# Bacteremia and adrenal gland abscess due to Nocardia cyriacigeorgica: a case report and review

Florian Saunier, Sylvain Grange, Josselin Rigaill, Marie-France Lutz, Amandine Gagneux-Brunon, Elisabeth Botelho-Nevers

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Florian Saunier, Sylvain Grange, Josselin Rigaill, Marie-France Lutz, Amandine Gagneux-Brunon, et al. Bacteremia and adrenal gland abscess due to Nocardia cyriacigeorgica: a case report and review. BMC Infectious Diseases, 2022, 22 (1), pp.966. 10.1186/s12879-022-07839-9. hal-04819914

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# Bacteremia and adrenal gland abscess due to *Nocardia cyriacigeorgica*: a case report and review

Florian Saunier<fnref n="1" />, Sylvain Grange², Josselin Rigaill³, Marie-France Lutz<fnref n="1" />, Amandine Gagneux-Brunon<fnref n="1" /> and Elisabeth Botelho-Nevers<fnref n="1" />*

### Abstract

**Background:** *Nocardia cyriacigeorgica* is one of the most common *Nocardia* species found in human infections, recently reclassified. Even though *Nocardia* may affect all organs by hematogenous dissemination, bacteremia are uncommon. Among all possible dissemination sites, the involvement of the adrenal glands is particularly rare.

**Case presentation:** We report here a rare case of *Nocardia* disseminated infection with notably bacteremia and adrenal gland abscess, in a 77-years-old immunocompetent man. Adrenal gland abscess diagnosis was made by imaging (computerized tomography, magnetic resonance and positron emission tomography scan). A complete regression of all lesions including the left adrenal gland was obtained after 6 months of antibiotics. A review of literature was also performed.

**Conclusion:** *Nocardia* bacteremia is a rare event but blood cultures may help to improve detection of *Nocardia* spp. in a non-invasive way. Adrenal abscess due to *Nocardia* spp. is very rare with only fourteen cases reported in the literature, but it is a true cause of adrenal masses. Our report suggests that clinician should be aware of this rare location and prioritize a non-invasive diagnosis strategy.

**Keywords:** *Nocardia cyriacigeorgica*, Nocardiosis, Adrenal gland abscess, Bacteremia

### Background

*Nocardia* is a genus of aerobic actinomycetes and belongs to the family of *Nocardiaceae* [1]. Bacteria are gram positive, branching, filamentous, and mildly acid-alcohol-fast [1, 2]. *Nocardia* species are ubiquitous, saprophytic and usual component of the soil, water and organic matter [1, 2]. Human infections arise mostly by inhalation and sometimes by skin inoculation [1, 2]. Currently, 123 *Nocardia* species are described according to the List of Prokaryotic names with Standing in Nomenclature

(http://www.bacterio.net), and at least 50 are clinically significant [3]. Thanks to molecular methods (heat shock protein (hsp65) gene, 16 S rRNA gene sequencing), a significant taxonomic changes and species reassignment within the genus were made, particularly among members of the former *N. asteroides* complex [3]. *Nocardia asteroides* drug pattern type VI is now known as *Nocardia cyriacigeorgica* [3]. Thus, it might be difficult for clinicians to understand all the recent changes of *Nocardia* taxonomy.

Nocardiosis may be localized or disseminated and occur predominantly in immunocompromised hosts [1]. The most common infection sites are the lungs, the central nervous system and the skin and soft tissues. All organs may potentially be affected by hematogenous dissemination but *Nocardia* spp. bacteremia are uncommon

<footnote>*Correspondence: elisabeth.botelho-nevers@chu-st-etienne.fr</footnote>

<footnote n="1">¹ Infectious Disease Department, University Hospital of Saint Etienne,
42055 Saint-Étienne, France
Full list of author information is available at the end of the article</footnote>
[1, 4, 5] and the involvement of the adrenal glands is par-
ticularly rare with only a few cases reported in the liter-
ature [6]. We report here a rare case of bacteremia and
adrenal gland abscess due to N. cyriacigeorgica. This case
is an opportunity to raise awareness of clinicians about
the recent change of Nocardia taxonomy, and to review
the frequency of bacteremic infection as well as adrenal
gland abscesses during Nocardiosis.

