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Intra-peritoneal abscess after an abdominal hysterectomy involving Cutibacterium avidum (former Propionibacterium avidum) highly resistant to clindamycin
Anaerobe 59 (2019) 176e183
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Clinical microbiology
Intra-peritoneal abscess after an abdominal hysterectomy involving Cutibacterium avidum (former Propionibacterium avidum) highly resistant to clindamycin M.C. Legaria a, *, C. Barberis a, J. Camporro b, G.M. Traglia a, A. Famiglietti a, D. Stecher b, C.A. Vay a tedra de Universidad de Buenos Aires, Facultad de Farmacia y Bioquímica, Hospital de Clínicas Jos e de San Martín, Departamento de Bioquímica Clínica, Ca Microbiología Clínica, Buenos Aires, Argentina Universidad de Buenos Aires. Facultad de Medicina, Hospital de Clínicas Jos e de San Martín, Servicio de Infectología, Buenos Aires, Argentina
a
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 24 April 2019 Received in revised form 20 June 2019 Accepted 24 June 2019 Available online 26 June 2019
Cutibacterium avidum is a gram-positive anaerobic rod belonging to the cutaneous group of human bacteria with preferential colonization of sweat glands in moist areas. The microorganism rarely cause disease, generally delayed prosthetic joint infections (PJIs). We describe the second case of intraperitoneal abscess by C. avidum after an abdominal surgery in an obese female patient and the first case after a non-prosthetic abdominal surgery due to a highly clindamycin resistant strain in a patient with underling conditions. The patient was successfully treated with surgical drainage and beta-lactam antibiotics. Although rare and apparently non-pathogenic, C. avidum may be involved in infections, especially in some high-risk patients with obesity who have undergone surgical incision involving deep folder of the skin. The microorganism was identified by phenotypic methods, MALDI-TOF MS and 16S rRNA gene sequencing. Susceptibility test should be performed in C. avidum because high level resistance to clindamycin could be present. We present a literature review of C. avidum infections. © 2019 Published by Elsevier Ltd.
Handling Editor: Vincent Rotimi Keywords: Cutibacterium avidum Cutibacterium spp. Propionibacterium avidum Propionibacterium spp. Abscess Clinical infections Antimicrobial resistance
Contents 1.
2.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1. Case presentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction On the skin surface, the anaerobic microbial community is mostly constituted by species belonging to the genera Propionibacterium. While these commensal microorganisms, are critical in
* Corresponding author. E-mail address: [email protected] (M.C. Legaria). https://doi.org/10.1016/j.anaerobe.2019.06.013 1075-9964/© 2019 Published by Elsevier Ltd.
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the regulation of skin homeostasis and prevents colonization from other harmful pathogens, they can also act as an opportunistic pathogen [1e3]. In 1946, Douglas and Gunter proposed the Propionibacterium genus [4,5], and recently, after a significant taxonomic revision the Propionibacterium species from the skin microbiota were replaced for Cutibacterium for Propionibacterium avidum, Propionibacterium acnes, Propionibacterium granulosum, and the more recently discovered species Propionibacterium namnetense [6] and
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Propionibacterium humerusii by Scholz and Kilian [6e8]. The skin Cutibacterium spp. composition varies with the site of the body. C. avidum lives mainly in moist areas, like the groin, axillae, perianal region and nares, and appeared during puberty while Cutibacterium acnes inhabits mainly sebum-rich areas, like the back, chest, face and scalp. It seems that water is the dominant environmental force for C. avidum, like sebum is for C. acnes [9e13]. C. avidum has been reported in a few cohort studies on PJIs [14e18], others derived from individual case reports [17,19e35] and a recently published series of skin and soft-tissue infections cases [36]. Here we present the case of intra-peritoneal abscess after an abdominal hysterectomy involving a high-level clindamycin resistant C. avidum isolate not previously described. A literature review was carried out. 2. Case presentation A 47-year-old female with history of HIV infection, with no detectable viral load, CD4: 680/mm3 (46%), follicular lymphoma in remission, obesity (body mass index (BMI) 38.7 kg/m2), steatosis and type II diabetes. She had undergone hysterectomy secondary to myomas that caused severe metrorrhagia and anemia. After 96 h, she started with fever (38.5 C), pain in hypogastrium and left flank with local erythema and induration. Physical examination revealed diffuse abdominal pain, predominantly in hypogastrium and in left flank, induration, erythema and swelling. On admission, hematocrit was 28%, hemoglobin 9,2 g/L, WBC 8.4 109/L, glycemia 79 mg/dl, normal blood clotting tests. Abdominal computed tomography scans showed a hydroaeric collection between the oblique and left transverse muscles, with extension to the rectus abdominis and a hyperdense effusion in the supravesical space that required surgical evacuation (Figs. 1e3). The samples obtained from the wound, abdominal wall and prevesical effusion, blood and urine were cultured. Blood (aerobic and anaerobic bottles, BACTEC™Media, Becton Dickinson) and urine cultures were negative. The three intraoperative samples were processed aseptically within 2 h after surgery. Gram stain showed leucocytes and small number of short gram-positive rods (Fig. 4). Aliquots were inoculated onto chocolate agar, blood agar plates (incubated under 5% CO2), Levine EMB agar eosin methylene blue agar plates (incubated under aerobic atmosphere), Brucella agar plates supplemented with 5% sheep blood, hemin, vitamin K (incubated under anaerobic atmosphere) and into anaerobic enrichment broths. C. avidum grew in pure culture. The microorganism was aerotolerant and showed colonies creamy,
Fig. 2. CT scan coronal plane.
