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Case Report
14 (
3
); 343-347
doi:
10.1055/s-0042-1744236

Granulicatella adiacens as an Unusual Cause of Empyema: A Case Report and Review of Literature

, , ,
1Department of Microbiology, All India Institute of Medical Sciences, Bhubaneswar, India
2Department of Microbiology and Infection Control, Vikash Multispeciality Hospital, Bargarh, Odisha, India
3Department of Pulmonary Medicine, All India Institute of Medical Sciences, Bhubaneswar, India

Address for correspondence: Ashoka Mahapatra, MD, Microbiology, Department of Microbiology, All India Institute of Medical Sciences, Bhubaneswar, 751019, India (e-mail: micro_ashoka@aiimsbhubaneswar.edu.in; meetasoka@yahoo.co.in).

Copyright: © 2022. The Indian Association of Laboratory Physicians. All rights reserved.
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Abstract

Granulicatella adiacens, a nutritionally variant Streptococcus (NVS), is part of the normal commensal flora of human mouth, genital, and intestinal tracts and rarely causes disease. It has been mostly reported from bacteremia and endocarditis cases, but rarely can cause vertebral osteomyelitis, pancreatic abscess, otitis media, and endovascular, central nervous system, ocular, oral, bone and joint, and genitourinary infections. Due to requirement of fastidious culture conditions and non-specific colony morphology, serious diagnostic difficulties may arise in cases of NVS infections. Here, we are reporting a rare fatal infection of G. adiacens presented with empyema complicated to sepsis and necrotizing fasciitis.

Clinicians should be aware of the pathogenic potential of Granulicatella adiacens (a normal commensal flora of human mouth, genital and intestinal tracts). Appropriate supplemented media and a reliable detection system should be used to identify these fastidious organisms. We present this rare case to bring awareness among clinicians regarding such a rare but potentially fatal infection.

Keywords

empyema
Granulicatella adiacens
nutritionally variant Streptococcus
sepsis

Introduction

Granulicatella adiacens is a nutritionally variant Streptococcus (NVS). Pyridoxine or other additional agents supplementation into standard media is required for its laboratory isolation.[1] Taxonomically, these bacteria were transferred from Streptococcus to a separate genus Abiotrophia[2] and later, on the basis of 16S rRNA gene sequencing this genus was divided into the genera Abiotrophia and Granulicatella (species Granulicatella adiacens, G. elegans, and G. balaenopterae).[3]

Granulicatella is part of the normal commensal flora of human mouth, genital and intestinal tracts and rarely causes disease. Granulicatella adiacens has been mostly reported to cause bacteremia and endocarditis, but rarely can cause vertebral osteomyelitis, pancreatic abscess, otitis media and endovascular, central nervous system, ocular, oral, bone and joint and genitourinary infections.[4]

Infections due to nutritionally variant Streptococcus may have a high mortality rate because of difficulties in robust and reliable diagnosis and therapeutic failures. In a recent survey, mortality rate in nutritionally variant Streptococcus infections was found to be 9.0%.[5] For treatment of Abiotrophia and Granulicatella endocarditis and other serious infections, penicillin or ceftriaxone is the drug of choice as per the American Heart Association (AHA) guidelines.[6] Through this article, we present a review and our experience of a rare case of empyema caused due to G. adiacens complicated to sepsis and necrotizing fasciitis and ultimately death.