Case presentation

A 77-year-old man with no medical history presented for several months a deterioration of his general status with depressive syndrome. In November 2017, he was admitted to the emergency room for respiratory distress. Physical exam revealed the absence of fever, irregular cardiac rate and oxygen saturation at 95% with 9 L of oxygen. Electrocardiogram showed atrial fibrillation. Chest X-ray revealed interstitial syndrome of pulmonary bases. Laboratory investigations revealed leukocytes count 20.4 G/L with 18.60 G/L neutrophils, C-reactive protein 447 mg/L and serum creatinine level 314 µmol/L. He was treated as a severe pneumonia by intravenous levofloxacin (500 mg/12 h) and ceftriaxone (2 g/24 h). The blood pressure fell and the patient was transferred to an intensive care unit where he was intubated because of severe refractory hypoxemia despite high oxygen flow.

A chest CT-scan (computerized tomography) was
performed and revealed a diffuse bilateral interstitial
syndrome. Five set of blood cultures grew Nocardia cyr-
iacigeorgica in aerobic bottles after respectively 67, 71, 81,
82 and 85 h (blood culture system BD BACTEC FX (Bec-
ton Dickinson®), identification was done using matrix-
assisted laser desorption-ionization—time of flight mass
spectrometry system (MALDI-TOF MS, Microflex LT,
Bruker). Antibiotic susceptibility was determined using
agar diffusion assay and ETEST® technique (bioMérieux),
following the CLSI guidelines (https://clsi.org/). The iso-
late was susceptible to imipenem, cefotaxime, amikacin,
clarithromycin, linezolid, doxycycline, and trimethoprim-
sulfamethoxazole (TMP-SMX). It was non-susceptible
to amoxicillin, ciprofloxacin and amoxicillin-clavulanic
acid (intermediate). A diagnosis of disseminated Nocar-
diosis was subsequently made and antibiotic regimen was
changed to linezolid (600 mg/12 h), cefotaxime (2 g/4 h)
and amikacin (1.5 g/24 h). As the patient continued to
work in the construction industry, we supposed that the
source of Nocardiosis was probably by inhalation.

A cerebral CT-scan was performed and revealed bilat-
eral lesions with circumferential contrast enhancement
and edema. The biggest lesion (13 mm) was in the right
occipital lobe. A chest, abdomen and pelvis (C.A.P) CT-
scan showed a left adrenal poly-lobed nodular hyper-
trophy of 57 × 33 × 62 mm (Fig. 1). A Positron Emission

Tomography scanner was also made, showing hyper-
metabolic left adrenal lesion (standardized uptake value
(SUV) max=14), pulmonary hypermetabolism in bilat-
eral postero-basal regions and pleural effusions (SUV
max=4.3), and no other suspect lesion. An abdominal
magnetic resonance imaging (MRI) was performed to
help distinguishing the nature of this adrenal hypertro-
phy (Fig. 1). The lesion was clearly in favor of a left adre-
nal abscess because of the MRI characteristic and the size
regression of the lesion under antimicrobial treatment.
Transthoracic and trans-esophageal echocardiography
showed no sign of endocarditis. HIV serology was nega-
tive but a CD4+T lymphopenia (402 cell/µL or 38%) was
observed. Serum protein electrophoresis revealed a nor-
mal rate of gamma globulin (10 g/L) with no monoclonal
spike. The patient was not diabetic.