Fig. 3. CT scan sagittal plane. Fluid collection with extension to the rectus abdominis muscle.
Fig. 1. CT scan, axial plane. Fluid collection with air bubble inside, between left transverse muscle and the oblique muscle and a supravesical fluid collection.
yellowish, and convex with wide zone of beta-hemolysis (Figs. 5 and 6). The identification was performed by conventional methods and by MALDI-TOF MS (Microflex LT Bruker Daltonics, Bremen, Germany) using MALDI Biotyper 3.1. The phenotypic identification included a positive reaction for catalase, CAMP factor, and esculin hydrolysis, and a negative test for urea and indole to
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Fig. 6. C. avidum on blood agar showing beta-hemolysis.
Fig. 4. Gram stain of material from the intraabdominal abscess showing numerous polymorphonuclear cells and gram-positive coccobacilli in clusters.
strands, using an ABIPrism 3100 BioAnalyzer equipment. The nucleotide sequences were analyzed using the Blast V2.0 software. The result showed a 99% nucleotide identity with Propionibacterium avidum DSM 4901 (GenBank accession number NR118647). The sequences for the 16S RNA ribosomal of C. avidum 825 were assigned GenBank accession number MK618585. The antibiotic susceptibility testing was performed using E-test rieux). A bacterial suspension adjusted to strips (AB Biodisk, Bio-Me a McFarland standard of 0.5 was inoculated onto brucella agar plates that were incubated under anaerobic conditions for 48 h. The minimal inhibitory concentration (MIC) were interpreted in accordance with Clinical Laboratory Standards Institute (CLSI) criteria for anaerobic organism in CLSI Document M100 [38]. C. avidum showed susceptibility to (MIC in mg/ml): ampicillin (0.125), ampicillin-sulbactam (0.125), piperacillin-tazobactam (0.75) and cefoxitin (1.5), and resistance (mg/ml) to metronidazole (256) and clindamycin (256). The patient was treated with vancomycin (1gr/12 h) and imipenem (500 mg/6 h) that was adjusted after bacteriological results to piperacillin-tazobactam (4.5gr/6 h). She completed 14 days of this last treatment with amoxicillin-clavulanic acid. There has been no evidence of recurrence to date. 3. Discussion
Fig. 5. C. avidum in Brucella blood agar plate.
