Pantoea agglomerans bacteraemia after uterine artery embolisation: an unusual pathogen

Abstract

A woman in her 40s presented to the emergency department (ED) with a 3-week history of nausea, vomiting and diarrhoea. Blood cultures were positive for Serratia and Pantoea agglomerans spp. One month before her ED visit, she underwent targeted uterine artery embolisation with particles by an interventional radiologist. Uterine artery embolisation is considered a safe alternative to surgical removal of fibroids or hysterectomy. The patient was initially treated with targeted antibiotics for a large infected uterine fibroid but ultimately required a hysterectomy for source control. To our knowledge, this is the first documented case of P. agglomerans infecting a uterine fibroid.

Background

Pantoea agglomerans is a gram-negative plant-based bacterium that rarely infects humans. Most documented cases have been reported in workers encountering plant material or contaminated medical equipment such as catheters or intravenous fluids in hospitals. P. agglomerans is an opportunistic pathogen manifesting in individuals with weakened immune systems, such as patients with diabetes, AIDS, cancer, lupus or organ transplant. Infection with this bacterium can present in several ways, including respiratory, urinary tract, soft tissue and bloodstream infections. Although P. agglomerans is not a typical human pathogen, medical providers should know its ability to infect immunocompromised patients.

Case presentation

A woman in her 40s who underwent targeted uterine artery embolisation (UAE) with particles for fibroid reduction 1 month earlier presented to the emergency department (ED) with a 3-week history of nausea, vomiting and diarrhoea. While in the ED, laboratory work showed a white cell count of 11.5×10⁹/L, haemoglobin of 96 g/L and mildly elevated alkaline phosphatase at 139 IU/L. At this time, she was taking a course of amoxicillin–clavulanate for acute sinusitis. After administration of crystalloids and antiemetics, she reported improvement of her symptoms and was discharged. When the blood cultures obtained during the ED visit returned positive for gram-negative bacteraemia, she was admitted and started on piperacillin and tazobactam.

Investigations

On hospital day 2, the leucocytosis worsened (white cell count of 16.9×10⁹/L), and blood culture microbiology revealed Serratia spp (specific species could not be identified) and two morphologically different strains of P. agglomerans growth in the blood. Both strains of P. agglomerans were pan-susceptible to antibiotic treatment (table 1). Susceptibility testing of the Serratia spp was not performed. CT of the abdomen and pelvis (figure 1) demonstrated multiple uterine fibroids, with the largest one showing heterogeneous attenuation with air locules. While the appearance of air locules can persist following interventional radiology (IR) embolisation, their presence at 1-month follow-up was suspicious for a superinfected degenerating fibroid, especially in the setting of bacteraemia. Adjacent smaller fibroids had features of degeneration and necrosis but no air locules consistent with targeted embolisation. The patient initially declined a hysterectomy; however, after worsening of symptoms for 3 days, she agreed to proceed with surgery.

Table 1.

Antibiotic susceptibility report of Pantoea agglomerans spp identified on blood culture

Antibiotic	P. agglomerans (1) Susceptibility, MIC (µg/mL)	P. agglomerans (2) Susceptibility, MIC (µg/mL)
Ampicillin	≤8 µg/mL susceptible	≤8 µg/mL susceptible
Ampicillin+sulbactam	4/2 µg/mL susceptible	4/2 µg/mL susceptible
Aztreonam	≤4 µg/mL susceptible	≤4 µg/mL susceptible
Cefazolin	≤2 µg/mL susceptible	≤2 µg/mL susceptible
Cefepime	≤2 µg/mL susceptible	≤2 µg/mL susceptible
Ceftazidime	≤1 µg/mL susceptible	≤1 µg/mL susceptible
Ceftriaxone	≤1 µg/mL susceptible	≤1 µg/mL susceptible
Cefuroxime- sodium	≤4 µg/mL susceptible	≤4 µg/mL susceptible
Ertapenem	≤0.5 µg/mL susceptible	≤0.5 µg/mL susceptible
Gentamicin	≤1 µg/mL susceptible	≤1 µg/mL susceptible
Levofloxacin	≤0.25 µg/mL susceptible	≤0.25 µg/mL susceptible
Pipercillin+tazobactam	≤4 µg/mL susceptible	≤4 µg/mL susceptible
Tetracycline	≤4 µg/mL susceptible	≤4 µg/mL susceptible
Tigecycline	≤2 µg/mL susceptible	≤2 µg/mL susceptible
Tobramycin	≤1 µg/mL susceptible	≤1 µg/mL susceptible
Trimethoprim+ sulfamethaxazole	≤2/38 µg/mL susceptible	≤2/38 µg/mL susceptible

MIC, minimal inhibitory concentration.

Figure 1.

CT of the abdomen and pelvis axial and coronal views demonstrating a large uterine fibroid with air locules (circled in yellow). Largest fibroid is an intramural lesion in the fundus measuring 13.6×10.5 cm.