Gradually, the patient's clinical condition improved
and two weeks after admission, he was transferred to the
infectious disease department. Antibiotic treatment was
changed to TMP-SMX (4.8 g/960 mg/24 h) and cefotax-
ime (12 g/24 h for one week and then 9 g/24 h). Nine-
teen days after beginning these antibiotics, the patient
developed skin rash, justifying stopping TMP-SMX and
replacing it by clarithromycin (1.5 g/24 h). Six weeks
after the beginning of the antibiotic treatment (Decem-
ber 16th, 2017), the patient has recovered, cefotaxime
was replaced by ceftriaxone (4 g/24 h) and he returned
home. After three months of antibiotic treatment (Febru-
ary 5th, 2018), ceftriaxone was changed to doxycycline
(200 mg/24 h) but still combined with clarithromycin
(1.5 g/24 h). A C.A.P and brain CT scan were performed
after six months of treatment (April 23th, 2018) and
showed a complete regression of all lesions including the
left adrenal gland with restitution *ad integrum* and anti-
biotics were discontinued (Fig. 1).

Discussion and conclusion

We report here a rare case of *Nocardia cyriacigeorgica*
disseminated infection in a non-immunocompromised
man with notably a bacteremia and an adrenal gland
abscess. The species involved in this case was not a new
species as firstly suspected by Yassin et al. [7], nor an
emerging pathogen, but in fact, *N. cyriacigeorgica* and
*N. asteroides* drug pattern type VI belong to the same
species [8]. It is no longer appropriate to mention the
*Nocardia asteroides* complex and its six «drug pattern
type» whom now are six different taxa: *N. abscessus* (drug
pattern I), *N. brevicatena* / *N. paucivorans* (drug pattern
II), *N. nova* complex (drug pattern III), *N. transvalensis*
complex (drug pattern IV), *N. farcinica* (drug pattern V)
and *N. cyriacigeorgica* (drug pattern VI) [3]. Thus, the
main *Nocardia* species isolated in the majority of human
infections are part of the former *N. asteroides* complex :
<figure><img src="image_3.png" /><figcaption>**Fig. 1** Abdominal CT and MR scan. Abdominal CT scan [1] in axial view, initial (1A) and 6 months after starting antibiotic treatment (1B). The large left adrenal abscess (white arrow) is accompanied by inflammation of the surrounding fat (blue arrow). Note the normalization of the left adrenal gland (red arrow) and the disappearance of the inflammation of the surrounding fat. MR images [2] acquired during the antibiotic treatment. The T2 with fat saturation images (2A) shows a hypersignal in the anterior part of the left adrenal gland (orange arrow). On the enhanced T1 sequence (2B), this image is not enhanced (white arrow) corresponding to the central part of the abscess (necrosis), while the rest of the adrenal gland is normally enhanced (purple arrow). The hypersignal in diffusion sequence (3C, green arrow), especially with a very low ADC (apparent diffusion coefficient) (3D), here less than 0.5·10⁻⁶mm² s⁻¹ (yellow arrow), leading to the diagnosis of abscess</figcaption></figure>

*N. farcinica*, *N. abscessus*, *N. cyriacigeorgica*, and *N. nova* [4, 9, 10] including cases reported prior to the availability of molecular tests [3, 8]. In our case, *N. cyriacigeorgica* was identified by MALDI-TOF MS. Although progress is still needed for the identification of uncommon species, MALDI-TOF MS is a valuable aid for more accurate and

rapid identification of *Nocardia* species [3]. This easier identification probably helps physicians to be more familiar to the complexity of *Nocardia* taxonomy [3].

