• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jcmPermissionsJournals.ASM.orgJournalJCM ArticleJournal InfoAuthorsReviewers
J Clin Microbiol. Jun 2007; 45(6): 1989–1992.
Published online Apr 18, 2007. doi:  10.1128/JCM.00632-07
PMCID: PMC1933083

Pantoea agglomerans, a Plant Pathogen Causing Human Disease[down-pointing small open triangle]

Abstract

We present 53 pediatric cases of Pantoea agglomerans infections cultured from normally sterile sites in patients seen at a children's hospital over 6 years. Isolates included 23 from the bloodstream, 14 from abscesses, 10 from joints/bones, 4 from the urinary tract, and 1 each from the peritoneum and the thorax. P. agglomerans was most associated with penetrating trauma by vegetative material and catheter-related bacteremia.

Pantoea agglomerans (formerly Enterobacter agglomerans) is a gram-negative aerobic bacillus in the family Enterobacteriaceae. All species of the genus Pantoea can be isolated from feculent material, plants, and soil (2), where they can be either pathogens or commensals (12). Within the genus, P. agglomerans is the most commonly isolated species in humans, resulting in soft tissue or bone/joint infections following penetrating trauma by vegetation (6, 7, 9, 14, 15). P. agglomerans bacteremia has also been described in association with the contamination of intravenous fluid (11), total parenteral nutrition (8), the anesthetic agent propofol (3), and blood products (1). However, spontaneously occurring bacteremia has rarely been reported, especially for children, and the role of P. agglomerans as a pathogen in other circumstances is unclear. Here, we present a large series of P. agglomerans infections in children that involve the bloodstream, soft tissue, and bones/joints.

This study reviewed all patients seen at Texas Children's Hospital, Houston, TX, with culture-documented P. agglomerans infections from January 2000 to December 2006. Patients were identified from hospital microbiology laboratory records. A retrospective review of medical records was performed for patients whose cultures were obtained from the following normally sterile sources: the bloodstream, catheter specimens from patients with urinary tract infections (UTIs) with ≥10,000 CFU/high-powered field, joint or body cavities, or incision sites and drainage of abscesses. Blood cultures were processed using the VITEK system of identification, and specimens that did not yield a result underwent DNA pyrosequencing. CLSI standards were used for disk diffusion testing (5). The study received institutional review board approval.

Overall, P. agglomerans was identified in 88 patient cultures from 53 sterile-site, 26 sputum, 3 urine, 3 surface swab, and 2 oropharyngeal sources. Of the 26 sputum cultures, only 1 grew P. agglomerans repeatedly, representing monomicrobic infection; more than one organism was isolated from all other sputum cultures, and the contribution of P. agglomerans was uncertain. Comorbid conditions in these patients included eight cases of cystic fibrosis, five cases of neurological impairment, five cases of tumor, and three cases of intestinal malabsorption.

For the 53 children whose sterile-site cultures grew P. agglomerans, sources included 21 central venous line (CVL)-related bacteremic episodes, 14 abscesses, 10 joint or bone cultures, 4 UTIs, 2 non-CVL-associated bacteremic episodes, 1 peritonitis episode, and 1 penetrating thoracic trauma. These sources are presented in Table Table11.

TABLE 1.
Patients with Pantoea agglomerans infection seen at Texas Children's Hospital from 2000 to 2006

Of the 21 patients with CVL infections, 8 had hematologic malignancies or bone marrow transplants, 7 had solid tumors, 3 had congenital heart disease, 1 had renal failure, 1 had necrotizing enterocolitis, and 1 had microvillus inclusion disease. One patient was neutropenic. Of the 21 patients, 14 had polymicrobial CVL infections necessitating line removal. Only 5/21 patients had two positive blood cultures; in all, bacteremia resolved within 48 h. Patients received 14 to 21 days of combination therapy with an aminoglycoside and either a broad-spectrum cephalosporin or ticarcillin-clavulanate. Three patients (two cardiac patients and one premature infant [cases 16, 17, and 19]) died of overwhelming sepsis shortly after P. agglomerans was isolated in their blood cultures; two of the three patients had polymicrobial infections. Two other patients had bacteremia without having a CVL. In both, bacteremia cleared after the first blood culture, and neither child had evidence of bone, joint, or soft tissue infection.