distinguish from other Cutibacterium spp. Identification by MALDITOF MS showed a spectral score of 2.223 for Cutibacterium avidum. In order to confirm the identification, 16S rRNA gene sequencing was performed. PCR reactions were carried out using the “Kit T-Plus ADN polimerasa SIEMBRA DIRECTA” according to manufacturer's instructions (INBIO HIGHWAY Inc, Argentine). PCR products of the 16S rRNA gene were obtained with the primers described by Weisburg et al. [37]. Sequencing was performed on both DNA
The present report presented differences and similarities with respect to C avidum infections previously reported. There is a paucity of published data on C. avidum infections, specially outlining factors associated with risks, diagnosis and management of these entities and the vast majority of these cases are prosthetic joint infections (PJIs). It is striking that the majority corresponded to late post-surgical infections in areas colonized by C. avidum. Most of them related to foreign bodies, mainly after implantation of arthroplasties. Direct inoculation is the main mechanism of the C. avidum infection, from groin skin folds [12,14e16,18,20,35]. Unlike Cutibacterium acnes which mainly causes shoulder PJIs [18,39], C. avidum is predominantly associated with hip arthroplasty [16,40], in patients with higher BMIs [15]. Indeed, patients
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colonized with C. avidum have higher BMI than those with C. acnes and Cutibacterium granulosum [12,14,16,18,35]. PJIs in the hip were associated to colonization of sweat glands in the groin, perianal regions and skin folds typically found in obese individuals which may facilitate their entry into the surgical wound [10,16,41]. C. avidum was also isolated in cases other than PJIs. (Table 1). The microorganism has been recovered also as a commensal from the axilla of adolescents, which probably increase with age [9]. Breast infections are the most common described [36], mainly in patients who had undergone a surgery [17,21e25], and also in cases without previous surgery [25,26]. C. avidum is also capable of causing infections in other sites than breast [17] such as buttock abscess [2], abscess of the root of the thigh [28], splenic abscess as a complication of cardiac catheterization [30,31], sacroiliitis with ilio-psoas muscle abscess and osteomyelitis [20], and others [36]. Finally, an abdominal wall and intraperitoneal abscess after a prosthetic parietoplasty like our case [19]. However, it is remarkable that in our patient the infection occurred after a surgery not associated with prostheses. It is notable that C. avidum cause mostly delayed infections (i.e. presenting one month and later after surgery) [16,25,27,32,34]. In fact, the microorganism can remain intracellular in a dormant state for weeks and months, which explains the long incubation period [32]. The re-isolation of the same strain causing a PJI 18 months later, suggest the persistence and long-term colonization capacity of C. avidum [14]. By contrast, the infection in our patient manifested within 96 h after an abdominal hysterectomy. As suggested by other authors, this difference may be explained, in part, because soft tissue compared to the joint prosthesis made local signs of inflammation earlier visible [18]. However, this was not the case either in C. avidum infections different from PJIs, such as: breast abscess after a mastectomy or mammoplasty [22,23,25]. intraperitoneal abscess by C. avidum after a prosthetic parietoplasty [19], infective endocarditis after cardiac surgeries [32,34], splenic abscess as a complication of cardiac catheterization [30,31], a buttock abscess after haemorrhoidectomy [27], in which the incubation period lasted several weeks or months after the aforementioned surgeries or interventions. Indeed, it is important to note that in the series of cases reported by Tena D. et al., an infection was defined a postoperative surgical infection if it was acquired within 30 days after the surgical procedure, thus the cases of breast infections included maybe occurred in patients with an older surgery [36]. Despite the fact that C. avidum infections developed mainly after surgery, it was important to take into account that other routes of infection are also feasible and can show similar findings (Table 1) such as bacteremia and arthritis