Even though *Nocardia* species can grow in a variety of blood culture media, bacteremia during Nocardiosis is rarely reported [5]. We reviewed large series of *Nocardia*
<table><caption>**Table 1** Cases of Nocardia spp. adrenal abscesses reported in literature (NR: not reported)</caption><thead><tr><th>References</th><th>Years</th><th>Patients characteristics</th><th>Symptoms</th><th>Disseminated Nocardiosis</th><th>Adrenal abscess side/ Nocardia species</th><th>Treatment</th><th>Outcome</th></tr></thead><tbody><tr><td>Kim et al. [25]</td><td>1991</td><td>Male, 38 years, AIDS</td><td>Left upper quadrant abdominal pain, fever, chills</td><td>Paraaortic and mesenteric lymphadenopathy</td><td>Left/N. asteroides</td><td>Cefoxitin<br>Surgical drainage of the mass</td><td>Died</td></tr><tr><td>Arabi et al. [23]</td><td>1996</td><td>Male, 39 years, AIDS</td><td>Epigastric pain, fever, vomiting</td><td>Brain, bacteremia</td><td>Bilateral/N. asteroides</td><td>Cefotetan, gentamicin, doxycycline then TMP-SMX, imipenem, amikacin, and ciprofloxacin</td><td>Survived</td></tr><tr><td>Midiri et al. [26]</td><td>1998</td><td>Female, 49 years, rheumatoid arthritis treated by corticosteroid therapy</td><td>Fever and left flank plain</td><td>Lung, spleen</td><td>Left/N. asteroides</td><td>TMP-SMX<br>Left adrenalectomy</td><td>Survived</td></tr><tr><td>Moiton et al. [11]</td><td>2002</td><td>Male, 69 years, active cancer, steroids</td><td>Pneumoniae, aphasia, motor deficit</td><td>Lung, brain, bacteremia</td><td>NR/N. farcinica</td><td>Ceftriaxone, TMP-SMX</td><td>Died</td></tr><tr><td>Chong et al. [27]</td><td>2004</td><td>Male, 34 years, AIDS</td><td>Fever, left loin pain, hematuria</td><td>No other location</td><td>Left/N. asteroides</td><td>Laparoscopic drainage</td><td>Survived</td></tr><tr><td>Elsayed et al. [19]</td><td>2005</td><td>Female, 69 years, type 2 diabetes mellitus, chronic lymphocytic leukemia, hypogammaglobulinemia</td><td>Malaise, right-sided flank and pleuritic chest discomfort, left leg weakness, ataxic gait</td><td>Lung, brain, bacteremia</td><td>Right/N. cyriacigeorgica</td><td>Meropenem, TMP-SMX</td><td>Survived (mild to moderate speech impairment, generalized weakness)</td></tr><tr><td>Haussaire et al. [10]</td><td>2008</td><td>Male, 35 years, kidney transplant, immunosuppressor treatment (calcineurin inhibitor, antimetabolite, steroids)</td><td>NR</td><td>Lung, kidney, pancreas, adrenal glands, bacteremia</td><td>NR/N. farcinica</td><td>TMP-SMX, carbapenem, amikacin</td><td>Survived (hypoacusis)</td></tr><tr><td>Tachezy et al. [28]</td><td>2009</td><td>Female, 71 years, former alcohol addiction, malnutrition</td><td>Fever, non-productive cough, adynamia</td><td>Lung, inferior vena cava, right hepatic and renal capsule, diaphragm, brain</td><td>Right/N. farcinica</td><td>Impenem, amikacin, TMP-SMX then TMP-SMX alone<br>Right adrenalectomy with resection of IVC diaphragm, retroperitoneum and Gerota's fascia</td><td>Survived</td></tr><tr><td>Al-Tawfiq and Al-Khatti [29]</td><td>2010</td><td>Female, 66 years, psoriasis treated by TNF-alpha therapy, type 2 diabetes</td><td>Fever, chills, profuse sweating, left upper quadrant abdominal pain</td><td>Left renal vein, spleen, retroperitoneal