There were 14 children from whom P. agglomerans was isolated during the drainage of abscesses. All isolates were polymicrobial. Of these 14 children, 13 responded to antistaphylococcal therapy. A child with cerebral palsy underwent extensive debridement of a sacral decubitus ulcer and received a prolonged antibiotic course due to suspected chronic osteomyelitis.

The seven patients (cases 38 to 44) who had osteomyelitis presented with local symptoms 4 to 6 weeks after a penetrating trauma with a stick, plant thorn, or glass shard. None of the patients were febrile. Two of the patients were determined to have subperiosteal reactions and erosions by radiography and chronic inflammation by histopathology. The average white blood cell count was 6,900 cells/mm3 (range, 6,300 to 11,500 cells/mm3); blood cultures were negative.

An 8-year-old girl (case 46) developed septic arthritis 5 weeks after receiving a penetrating injury to the knee from a thorn. The patient's white blood cell count was 11,500 cells/mm3, her erythrocyte sedimentation rate was 16 mm/h, and her C-reactive protein level was 0.7 mg/ml. Arthrocentesis showed 17,600 white blood cells/mm3 (89% neutrophils, 11% monocytes) and 1,700 red blood cells/mm3. Gram staining and blood cultures were negative; a joint culture grew P. agglomerans. The child responded well to a 3-week course of therapy.

Antimicrobial susceptibilities were determined by Kirby-Bauer disk diffusion. All 53 isolates from sterile sites were uniformly susceptible to amikacin, gentamicin, meropenem, and trimethoprim-sulfamethoxazole. In addition, 92.5% of isolates were susceptible to broad-spectrum cephalosporins and semisynthetic penicillins, 62.3% to extended-spectrum cephalosporins, and 47.2% to ampicillin. Quinolone susceptibilities and MICs were not routinely determined for all specimens, given the association between quinolone use and arthropathy in juvenile-animal studies.

Of the 37 prior reports of P. agglomerans infections in children (Table (Table2),2), 5 were related to penetrating trauma and 30 (81%) to the contamination of parenteral fluids (8, 11). There is only one report of spontaneous P. agglomerans bacteremia: in a child with sepsis after rotavirus gastroenteritis (4). In that instance, it was postulated that the preceding gastrointestinal insult facilitated bacterial translocation across the gut mucosa.

TABLE 2.
Previously reported pediatric cases of Pantoea/Enterobacter agglomerans infection

In this series, 43% (23/53) of patients had bacteremia, and 91% of these infections were related to the presence of a CVL. There was neither clustering of cases temporally nor evidence of parenteral-fluid contamination. The true pathogenicity of this bacterium is difficult to discern due to the polymicrobial nature of most of the bacteremic infections, which had not been described previously. This necessitated prolonged, broad-spectrum antibiotic courses. P. agglomerans bacteremia appeared to be transient and did not recur during therapy, and antibiotic courses of 10 to 14 sterile days appeared to be curative. One limitation was that some of the less common Enterobacteriaceae species can be misidentified or susceptibilities incorrectly reported by automated methods (13). Confirmatory tests were not routinely performed for this pathogen unless the VITEK system did not provide an identification.

In conclusion, P. agglomerans is an uncommon cause of infection in children. It can cause bacteremia, often in association with more-conventional pathogens, in children with indwelling central access. However, antimicrobial susceptibility patterns mirror those of other gram-negative enteric pathogens. Diagnoses of bone/joint infections are often delayed due to both the indolent nature of the pathogen and the low level of clinical suspicion for this bacterium. Consequently, the diagnosis is often made when a child has evidence of chronic osteomyelitis, altering the treatment duration and prognosis. P. agglomerans should be suspected as the etiologic agent in cases of penetrating trauma by soil-encrusted objects or vegetation that remain refractory to conventional antimicrobial therapy.

Acknowledgments

We thank Edward O. Mason and Pam Zapalac for patient identification.

A. C. Cazacu's salary was supported by grant D43-TW01036 from the Fogarty International Center of the National Institutes of Health.

None of the authors reports a conflict of interest.

Footnotes

[down-pointing small open triangle]Published ahead of print on 18 April 2007.