of the hip after intraarticular glucocorticoid injection [35], cervical osteomyelitis presumably by hematogenous spread [29], a root of a thigh abscess in a patient with seborrhic dermatitis associated with maceration of the skin at the level of inguinal fold [28], a recurrent breast abscess that resulted from mammary duct ectasia [26], two cases of splenic abscess after cardiac catheterization [30,31], a perianal abscess associated with a primary skin and soft tissue lesion containing dead cells and tissues that attracted bacteria after hemorrhoidectomy [27] and other similar cases [36]. Underlying conditions apart from obesity, presence of foreignbody and previous surgery were noted in rare occasions of C. avidum infections. (Table 1). For example, in monoclonal gammopathy [35], longstanding history of hepatitis B virus induced liver cirrhosis [27], ductal carcinoma in situ [25], rheumatoid arthritis and obstructive lung disease under corticoid therapy [14], and diabetes mellitus [29,34,36]. Moreover the smoker patients, such as a heavy smoker patient, in which tobacco have likely increased the pathogen's morbidity and affected wound healing [24,36]. The patient with an infected seroma had a chronic
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obstructive pulmonary disease, an ischemic heart disease, a chronic renal failure and an abdominal surgery [36}. Our patient presented HIV infection, follicular lymphoma in remission, obesity, steatosis and type II diabetes. It is noteworthy that C. avidum infections in immunocompetent patients also were reported [14,22,25,26,28,36]. C. avidum may be more virulent [15,18] and show higher hemolytic activity than C. acnes [16, 35. 42, 43]. This last event could have implications for potential side effects in the host and -like the hemolytic phenotype of C. acnes-may represent a more pathogenic strain [42,44,45]. Moreover, this characteristic was very striking at the time of the phenotypic identification in our strain. An exopolysaccharide-like structure seems to play a role in bacterial adherence and biofilm formation [14], such as in the presence of implanted foreign materials [46]. In cases like ours, in which prosthetic materials were absent, sutures may host bacteria during their resorption phase favoring the infection after surgery [24,47e49]. Only one case of C. avidum intra-peritoneal infection have been described [19]. In this case the patient was referred to the hospital two months after prosthetic parietoplasty, while in our case the infection manifested 96 h after an abdominal hysterectomy without prostheses. Similarly, the patients were female, and had similar age (46 and 47 years, respectively), high BMI (30.1 and 38.7 kg/m2, respectively), previous abdominal surgery, hydroaeric and multiple collected intra-peritoneal effusions. In both patients, the infection sites were surgically evacuated yielding purulent fluid that showed gram-positive rods and pure growth of C. avidum. Also, both received antibiotic treatment and presented favorable evolution. Unfortunately, the case of post abdominal surgery infection included in the series reported by Tena D et al., have not complete data available to be compared [36]. If we observe the reported cases of C. avidum infections other than PJIs (n ¼ 30, Table 1), 73% (22/30) were female and the median age was 53 (range: 23e85 years). Three patients had prosthetic valve endocarditis, two died, but the other had a favorable outcome. Of the remaining 27 patients, 22 (73%) resulted in cure of the infection, 4 presented recurrence, 1 unknown, and 1 presented lowgrade inflammation, and a mastectomy was being considered. Sixteen patients (53%) had a history of previous surgery (15) or catheterization (1), six of them with foreign body. Fourteen (47%) had a breast infection, 6 after breast surgery. Surprisingly, obesity was observed in all cases the BMI/obesity was reported (5). Blood cultures were positive in 5/11 (45.5%) reported cases, sacroilitis (n ¼ 1), septic arthritis (n ¼ 1) and endocarditis (n ¼ 3). Surprisingly, C. avidum grew in pure culture in 25/30 (83%) of cases. There is not treatment consensus for Cutibacterium infections. However, it seems that eradication is best achieved by a combination of both appropriate antimicrobial and surgical treatment [18,19,32]. The extracellular factors produced