and mesenteric lymphadenopathies</td><td>Bilateral/N. farcinica</td><td>Vancomycin, meropenem then TMP-SMX, linezolid<br>Aspiration and biopsy of the left adrenal lesion</td><td>Died</td></tr><tr><td>de Montmollin et al. [24]</td><td>2012</td><td>Female, 59 years, chronic parenteral nutrition, malnutrition, hemodialysis</td><td>Fever, right lumbar region pain</td><td>Bacteremia</td><td>Right/N. farcinica</td><td>Amikacin, cefuroxime then TMP-SMX<br>Echography-guided aspiration and drainage</td><td>Died</td></tr><tr><td>Jackson et al. [6]</td><td>2017</td><td>Male, 69 years</td><td>Fever, night sweats, left upper quadrant abdominal pain</td><td>Lung, central nervous system, bone marrow, left renal vein, bacteremia, urine</td><td>Left/N. farcinica</td><td>Meropenem, TMP-SMX</td><td>Survived</td></tr></tbody></table>
<table><caption>**Table 1 (continued)**</caption><thead><tr><th>References</th><th>Years</th><th>Patients characteristics</th><th>Symptoms</th><th>Disseminated Nocardiosis</th><th>Adrenal abscess side/ Nocardia species</th><th>Treatment</th><th>Outcome</th></tr></thead><tbody><tr><td>Jackson and Shorman [20]</td><td>2018</td><td>Male, 39 years, splenectomy, intravenous drug user</td><td>Fever, generalized weakness, abdominal pain, orthostatic symptoms</td><td>Heart, bacteremia</td><td>Bilateral/N. farcinica</td><td>Meropenem, TMP-SMX<br>Bilateral percutaneous drains in the adrenal glands</td><td>Survived (at 4 weeks of treatment, then lost to follow-up)</td></tr><tr><td>Langmaid et al. [21]</td><td>2020</td><td>Male, 35 years, immunocompetent</td><td>Fever, dry cough and left-sided abdominal pain</td><td>Lung</td><td>Left/N. cyriacigeorgica</td><td>Meropenem, TMP-SMX<br>then ceftriaxone and TMP-SMX</td><td>Survived</td></tr><tr><td>Pender et al. [22]</td><td>2022</td><td>Male, 57 years, poorly controlled type 2 diabetes mellitus</td><td>Left upper quadrant abdominal pain, subjective fevers, diaphoresis, tachycardia, anorexia, nausea, weight loss</td><td>Lung</td><td>Left/N. beijingensis</td><td>Left adrenalectomy<br>TMP-SMX, linezolid<br>Left adrenalectomy</td><td>Survived</td></tr><tr><td>This case</td><td>2017</td><td>Male, 77 years, no predisposing factors</td><td>Deterioration of general status, depressive syndrome, respiratory distress</td><td>Lung, brain, bacteremia</td><td>Left/N. cyriacigeorgica</td><td>Cefotaxime, TMP-SMX<br>then cefotaxime, clarithromycin then doxycycline and clarithromycin</td><td>Survived</td></tr></tbody></table>
infection published [10–17] and found that bacteremia frequency range from 3.7 to 26.5% with a mean value of 10,1%. The study reporting the higher rate of bacteremia (26.5%) included mainly immunocompromised patients with 50% of disseminated forms [10]. Blood cultures seem then useful in the diagnosis of Nocardiosis. In the review of Kontoyiannis et al. [5], the isolation of *Nocardia* in blood culture preceded the isolation from other sites in 44% (8/18) of cases and blood cultures were the only source of diagnostic material in one-fourth of the cases (9/36). Thus, detection of *N. cyriacigeorgica* in blood cultures allowed a quick diagnosis and accurate treatment that probably improved the prognosis of our patient.

