle cell anaemia No Osteomyelitis No NA No Recovery
10 M/11 y NA NA Osteomyelitis No NA No Recovery
11 F/14 y SLE Yes Bilateral knee osteoarthritis Sepsis NA No Recovery
12 F/7 m No No Proximal humerus No 10W No Recovery
13 M/14 y No No Ankle arthritis Gastro-enteritis NA NA NA
2 M/10 m No No Hip osteoarthritis No 8W Joint drainage No Recovery

Ref, reference, corresponds to the same number on the reference list; M, male; F, female; y, years; m, months; IS, immunosuppressed; NA, not available; SLE, systemic lupus;
W, weeks

TABLE 2. Adult patients with bone and/or joint infection due to Salmonella enterica subsp. arizonae

IS Type of bone/joint Other sites Anti biotic Other

Ref Sex/age Co-morbidity infection of infection course treatment Relapse Outcome

14 F/63 y ITP NA Knee osteoarthritis No NA Bone curettage NA Death

15 F/52 y SLE Yes Bilateral knee arthritis UTI gastro enteritis NA Joint drainage Yes, treated Recovery
DM II + peritibial abscess by 3 m Abx.
16 F/23 y SLE Yes Knee and shoulder arthritis No NA Yes Recovery
+ tibial abscess
17 M/53 y Ethylism No Vertebral osteomyelitis Gastro enteritis 3W Yes, 1 y Abx. Recovery
18 M/73 y DMII No Right ankle arthritis Septic aortic Lifelong Joint drainage + amput. No Recovery
aneurysm UTI
19 F/31 y SLE Yes Left knee arthritis No 6W No Death
19 M/41 y S/P RT, chronic HBV Yes Right knee arthritis Kidney abscess 4W Yes, 1 Death
week Abx.
19 F/48 y Waldenstrom No Left knee arthritis UTI sepsis 4W Repeat drainage Yes Death
macro-globulinemia gastro enteritis
20 F/71 y RA Yes Iliac abscess Gastro enteritis No Recovery
+ sacroiliac arthritis
11 M/27 y Dermato-myositis Yes Hip arthritis on THA No NA Repeat drainage No Recovery
11 F/34 y SLE Yes Knee arthritis No NA Joint drainage No Recovery
11 F/36 y SLE Yes Knee and shoulder arthritis No 6W Joint drainage No Recovery
11 F/29 y SLE Yes Shoulder and bilateral Sepsis 4W No Recovery
knee arthritis
11 F/61 y Primary biliary NA Vertebral osteomyelitis UTI NA No Recovery
cirrhosis
PP F/32 y Pemphigus Yes Proximal tibial abscess No 1y No Recovery

Abx, antibiotic treatment; Amput., amputation; Ref, reference; F, female; M, male; y, years; m, months; IS, immunosupressive therapy; NA, not available; SLE, systemic lupus
erythematosis; DMII, diabetes mellitus type 2; ITP, idiopathic thrombocytopenic purpura; UTI, urinary tract infection; HVB, hepatitis B virus; RA, rheumatoid arthritis; s/p RT,
status post-renal transplantation; PP, present patient.

The major source of Salmonella infection is food; how-
ever, an estimated 3–5% of all cases of salmonellosis in
humans are associated with exposure to exotic pets, indicat-
ing some 74 000 Salmonella infections annually in the US
alone [22,23]. Our case should serve as an important remin-
der of the risk animal exposure poses for immunocompro-
mised patients. The Center for Disease Control (CDC) has
published guidelines for the prevention of opportunistic
infections among haematopoietic stem cell transplant (HSCT)
recipients, with a special section dedicated to the prevention
of pet-transmitted zoonoses [24]. According to these guide-
lines, precautions include optimal maintenance of the pet’s
health and avoidance of contact with animal waste and litter
boxes. Certain animals may present specific risks, including
reptiles: as many as 90% of the latter may be carriers of Sal-
monella. Patients are therefore advised to avoid all contact
with reptiles and their surroundings. These guidelines were
intended specifically for HSCT recipients, because they are
most vulnerable, but other individuals, who are immunocom-
promised to varying degrees, are also at increased risk for
animal-transmitted infections. According to the CDC guide-
lines, there is no need to part with most pets, with the pos-
sible exception of reptiles, but it is important to understand
the risks and to avoid unnecessary exposure [25].
In conclusion, isolation of Salmonella enterica subsp. arizo-
nae should prompt inquiry regarding exposure to snakes or
other reptiles and, in adult patients without known immuno-
compromise, investigation regarding underlying morbidity.
People interested in keeping such animals as pets should be
educated regarding the involved risks as well as risk-reducing
behaviour according to the CDC recommendations.
Transparency Declaration
The authors have no dual or conflicting interests.

