Gordonia bronchialis Bacteremia and Pleural Infection: Case Report and Review of the Literature

Abstract

Gordonia species are aerobic actinomycetes recently recognized as causing human disease, often in the setting of intravascular catheter-related infections. We describe a case of Gordonia bronchialis bacteremia and pleural space infection in the absence of an indwelling intravascular catheter and review the breadth of reported infections with this emerging pathogen.

CASE REPORT

A 52-year-old woman with a history of Hodgkin's lymphoma, prior splenectomy, and breast cancer was experiencing recurrent pleural effusions over several months prior to admission and presented with bloody drainage from an indwelling pleural catheter. The patient had been diagnosed with Hodgkin's lymphoma 35 years earlier and was treated with radiation therapy to the neck, chest, and abdomen at that time. She underwent a splenectomy for a splenic artery aneurysm 14 years prior to presentation. Five years prior to presentation, she had cardiac surgery for radiation-induced valvular disease, with placement of a St. Jude's mechanical prosthetic valve at the aortic position and repair of mitral and tricuspid valves with biological prosthetic material; a cardiac pacemaker for a heart block was placed. Four years prior to presentation, she had undergone bilateral mastectomies for breast cancer and was subsequently treated with tamoxifen and then anastrozole. Six months prior to presentation, she developed bilateral pleural effusions. The pleural fluid sampled on two occasions was consistent with exudative effusions, with slight lymphocyte predominance and negative Gram stains and cultures, including mycobacterial culture; cytology for malignant cells was negative. Based on these studies, the etiology of the pleural disease was unclear but was thought to be a late complication of her radiation therapy 35 years previously. Bilateral indwelling pleural catheters were placed, and the left-sided catheter was later removed when drainage ceased. In the weeks prior to the most recent presentation, the patient initiated systemic anticoagulation therapy for atrial fibrillation. She subsequently developed bloody drainage from the remaining right-sided indwelling pleural catheter, at which time she was admitted for further evaluation. She did not experience fever, chills, night sweats, cough, or other new symptoms.

At the time of admission, the patient was afebrile. Blood cultures were drawn, and empirical therapy with vancomycin and ceftazidime was initiated. Anticoagulation therapy was discontinued. She subsequently developed rapid respiratory deterioration. On the fourth hospital day, video-assisted thorascopic surgery (VATS) was performed for drainage of a right-sided loculated pleural effusion, decortication, and placement of a right-sided chest tube (Fig. 1). She subsequently improved clinically, remaining afebrile on empirical antibacterial therapy. However, after 4 days of incubation, the aerobic blood culture bottle drawn on the day of admission grew Gram-positive rods, which also stained weakly acid fast (Fig. 2). All further blood cultures after initiation of antibiotics were without growth.

Fig. 1.

Chest computed tomography at the time of admission (A) and after surgical drainage and decortication of the right-sided bloody effusion (B).

Fig. 2.

Modified acid-fast staining of the pathogen from blood cultures at the time of admission.

The organism was preliminarily identified as an aerobic actinomycete, possibly a Nocardia sp. or Rhodococcus sp. based on observed morphology, and was referred to the Anaerobe Research Laboratory for further characterization by long-chain fatty acid analysis using the MIDI system (Microbial Identification Systems, Newark, DE) and the clinical identification library, which includes long-chain fatty acid profile data for Gordonia species. Antibacterial therapy was changed from vancomycin and ceftazidime to intravenous trimethoprim-sulfamethoxazole and imipenem-cilastatin. Transthoracic and transesophageal echocardiography demonstrated no vegetations or other abnormalities of the cardiac valves, including the mechanical prosthetic aortic valve or the pacemaker. The patient was subsequently transitioned to oral trimethoprim-sulfamethoxazole therapy at a dose equivalent to 12 mg/kg body weight/day and discharged to a rehabilitation facility, with final identification of the pathogen still pending.