REFERENCES

1. Alvarez, F. E., K. J. Rogge, J. Tarrand, and B. Lichtiger. 1995. Bacterial contamination of cellular blood components. A retrospective review at a large cancer center. Ann. Clin. Lab. Sci. 25:283-290. [PubMed]
2. Andersson, A. M., N. Weiss, F. Rainey, and M. S. Salkinoja-Salonen. 1999. Dust-borne bacteria in animal sheds, schools and children's day care centres. J. Appl. Microbiol. 86:622-634. [PubMed]
3. Bennett, S. N., M. M. McNeil, L. A. Bland, M. J. Arduino, M. E. Villarino, D. M. Perrotta, D. R. Burwen, S. F. Welbel, D. A. Pegues, and L. Stroud. 1995. Postoperative infections traced to contamination of an intravenous anesthetic, propofol. N. Engl. J. Med. 333:147-154. [PubMed]
4. Cicchetti, R., M. Iacobini, F. Midulla, P. Papoff, M. Mancuso, and C. Moretti. 2006. Pantoea agglomerans sepsis after rotavirus gastroenteritis. Pediatr. Infect. Dis. J. 25:280-281. [PubMed]
5. Clinical and Laboratory Standards Institute. 2000-2006. Performance standards for antimicrobial disk susceptibility testing, 10th to 16th informational supplements. Clinical and Laboratory Standards Institute, Wayne, PA.
6. De Champs, C., S. Le Seaux, J. J. Dubost, S. Boisgard, B. Sauvezie, and J. Sirot. 2000. Isolation of Pantoea agglomerans in two cases of septic monoarthritis after plant thorn and wood sliver injuries. J. Clin. Microbiol. 38:460-461. [PMC free article] [PubMed]
7. Flatauer, F. E., and M. A. Khan. 1978. Septic arthritis caused by Enterobacter agglomerans. Arch. Intern. Med. 138:788. [PubMed]
8. Habsah, H., M. Zeehaida, H. Van Rostenberghe, R. Noraida, W. I. Wan Pauzi, I. Fatimah, A. R. Rosliza, N. Y. Nik Sharimah, and H. Maimunah. 2005. An outbreak of Pantoea spp. in a neonatal intensive care unit secondary to contaminated parenteral nutrition. J. Hosp. Infect. 61:213-218. [PubMed]
9. Kratz, A., D. Greenberg, Y. Barki, E. Cohen, and M. Lifshitz. 2003. Pantoea agglomerans as a cause of septic arthritis after palm tree thorn injury; case report and literature review. Arch. Dis. Child. 88:542-544. [PMC free article] [PubMed]
10. Lau, K. K., B. H. Ault, and D. P. Jones. 2005. Polymicrobial peritonitis including Pantoea agglomerans from teething on a catheter. South. Med. J. 98:580-581. [PubMed]
11. Matsaniotis, N. S., V. P. Syriopoulou, M. C. Theodoridou, K. G. Tzanetou, and G. I. Mostrou. 1984. Enterobacter sepsis in infants and children due to contaminated intravenous fluids. Infect. Control 5:471-477. [PubMed]
12. Monier, J.-M., and S. E. Lindow. 2005. Aggregates of resident bacteria facilitate survival of immigrant bacteria on leaf surfaces. Microb. Ecol. 49:343-352. [PubMed]
13. Stone, N. D., C. M. O'Hara, P. P. Williams, J. E. McGowan, Jr., and F. C. Tenover. 2007. Comparison of disk diffusion, VITEK 2, and broth microdilution antimicrobial susceptibility test results for unusual species of Enterobacteriaceae. J. Clin. Microbiol. 45:340-346. [PMC free article] [PubMed]
14. Ulloa-Gutierrez, R., T. Moya, and M. L. Avila-Aguero. 2004. Pantoea agglomerans and thorn-associated suppurative arthritis. Pediatr. Infect. Dis. J. 23:690. [PubMed]
15. Vincent, K., and R. M. Szabo. 1988. Enterobacter agglomerans osteomyelitis of the hand from a rose thorn. A case report. Orthopedics 11:465-467. [PubMed]

Articles from Journal of Clinical Microbiology are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...