by C avidum are considered important factors that contribute to limitation of antibiotic access to the site of infection. Although in some cases, of C. avidum infections antimicrobial monotherapy was used [19] the combination of antibiotics is more frequently reported as treatment of choice [14,28]. In most of them rifampicin has been associated with cefazolin [35], penicillin, ciprofloxacin [32], clindamycin [14], daptomycin, penicillin [32], vancomycin, gentamicin [33], or amoxicillin and levofloxacin [18,29,33]. Some authors have reported that a rifampin-containing treatment should be considered in some serious infections like Cutibacterium prosthetic infective endocarditis due to its activity against planktonic and biofilm Cutibacterium, the very low MIC, the excellent oral bioavailability and the high tissue penetration [32]. Surgery is needed in a high proportion of patients, mainly due to infection extension and abscess formation [27]. Our patient was
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Table 1 Main features of reported cases of C. avidum infections other than PJIs. Author Gender/Age (year)/ Publication date Country
Comorbities/Predisposing condition
Braun DL F/70/ Biological aortic valve replacement surgery 2013 Switzerland
Site/Previous surgery/ BMI/CRP/WC/ Outcome Surgery, drainage Length from surgery Temperature ( C) or treatment/AM to infection fever/Isolation source/BC treatment/Length of AM treatment Prosthetic valve endocarditis/Aortic valve surgery/3 months
Prosthetic valve endocarditis/Aortic valve surgery/8 months Prosthetic valve endocarditis/c/ Cardiac surgery/~6 months Cervical Rodrigues F M/ DM/8 kg weight loss in 3 months, intra-muscular quinine osteomyelitis/Gluteal 77/2018 abscess (Streptococcus injection (Malaria) France pneumoniae) surgically drained/-2 months Osteomyelitis, psoas Estoppey O M/ Surgical repair of an inguinal hernia abscess, sacroiliitis/ 67/1997 hernia surgery/10 Switzerland days Right breast abscess/ Werno AM F/ Right total mastectomy and mastectomy and transverse rectus abdominis 53/2004 muscle flap reconstruction for a rectus abdominis New multicentric ductal carcinoma in muscle flap Zealand reconstruction/1 situ month Left breast abscess/ Werno AM F/ Left breast abscess, granulomatous mastitis No/33/2004 New Zealand Bilateral breast Levin B. F/56/ Bilateral breast reduction surgery infections/breast 2008 reduction surgery/1 Australia month Bradbury RS F/ Recurrent breast abscess, history Breast abscess/-/of puerperal mastitis, mammary 44/2011 duct ectasia Australia Bilateral breast reduction Bilateral breast Kritikos A F/ surgery abscess/breast 37/2015 reduction surgery/7 Switzerland weeks Panagea S F/ Bilateral breast reduction Bilateral breast 40/2005 UK surgery abscess/breast reduction surgery/3 weeks Unilateral breast di Summa PG Bilateral breast reduction abscess/breast F/36/2015 surgery/tobacco smoker reduction surgery/3 Austria weeks Splenic abscess/ Dunne WM M/ Placement of four coronary coronary bypass bypass grafts, malaria. during 61/1986 surgery/8 weeks World War II USA LoureiroAmigo J F/ 85/2016 Spain Vetromile F M/ 67/2001 Argentina
Permanent pacemaker implantation, HA, DM, bioprosthetic aortic valve, weight loss. Prosthetic mitral valve, weight loss
Vohara A M/ 79/1998 USA
Cardiac catheterization with angioplasty. DBT. AHT
Bentorki AA M/26/2013 Algeria
Depressive episode, seborrheic dermatitis associated with maceration of the skin at the level of inguinal fold. Intraarticular (hip) glucocorticoid treatment, steoarthritis, overweight, weight loss (5 kg), ynphoma.
Million M F/ 78/2008 France
NR/208/NR/37.6 C/Aortic Prosthetic valve Favorable vegetation þ BC/POS replacement/AMC, PEN þ GEN, PEN þ RIF, CIP þ RIF/ 12 weeks NR/86/14 109/38.3 C/ Yes/ Fatal BC/POS DAP þ AMP þ CRO, PEN/13 days
Co-infection
Identification
No
NR
No
MALDI-TOF MS
NR/NR/NR/NR, fever/BC/ POS
-/VAN þ GEN þ RIF/ Fatal 99 days
No
NR
NR (obese)/68/NR/ afebrile/Two vertebral discs/NEG
Surgery/AMX þ RIF/ Favorable 6 weeks
No
NR
NR/NR/16.6 109/ afebrile/abscess, bone biopsy, BC/POS
Surgery-/CIP þ AC/- Favorable
No
NR/NR/12.0 109/ afebrile/abscess/NR
Drainage/ flucloxacillin, penicillin/NR
Favorable
No
API Coryne Conventional 16S rRNA sequencing
NR/103/12.9 109/ 37.2 C/abscess, wound, tissue/NR
Drainage/AMC, doxycycline
No Low-grade inflammation. Mastectomy?