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Clinical Microbiology and Infection ª2011 European Society of Clinical Microbiology and Infectious Diseases, CMI, 18, 167–170
170 Clinical Microbiology and Infection, Volume 18 Number 2, February 2012
References
1. Hoag JB, Sessler CN. A comprehensive review of disseminated Salmo-
nella arizona infection with an illustrative case presentation. South
Med J 2005; 98: 1123–1129.
2. Schneider L, Ehlinger M, Stanchina C et al. Salmonella enterica subsp.
arizonae bone and joints sepsis. A case report and literature review.
Orthop Traumatol Surg Res 2009; 95: 237–242.
3. Caldwell ME, Ryerson DL. Salmonellosis in certain reptiles. J Infect
Dis 1939; 65: 242–245.
4. Tindall BL, Grimont PA, Garrity GM, Euzéby JP. Nomenclature and
taxonomy of the genus Salmonella. Int J Syst Evol Microbiol 2005; 55:
521–524.
5. Centers of disease control prevention (CDC). Reptile-associated sal-
monellosis – selected cases 1998–2002. MMWR 2003; 52: 1206–
1209.
6. Sechter I, Altmann G, Cahan D, Gerichter ChB. Arizona infections in
Israel (1957–1969). Ann Inst Pasteur 1970; 119: 323–328.
7. Fischer RH. Multiple lesions of bone in Letterer Sieve disease; report
of a case with culture of paracolon Arizona bacilli from bone lesions
and blood followed by response to therapy. J Bone Joint Surg 1953;
35: 445–465.
8. Hruby MA, Honig GR, Lolekha S, Gotoff SP. Arizona hinshawii: oste-
omyelitis in sickle cell anemia. Am J Dis Child 1973; 125: 867–868.
9. Ogden JA. Light TR. Pediatric osteomyelitis: II. Arizona hinshawii
osteomyelitis. Clin Orthop Relat Res 1979; 139: 110–113.
10. Croop JM, Shapiro B, Alpert G, Campos JM, Zavod W. Arizona hins-
hawii osteomyelitis associated with a pet snake. Pediatr Infect Dis
1984; 3: 188.
11. Kraus A, Guerra-Bautista G, Alarćon-Segovia D. Salmonella arizona
arthritis and septicemia associated with rattlesnake ingestion by
patients with connective tissue diseases. A dangerous complication of
folk medicin. J Rheumatol 1991; 18: 1328–1331.
12. Nowinski RJ, Albert MC. Salmonella osteomyelitis secondary to
iguana exposure. Clin Orthop Relat Res 2000; 372: 250–253.
ª2011 The Authors
Clinical Microbiology and Infection ª2011 European Society of Clinical Microbiology and Infectious Diseases, CMI, 18, 167–170
CMI
13. Foster N, Kerr K. The snake in the grass – Salmonella arizonae gas-
troenteritis in a reptile handler. Acta Pediatr 2005; 94: 1165–1166.
14. Krag D, Shean DB. Serious human infections due to bacillus of the
Arizona group. Calif Med 1959; 90: 230–233.
15. Guckian JC, Byers EH, Perry JE. Arizona infection of man. Arch Intern
Med 1967; 119: 170–175.
16. Smilack JD, Goldberg MA. Bone and joint infections with Arizona
hinshawii: report of a case and review of the literature. Am J Med Sci
1975; 270: 503–507.
17. Keren DF, Rawlings W, Murray HW, Leonard WR. Arizona hinshawii
osteomyelitis with antecedent enteric fever and sepsis. A case report
with review of the literature. Am J Med 1976; 60: 577–582.
18. McIntyre KE Jr, Malone JM, Richards E, Axline SG. Mycotic aortic
pseudoaneurysm with aortoenteric fistula caused by Arizona hinshawii.
Surgery 1982; 91: 173–177.
19. Quismorio FP Jr, Jakes JT, Zarnow AJ, Barber D, Kitridou RC. Septic
arthritis due to Arizona hinshawii. J Rheumatol 1983; 10: 147–150.
20. Cone LA, Boughton WH, Cone LA, Lehv LH. Rattlesnake capsule-
induced Salmonella arizonae bacteremia. West J Med 1990; 153: 315–
316.
21. Gunell M, Kotilainen P, Jalava J, Huovinen P, Siitonen A, Hakanen AJ.
In vitro activity of azithromycin against nontyphoidal Salmonella enteri-
ca. Antimicrob Agents Chemother 2010; 54: 3498–3501.
22. Woodward DL, Khakhria R, Johnson WM. Human salmonellosis
associated with exotic pets. J Clin Microbiol 1997; 35: 2786–2790.
23. Mermin J, Hutwagner L, Vugia D et al. Reptiles, amphibians and
human Salmonella infection: a population-based, case control study.
Clin Infect Dis 2004; 38 (suppl 3): S253–S261.
24. Centers of disease control and prevention (CDC). Guidelines for
preventing opportunistic infections among hematopoietic stem cell
transplant recipients, 1999. MMWR 2000; 49(No. RR-10):1–125.
25. Olsthain-Pops K, Yinnon AM. Pasteurella multocida sepsis – should
immunocompromised patients give up their pets? (Editorial). IMAJ
2008; 10: 648–649.
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