Materials and Methods

Case History

A 68-year-old male patient presented with left side chest pain and pain in lower limbs to the emergency department. On examination, the body temperature was 38.5°C, blood pressure 78/50 mm Hg, and pulse rate was 93/min. On chest examination, heart sounds were normal but respiratory rate was 28/min, vesicular breath sound and crepitations were present in the left chest. He was a known case of type 2 diabetes mellitus, hypertension and osteoarthritis of knee joints. He was alcoholic. Chest X-ray showed left-sided encysted pleural effusion. The patient was diagnosed with left-sided empyema with ruptured baker's cyst and septic shock. On ultrasound-guided aspiration, thick pus was aspirated and sent for biochemical analysis, bacteriological culture and sensitivity, Ziehl–Neelsen stain and CBNAAT (Cartridge-based nucleic acid amplification test). Simultaneously, one set of blood (BACT/ALERT FA Plus and BACT/ALERT FN Plus) and urine samples were sent for bacteriological culture. The patient was diagnosed as a case of left-sided empyema with septic shock and transferred to the ICU for management. Intercostal chest tube was placed and fluid was drained. The patient was managed with intravenous saline infusion and empirical antibiotic (inj. cefuroxime) was started. Laboratory findings showed an increased total leukocyte count (18,580/mm3), absolute neutrophil count (17,290 mm3), increased C-reactive protein (CRP 11.2 mg/dL), and hemoglobin level was 11.2 g/dL. Fasting blood sugar was 201 g/dL and serum uric acid was 8.9 mg/dL. Kidney function test was also deranged with serum urea level 102 mg/dL and creatinine 1.2 mg/dL. Pleural pus grew minute colonies on sheep blood agar after 48 hours, which were gram-positive cocci in small chains, catalase-negative, and subsequently identified as Granulicatella adiacens using the VITEK2 system (bioMérieux, France) using Gram positive (GP) identification card with 98% probability index. Antimicrobial susceptibility was performed using the E-test method (HiMedia, Mumbai, India) and MICs in µg were reported according to the EUCAST Clinical Breakpoints.[7] The isolate was sensitive to benzylpenicillin (MIC: 0.002 μgm/ml), ampicillin (0.016 μgm/ml), ampicillin sulbactam (0.016 μgm/ml), ceftriaxone (0.002 μgm/ml), teicoplanin (0.016 μgm/ml), vancomycin (0.016 μgm/ml) and linezolid (0.5 μgm/ml) and resistant to gentamicin (MIC >16 μgm/ml) and cotrimoxazole (MIC > 40 μgm/ml). After 5 days of incubation, blood culture also grew same organism with same sensitivity pattern. Urine culture was sterile. There was no significant improvement from the first presentation, except reduced drain fluid from intercostal site. As per the culture report, the empirical antibiotic was changed to inj. ceftriaxone and inj. linezolid. On the fifth day of targeted therapy, pleural pus was still there although minimal, and was sent for bacterial culture was sterile. But on the seventh day of hospitalization, the patient developed right lower limb necrotizing fasciitis with myonecrosis. Fasciotomy was done and it revealed necrotic muscles of lower leg posterior compartment with hematoma in the intra-muscular compartment. Unfortunately, the patient passed away on twelfth day of hospitalization due to acute myocardial infarction.

Discussion

We did the literature search over past 10 years (2011–2020) using search engines PubMed using the MeSH term, “Granulicatella adiacens.” Case reports with only monomicrobial infection due to G. adiacens were included in the review. All articles published in English were included in this analysis.

We reviewed 77 literatures on the subject (G. adiacens) over the past 10 years (2011–2020). Using the inclusion and exclusion criteria, 24 literature were found relevant and included in the review.[8-31] Clinical details of all published literature are compiled in the ►Table 1. As per the review of literature of last 10 years, G. adiacens is found to be the cause of various infections such as bacteremia, endocarditis, osteomyelitis, septic arthritis, discitis, prosthetic joint infections, carbuncle, bacterascites (spontaneous bacterial peritonitis), dacryocystitis, and abscess. Out of these, 13 isolated from blood (4 bacteremia, 8 endocarditis, 1 septic arthritis), 10 from synovial fluid/pus (6 prosthetic joint infection, 2 osteomyelitis, 2 discitis), one each from dacryocystitis, bacterascites, and carbuncle. Further extending search in PubMed using MeSH terms such as “empyema” and “Granulicatella” found only one case report of empyema (pleural pus) caused by Granulicatella elegans.[32] None of them were from empyema pus and blood simultaneously except our present report of G. adiacens. All cases were reported from abroad, except three from India: one from New Delhi (suprapatellar abscess), one from Odisha (carbuncle), and the present study from Bhubaneswar, Odisha (empyema pus and blood). To the best of our knowledge, the present study is the first case report of thoracic empyema caused by G. adiacens complicated to necrotizing fasciitis and sepsis.