Primary pleuropulmonary infection was suspected as the underlying cause of the bacteremia, so further laboratory studies of both the blood isolate and the available pleural specimens were performed. Pleural tissue biopsied at the time of placement of the indwelling pleural catheter 3 months prior to this presentation was examined with tissue Gram and acid-fast staining, and no organisms were identified. Pleural tissue from the surgical drainage of the right-sided bloody pleural effusion on the fourth hospital day of this presentation later grew Gram-positive rods in culture. Both the blood isolate and the pleural isolate were sent to the Actinomycete Reference Laboratory of the Centers for Disease Control and Prevention (CDC), where both isolates were identified as Gordonia bronchialis by 16S rRNA gene (1,495-bp) sequencing analysis (16). Both patient isolates were 100% similar to G. bronchialis type strain ATCC 25592. Using established procedures (22), with gyrB gene (approximately 1,245-bp) sequencing, both patient isolates were 100% similar to each other and 93% related to the type strain of G. bronchialis. There were no differences between the two patient isolates in the utilization of carbohydrates and hydrolysis of various substrates, using methods previously described (6). Antimicrobial drug susceptibility patterns and breakpoints, as determined by the use of published NCCLS standards (5), of G. bronchialis at the CDC laboratory revealed that the organism had intermediate resistance to clarithromycin but was susceptible to all other antibiotics tested: amoxicillin-clavulanate, amikacin, ceftriaxone, ciprofloxacin, linezolid, minocycline, trimethoprim-sulfamethoxazole, tigecycline, and vancomycin. The patient was subsequently transitioned to oral ciprofloxacin and minocycline therapy based on the low MIC results observed from susceptibility testing. She completed a 3-month course of antibiotic therapy and has recovered.

The Gordonia (previously Gordona) genus was first differentiated from other aerobic actinomycetes in 1971 (24). Microbiologic diagnosis of Gordonia species is difficult, often resulting in incorrect identification as other actinomycetes or mycobacteria, as initially occurred in this case. However, increasing use of 16S rRNA sequencing has significantly improved organism identification. In recent years, there have been reports of a variety of infections due to several of the Gordonia spp., such that Gordonia spp. now comprise a significant minority of the aerobic actinomycetes isolated in human diseases. A study in Thailand found that of 171 aerobic actinomycete isolates sent to the National Institutes of Health for identification between 1996 and 2003, approximately 56% were Nocardia spp., 12% Mycobacteria spp., 11% Streptomyces spp., 8% Rhodococcus spp., 6% Gordonia spp., 0.6% Tsukamurella spp., and 0.6% Corynebacterium spp. (18). Since the Gordonia genus was named, there have been 29 different species identified. Several types of infections caused by these Gordonia spp. have been described in the literature, including sternal wound infections (20), ventriculitis with an underlying ventricular shunt (2), otitis externa (10), bronchitis (10), skin and soft tissue infections (1, 13), arthritis associated with a biological absorbable bone/joint screw (11), recurrent breast abscess (26), granulomatous mastitis following nipple piercing (27), keratitis/conjunctivitis (12), endocarditis related to an underlying central venous catheter (15, 25), and bacteremia (both catheter related and without an indwelling catheter) (4, 23).

Gordonia bronchialis, the species isolated in this case, is the type species of Gordonia, first identified from samples of soil and sputum obtained from patients with pulmonary disease (cavitary tuberculosis and bronchiectasis) (24). In our review of the literature, we identified 11 other reported cases of G. bronchialis infections in humans (Table 1), 7 of which were sternal surgical site infections during an outbreak in a single hospital, which was traced to an operating room nurse (20). Of the remaining four cases, one was a case of ventriculitis related to a ventricular shunt infection in a neonate, one was a case of recurrent breast abscess, and two were cases of bacteremia (2, 26). Of the two cases of bacteremia, neither was thought to be due to an indwelling central venous catheter (CVC), which is unusual for Gordonia bacteremia. One case of bacteremia occurred in a patient with nonketotic hyperosmolar coma due to diabetes, and the bacteremia was of unclear significance (3). The other was similar to the case presented here in that the patient had underlying chronic pleuropulmonary disease with a sequestrated lung and developed bacteremia without a current indwelling CVC (23). In that case, the patient was treated with surgical drainage of abscesses, intravenous vancomycin, and ceftriaxone for more than 2 months, followed by oral amoxicillin-clavulanate for 6 weeks, and made a full recovery.