On day 3 of admission, she had a robotic-assisted hysterectomy, bilateral salpingectomy and a mini-laparotomy (figure 2). After detachment of the uterus, morcellation showed fibroid necrosis and a large amount of pus inside the uterine cavity. The specimen cultures were also positive for P. agglomerans. Repeat susceptibility testing was not performed on the uterine culture as it was the same species identified on blood culture. Histology of the uterus demonstrated a myometrium with multiple leiomyomas (0.7–12 cm) with variable infarction and intravascular embolic material within and adjacent to leiomyomas. After further investigation, known risk factors for Pantoea infection, such as intravenous drug use or handling feculent material, plants or soil, was not part of her medical history. IR fibroid embolisation with particles was performed at an outside hospital and the content of the particles was not able to be identified.

Figure 2.

Gross histology of uterus post-hysterectomy. Myometrium contained multiple leiomyomas (0.7–12.0 cm). Infected fibroid circled in yellow.

Differential diagnosis

Initial differential diagnosis included gastroenteritis and antibiotic side effects as the patient was on amoxicillin–clavulanate for sinusitis. She was initially discharged with symptomatic management consisting of antiemetics and oral hydration. However, once the patient’s blood cultures resulted positive, she was admitted for systemic treatment. This initiated a search for the source of her bacteraemia, which resulted in finding uterine fibroids with air locules on CT imaging suggesting infection. Uterine specimen culture matching blood culture species after hysterectomy further validated the source of infection.

Treatment

The patient was initially treated with intravenous piperacillin and tazobactam for gram-negative bacteraemia. The source of her bacteraemia and sepsis was identified as likely infected uterine fibroids on CT imaging. After clinical worsening, she underwent a robotic-assisted hysterectomy, bilateral salpingectomy and a mini-laparotomy for source control of her infection.

Outcome and follow-up

The patient recovered from surgery without complications. Her blood cultures remained negative at 72 hours after surgery, and she was discharged on a 14-day course of oral ciprofloxacin. At 2-year follow-up, she has returned to working full-time and is doing well.

Discussion

Uterine fibroids are the most prevalent benign tumours of women of reproductive age, varying from 5% to 70%, depending on age, race, age at menarche and family history.^{1 2} Despite their benign nature, they may tremendously impact life with symptoms such as dysmenorrhoea, heavy menstruation, dyspareunia and sometimes impaired fertility.³ Treatment is based on the severity of symptoms and ranges from medical to interventional and surgical.^{4 5} Embolisation involves injecting small pro-embolic particles such as polyvinyl alcohol into the associated artery supplying the targeted fibroid.⁶ UAE has emerged as a safe and effective modality with risks ranging from fever and allergic reactions to life-threatening infections.3 4 7 8

Infectious complications of UAE are rare. The most extensive study to date consisted of 414 UAE procedures and revealed no specific risk factor for infection, with only five patients (1.2%) experiencing severe complications.⁹ Although UAE is considered a low-risk procedure, close surveillance is recommended due to the morbidity associated with a uterine infection.

P. agglomerans in humans is an opportunistic organism that may infect via exogenous, nosocomial and endogenous mechanisms.¹⁰ Exogenous infection is the most common route, occurring via the deposition of infectious materials into an already open wound or piercing of the skin, as predominantly seen in gardeners, children and agricultural workers.¹⁰ A retrospective study by Vaiman et al identified P. agglomerans infection in nine patients with a history of traumatic injury, and further investigation revealed foreign plant material in all nine of them, giving evidence to its origin.¹¹ Nosocomial infection is the second most common pathway and is caused by contamination on medical equipment, staff or pharmaceuticals. There have been a few instances of nosocomial outbreaks of P. agglomerans, the most significant of which was in 1970, with 152 cases of septicaemia with a 13% mortality; the cause was found as factory contamination of intravenous fluids.¹² The least common pathway is the endogenous or sporadic mode of infection, seen in those with already underlying subclinical P. agglomerans infection aggravated by a procedure or weakened immune system.¹³

The clinical manifestations of P. agglomerans infection range from asymptomatic to life-threatening. The infection presents predominantly as septic arthritis, synovitis, endophthalmitis, dacryocystitis, endocarditis and osteomyelitis.¹⁰ Effective treatments include ampicillin–sulbactam, piperacillin–tazobactam and third-generation cephalosporins. The route of infection was unclear in our patient; however, procedure-related infection was suspected as no other risk factors were present. The facility where the patient underwent UAE was contacted to encourage investigation of possible contamination during this procedure. This is the first case in literature in which P. agglomerans was isolated in an infected fibroid.

Learning points.

• While uterine artery embolisation is a low-risk procedure, educating the patient on potential complications, such as a hysterectomy, is essential.

• Pantoea agglomerans is a common pathogen that infects animals and plants. However, it is an opportunistic pathogen that can infect individuals with weakened immune systems.

• In a patient who presents with signs of systemic illness post-uterine artery embolisation for uterine fibroid management, one should consider the possibility of fibroid infection.

Ethics statements

Patient consent for publication

Consent obtained directly from patient(s).