Low bacteremia frequency during *Nocardia* could be explained by a too short incubation time of blood cultures, a co-infection with more resilient organisms (as Gram-negative bacteria), an infrequent and intermittent bacteremia or an empiric treatment with good activity against *Nocardia* [5, 18]. Nowadays, usual blood culture media allows the detection of *Nocardia* spp., although specific media increase detection of *Nocardia* spp. such as biphasic brain-heart infusion or Castañeda media. In our case, the bacteremia was detected using BD BAC-TEC FX (Becton Dickinson®). The growth of bacteria on usual blood culture probably increases the diagnosis of bacteremia in this infection. To increase awareness about *Nocardia* infections in microbiology laboratories and to improve the yield of cultures for *Nocardia*, it may be advisable to increase duration of incubation and perform subcultures on to blood agar from the broth [5, 18].

Hematogenous dissemination of Nocardiosis can affect all organs, but some are rarely involved such as the adrenal glands. Only fourteen cases of *Nocardia* adrenal abscesses are reported in the literature. Adrenal abscesses are caused by *N. farcinica* (7/14), *N. asteroides* (4/14) and *N. beijingensis* (1/14) (see Table 1) [6, 10, 11, 19–22]. *N. cyriacigeorgica* is involved in only two cases [19, 21]. Adrenal masses are benign or malignant tumours most of the time but infectious causes (abscesses) must also be considered [6]. Disseminated Nocardiosis with adrenal abscesses can masquerading as malignant disease and commonly leading to an invasive strategy (puncture, laparoscopic drainage, adrenalectomy) to make a diagnosis and can lead to injury (see Table 1) [6, 10, 11, 19–22]. In our case, the presence of bacteremia, the use of medical imaging and biology and the evolution under treatment (lesion with progressive regression and restitution ad integrum after 6 months of antibiotic regimen) helped us to confirm infectious nature of the adrenal mass. Among the cases of *Nocardia* adrenal abscess [6, 10, 11, 19–22], seven were associated with bacteremia (7/14 i.e. 50%) [6, 10, 11, 19, 20, 23, 24] and only one did not underwent an invasive procedure for diagnosis [23]. Furthermore, in a

recent similar case, the patient underwent adrenalectomy and blood cultures taken 3 days prior to surgery grew *N. cyriacigeorgica* [21]. When we face an adrenal tumour with associated lesions (lung, brain etc.), it is therefore important to take time and promote non-invasive strategies such as medical imaging and biology (blood cultures particularly) to make a diagnosis. Moreover, even if some authors suggested that draining abscess collection is crucial to a successful outcome [5], in our case, a strategy with antibiotic regimen only was successful.

In conclusion, the *Nocardia* spp. taxonomy underwent many changes in recent years and despite complexity, knowledge of most common species is needed. *Nocardia* bacteremia is a rare event but blood cultures may help to improve detection of *Nocardia* spp. in a non-invasive way. Despite *Nocardia* spp. adrenal abscess being very rare with only fourteen cases reported, it is a true cause of adrenal masses. Our report suggests that clinician should be aware of this rare location and prioritize a non-invasive strategy.

**Abbreviations**

Hsp65: Heat shock protein; rRNA: Ribosomal ribonucleic acid; CT: Computerized tomography; MALDI-TOF MS: Matrix-assisted laserdesorption-ionization-time of flight mass spectrometry; TMP-SMX: Trimethoprim-sulfamethoxazole; C.A.P: Chest, abdomen and pelvis; SUV: Standardized uptake value; MRI: Magnetic resonance imaging; HIV: Human immunodeficiency virus.

**Acknowledgements**

The authors warmly thank the patient for agreeing to submit his case.

**Author contributions**

FS collected the data, performed the literature review and wrote the manuscript. SG provided and analyzed imaging. MFL took care of the patient. JR performed the bacterial isolation and identification. EBN and AGB supervised the process of drafting the manuscript and revised all versions. All authors read and approved the final manuscript.

**Funding**

This research received no external funding.

**Availability of data and materials**

Not applicable.

**Declarations**

**Ethics approval and consent to participate**

Not applicable.

**Consent for publication**

Written informed consent was obtained from the patient for publication of this case report.

**Competing interests**

The authors declare that they have no competing interests.

**Author details**

¹Infectious Disease Department, University Hospital of Saint Etienne, 42055 Saint-Étienne, France. ²Department of Radiology, University Hospital of Saint Etienne, 42055 Saint-Étienne, France. ³Laboratory of Infectious Agents and Hygiene, University Hospital of Saint-Étienne, 42055 Saint-Étienne, France.
Received: 10 August 2021 Accepted: 3 November 2022

Published online: 29 December 2022

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