Table 1.

Summary of clinical reports of infections with Gordonia bronchialis

Type(s) of infection	No. of cases	Patient age(s)	Underlying condition(s)	Yr of publication (reference)
Bacteremia and pleural infection	1	52 yr	Lymphoma, splenectomy, breast cancer, and pleural effusions	2011 (this case report)
Bacteremia	1	67 yr	Diabetes and nonketotic hyperosmolar coma	2009 (3)
Intraventricular shunt	1	45 days	Premature neonate	2007 (2)
Recurrent breast abscess	1	43 yr	Pituitary adenoma	2005 (26)
Bacteremia	1	58 yr	Sequestrated lung and diabetes	2004 (23)
Sternal wound (hospital outbreak traced to operating room nurse)	7	51–68 yr	Surgery	1991 (20)

Gordonia bronchialis is the identified species in only a minority of human infections due to Gordonia spp. and rarely a cause of bacteremia. In our review of the literature, we identified 30 other reported cases of Gordonia bloodstream infections, with only 2 of these due to G. bronchialis (Table 2). Of the 30 cases of bacteremia, 22 were related to indwelling central venous catheters (CVCs), most were due to Gordonia sputi or Gordonia terrae, and most occurred in patients with an underlying malignancy or other immunocompromised states.

Table 2.

Reported bloodstream infections with Gordonia species

Gordonia species	Type(s) of infection	No. of cases	Patient age (yr)	Underlying condition(s)a	Yr of publication (reference)
G. bronchialis	Bacteremia and pleural infection	1	52	Lymphoma, splenectomy, breast cancer, and pleural effusions	2011 (this case report)
G. polyisoprenivorans	Bacteremia due to CVC and pneumonia	1	17	Leukemia	2010 (9, 14)
G. sputi	Bacteremia due to CVC	3	43	SLE and pulmonary hypertension	2009 (19)
			46	HIV, hepatitis C, pulmonary hypertension
			78	Mesenteric ischemia and TPN
	Bacteremia and a likely contaminant	1	60	Pneumonia and pleural effusion
G. bronchialis	Bacteremia	1	67	Diabetes and nonketotic hyperosmolar coma	2009 (3)
G. terrae	Bacteremia due to CVC	1	58	Leukemia	2009 (13)
	Bacteremia	2	23	Leukemia and BMT	2009 (13)
			75	COPD and atrial fibrillation
G. sputi	Bacteremia due to CVC	1	14	Short bowel syndrome and TPN	2009 (13)
	Bacteremia	1	49	Gastric cancer and diabetes	2009 (13)
	Bacteremia due to CVC	1	69	Laryngeal cancer	2009 (13)
G. terrae	Bacteremia due to CVC	1	24	Sepsis, abuse of methandienone, dyspnea	2007 (8)
	Bacteremia due to CVC	3	3	Wilms' tumor	2007 (2)
			3	Leukemia
			5	LACH syndrome and hypogammaglobulinemia
G. otitidis	Bacteremia due to CVC	1	11	Periodic fever syndrome and bowel necrosis	2007 (2)
G. polyisoprenivorans	Catheter-related bacteremia and native valve endocarditis	1	78	Osler-Weber-Rendu and myelodysplastic syndromes	2006 (25)
G. terrae	Bacteremia and acute cholecystitis	1	61	Hepatitis C	2006 (7)
G. bronchialis	Bacteremia	1	58	Sequestrated lung and diabetes	2004 (23)
G. polyisoprenivorans	Bacteremia due to CVC	1	26	Leukemia and BMT	2004 (12)
G. terrae	Bacteremia due to CVC	5	28	Leukemia and splenectomy	2003 (17)
			44	Brain tumor
			54	Leukemia
			46	Unknown primary cancer, metastatic to liver
			60	Thyroid cancer with metastasis
Gordonia sp. most closely resembling G. sputi	Catheter-related bacteremia and native valve endocarditis	1	31	Splenectomy, hemoglobinopathy, and cirrhosis	2000 (15)
G. sputi	Bacteremia due to cutaneous lesions	1	34	Metastatic melanoma and IL-2 treatment	1996 (21)
G. terrae	Bacteremia due to CVC	1	43	Chronic intestinal pseudo-obstruction syndrome and TPN	1992 (4)
Unidentified Gordonia sp.	Bacteremia due to CVC	1	65	Breast and ovarian cancer and TPN	1992 (4)