Table 1 Clinicoepidemiological details of infections caused by Granulicatella adiacens
Infections caused by Granulicatella adiacens Year Geographical location Age/sex Clinical diagnosis Clinical samples References
Bacteremia 2011 Charlottesville, Virginia 89 y/F Multiple trauma victim with bacteremia Blood 8
2011 New Haven, Connecticut, USA 1 d/Mch Early onset neonatal sepsis Blood 9
2013 Rome, Italy 7 y/F Shone syndrome (coarctation of aorta, mitral stenosis and subvalvular aortic stenosis) with Bacteremia Blood 10
5 y/M Infundibular pulmonary stenosis with Bacteremia. Blood
Endocarditis 2013 San Diego, CA, U.S.A. 50 y/M Bivalvular (mitral and aortic valves) endocarditis Blood 11
2013 Kerala, India 63 y/M Infective endocarditis Blood 12
2015 Australia 57 y/M Subacute Bacterial endocarditis with type II mixed cryoglobulinemia Blood 13
2016 Tokyo, Japan 67 y/F Infective endocarditis with Sjogren's syndrome with oral complications Blood 14
2019 Columbia, USA 44 y/F Endocarditis, osteomyelitis, brain abscess Blood 15
2019 Switzerland 32 y/F Cardiac implantable electronic device related infection and bioprosthesis endocarditis Blood 16
2019 U.S.A. 82 y/M Bilateral lower extremity purpuric rash and complete heart block secondary to infective endocarditis Blood 17
2020 Farmington CT, United States 46 y/M Infective endocarditis and glomerulonephritis Blood 18
Prosthetic joint infection 2013 Paris, France 55 y/M Prosthetic joint infection (knee) after dental treatment Knee fluid aspirate 19
2016 Peterborough, Cambridgeshire, PE3 9GZ, UK 81 y/M Prosthetic joint infection (hip) Pus aspirate from hip 20
2017 Marseille, France 75 y/M Prosthetic joint infection (hip) Synovial fluid 21
65 y/M Prosthetic joint infection (knee) Synovial fluid
44 y/F Prosthetic joint infection (hip) Surgical biopsy sample
2017 Eau Claire, WI, USA 64 y/M Prosthetic joint infection (knee) Synovial fluid 22
Osteomyelitis 2016 Swedish Neuroscience Institute 46 y/M Vertebral osteomyelitis Vertebral body biopsy tissue 23
2018 Kitakyushu, Japan. 10 y/F Mandibular osteomyelitis Bone marrow fluid 24
Septic arthritis 2019 Iowa City, Iowa 5 y/M Ruptured appendicitis and retrocecal abscess presenting as atraumatic knee pain Blood 25
Discitis 2013 Tokyo, Japan 48 y/F Pyogenic discitis Blood and disk biopsy sample 26
2020 Rome, Italy 51 y/M Spondylodiscitis (L1-L2 and L5-S1 discs) disk biopsy sample 27
Dacryocystitis 2015 Morgantown, WV 26505, USA 46 y/F Dacryocystitis Purulent material from lacrimal sac 28
Bacterascites 2015 Charlottesville, VA 22908, USA 50 y/M Large distended abdomen (ascites) Ascitic fluid 29
Abscess 2018 New Delhi, India 30 y/M Suprapatellar abscess Aspirated pus from Knee joint swelling 30
18 y/M Elbow abscess Pus swab
Carbuncle 2012 Odisha, India 56 y/M Carbuncle, multiple discharging sinus over right scapular region Pus 31
Empyema 2016 South Africa 30 y/F Empyema underlying TB and HIV Caused by Granulicatella elegans Pleural pus 32
Empyema 2020 Odisha, India 68 y/M Empyema underlying diabetes mellitus and alcoholism Pleural pus and Blood Present study

Necrotizing fasciitis is a destructive and rapidly progressive soft tissue infection with significant morbidity and mortality. It may necessitate surgical intervention and may progress to systemic involvement, septic shock, and multiorgan failure without intervention. Although the exact cause of necrotizing fasciitis in the present case is not clear, as clinical sample could not be sent for microbiological investigations. But association with G. adiacens infection cannot be ruled out as there is one published report of cervical necrotizing fasciitis due to polymicrobial cause including G. adiacens following dental extraction and its surgical management.[33]

Due to requirement of fastidious culture conditions and non-specific colony morphology, serious diagnostic difficulties may arise in cases of NVS infections. Commercial blood culture media contain pyridoxal and support the growth of NVS. However, in the present case, the bacteria isolated from pleural pus and blood samples grew on commercial 5% sheep blood agar (without any additional supplement) as cited in other reports.[31]

With evolvement of the newer advanced laboratory systems, that is, the MALDI-TOF (VITEK MS, Bruker MS) system and the VITEK 2 system, NVS can be identified up to the species level. In our case also, the isolate was identified using the VITEK 2 system.

As NVS are parts of normal commensal flora of human mouth, genital and intestinal tracts, their exact pathogenic role is unclear. Proteins secreted by these species may act as virulence determinants for interaction with the host. The secretome of G. adiacens is well documented in infective endocarditis and oral infections. More importantly, G. adiacens secretome comprised several putative virulence proteins, which enhance bacterial colonization and virulence through their multifunctional roles.[34,35]Granulicatella and Abiotrophia spp. have the ability to bind to fibronectin and other extracellular matrix proteins and this binding ability appears to correlate with their degree of infectivity.[36]

Thus, clinicians should be aware of the pathogenic potential of these organisms. They can be easily overlooked because of their poor growth or no-growth on conventional solid media. NVS should be suspected when Gram stain shows microbial cells but cultures are negative. Due to the difficulties in identification of these bacteria, it is crucial for microbiology staff to be vigilant to prevent misidentification. For culture-negative cases, molecular test or Matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOFMS) would be a faster and reliable method for identification. The difficulty in identifying these organisms leads to delays in diagnosis. In addition, the results of susceptibility testing may not be accurate or reliable. Therefore, appropriate supplemented media and a reliable detection system should be used to identify these fastidious organisms.

Acknowledgments

We would like to thank Mrs. Alakananda Mahapatra, laboratory technician, for technical help.

Conflict of Interest

None declared.

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