^aAbbreviations: CVC, central venous catheter; SLE, systemic lupus erythematosus; HIV, human immunodeficiency virus; TPN, total parenteral nutrition; BMT, bone marrow transplant; COPD, chronic obstructive pulmonary disease; LACH, leukoencephalopathy, arthritis, colitis, and hypogammaglobulinemia; IL-2, interleukin-2.

Our case represents a rare instance of Gordonia bacteremia in the absence of a current indwelling intravascular catheter. In our case, the source of the bacteremia may have been a primary pleuropulmonary infection, although inoculation via intravascular catheters during prior hospital admissions cannot be excluded. A pleuropulmonary infection may have been chronic and the original cause of the patient's pleural effusions, which developed 6 months prior to her presentation with bacteremia. The patient had reported gardening regularly during the preceding summer in the weeks and months prior to the development of her pleural effusions, indicating possible soil inhalation exposure to G. bronchialis. Alternatively, it is possible that the G. bronchialis infection was a recent infection related to the indwelling pleural catheter. Our patient's history of hematologic malignancy, radiation therapy, and splenectomy may have predisposed her to this rare infection.

There are no standardized recommendations for treatment of infections due to Gordonia spp. Available data suggest that Gordonia spp., in contrast to some other actinomycetes, such as Rhodococcus spp., are generally susceptible to many antimicrobial drugs. Susceptibility testing at reference laboratories has been useful to guide the choice of antibiotic therapy in the reported cases of human infection with Gordonia spp. In the previous reported cases of Gordonia bacteremia, numerous different antibiotics were used, either alone or in a variety of combinations, including vancomycin (often in combination with an expanded-spectrum cephalosporin or carbapenem or with rifampin in some pediatric patients), linezolid, amoxicillin or amoxicillin-clavulanate (often as a subsequent oral treatment after completion of intravenous therapy), trimethoprim-sulfamethoxazole, ceftriaxone, ceftazidime, piperacillin-tazobactam, ticarcillin-clavulanate, imipenem-cilastatin, meropenem, ciprofloxacin, levofloxacin, amikacin or gentamicin (in combination with a cephalosporin or carbapenem), azithromycin, and clindamycin. The duration of treatment also varied from case to case, with many patients completing between 6 and 12 weeks of antibiotic therapy. For catheter-associated Gordonia infections, catheter removal is recommended for infections in children, but there are no formal guidelines for management of catheters in adults. In the majority of the cases described above, the catheters were removed as a part of treatment of the Gordonia infection. The prognosis for Gordonia bloodstream infections is variable, depending on the underlying conditions of the host, the clinical factors related to the infection, and the time to diagnosis.

Nucleotide sequence accession numbers.

The 16S rRNA gene sequences from G. bronchialis X0216 (81-10) and X0217 (82-10) were deposited in GenBank under accession numbers HQ316181 and HQ316182, respectively. The gyrB gene sequences of X0216 (81-10) and X0217 (82-10) were deposited in GenBank under accession numbers HM352642 and HM352643, respectively.