API Coryne Conventional 16S rRNA sequencing
NR/7.1/10.3 109/NR/ necrosic area (nipples) and deep swab from both breasts/NR NR/NR/NR/NR/breast tissue/NR
Debridement/MEM, Favorable MOX augmentin/~8 weeks
No
Surgery/ND/-
Favorable
No
API Coryne 16S rRNA sequencing
Favorable
No
MALDI-TOF MS
NR/135/22.5 109/ 37.2 C/abscess/NEG
Drainage/FLU þ BEN Favorable PEN, AMC/~5 weeks
No
API Coryne Conventional 16S rRNA sequencing
NR/6/11 109/afebrile/ abscess/NR
Drainage/AMC, AMX/~6 week
Favorable
No
NR
Favorable
No
Surgery/NR/-
Favorable
No
Conventional Gas chromatographic analysis of volatile acids NR
Drainage/CIP, MTZ þ CFZ, CFX/2 weeks
Favorable
No
API Coryne Conventional
Favorable
No
Conventional
NR/16/9.1 109/afebrile/ -/AMC, AMX/6 abscess/NR weeks
NR/NR/5.6 109/38.0 C/ Surgery/NR/splenic abscess/NEG
NR/NR/13.1 109/ Splenic abscess/ cardiac 38.9 C/splenic abscess/ catheterization/6 NEG weeks Abscess of the root of NR/26/11.1 109/ the thigh/-/afebrile/abscess/NR
Septic arthritis of the 30.5/185e218/6.5 109/ Surgery/CFZ þ RIF/ hip/-/12 weeks 38.5 C/joint fluid þ acetabulum þ BC/ POS
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Table 1 (continued ) Author Gender/Age (year)/ Publication date Country
Comorbities/Predisposing condition
Site/Previous surgery/ BMI/CRP/WC/ Outcome Surgery, drainage Length from surgery Temperature ( C) or treatment/AM to infection fever/Isolation source/BC treatment/Length of AM treatment
Wang TKF M/ 70/2002 Hong Kong
Hemorrhoidectomy. Hepatitis B carrier, chronic liver failure, ascites, splenomegaly, testicular atrophy, primary skin and soft tissue lesion Breast cancer, breast surgery
Perianal subcutaneous abscess/ Hemorrhoidectomy/ 17 month Surgical wound infection, necrotizing infection/NR/-
Series of 11 cases: Tena D 1-F/43/ 2019 Spain 2-F/66/2019 No
NR/NR/NR/NR/breast exudate/NR
NR/NR/NR/NR/Breast abscess/NR Breast abscess/No/NR/NR/NR/NR/Breast abscess/NR Breast abscess, NR/NR/NR/NR/Breast necrotizing infection/ abscess, aspirate/NR No/-
No
4-F/49/2019
Depression
5-F/46/2019
No
Breast abscess/No/-
6-F/23/2019
No
Breast abscess/No/-
7-F/47/2019
Smoking
Breast abscess/No/-
8-M/39/2019
Smoking, dyslipemia
9-M/33/019
Smoking, hidradenitis (axilla)
Infected sebaceous cyst (retroauricular)/ No/Axillary abscess/No/-
10-M/77/2019 AH, COPD, IHD, CRF, abdominal Infected seroma surgery (abdominal)/ abdominal surgery/11-F/51/2019 DM, obesity, hidradenitis Suppurative hidradenitis (pubis)/ No/Abdominal wall, Janvier F F/46/ Prosthetic parietoplasty/ 2013 France abdominal wall eventration 14 intra-peritoneal abscess/prosthetic months after an abdominal parietoplasty/2 hysterectomy months Present case F/ Hysterectomy. HIVþ, follicular Intra-peritoneal lymphoma, DBT, steatosis. collections/ 47 Abdominal Argentina hysterectomy 96 h.
Identification
Favorable
No
API Coryne Conventional
Debridement/AMC, Favorable VAN LNZ/17 days
No
MALDI-TOF MS
Drainage/CLIN/15 days Drainage/AMC/13 days Drainage, debridment/ IMP,Cefditoren/15 days Drainage/AMC/7 days Drainage/AMC/7 days No (spontaneous dranage)/LEV,CLIN/ 22 days Drainage/AMC/7 days
Finegoldia MALDI-TOF MS magna Finegoldia MALDI-TOF MS magna Peptoniphilus MALDI-TOF MS harei
NR/NR/7.5 109 Drainage/ (baseline level 4.9 109) AMP þ CLOX/1 week afebrile/abscess/NR
Breast abscess/No/-
3-F/41/2019
Co-infection
NR/NR/NR/NR/Breast abscess/NR NR/NR/NR/NR/Breast abscess/NR NR/NR/NR/NR/Breast abscess/NR NR/NR/NR/NR/abscess sebaceous cyst retroauricular/NR NR/NR/NR/NR/axillary abscess/NR NR/NR/NR/NR/seroma/ NR
Favorable Favorable Recurrence
Favorable
No
MALDI-TOF MS
Favorable
No
MALDI-TOF MS
Recurrence
Actinotignum MALDI-TOF MS shaalii
Recurrence
No
MALDI-TOF MS
Drainage/AMC/10 days No/AMC/10 days
Favorable
No
MALDI-TOF MS
Recurrence
No
MALDI-TOF MS
No/CIP, CLIN NR
Unknown
Actinomyces neuii
MALDI-TOF MS
Surgery/AMC/4 weeks
Favorable
No
MALDI_TOF MS API Coryne 16S rRNA sequencing
38.7/NR/8.5x109/38.5 C/ Surgery/VAN þ IMP, Favorable TAZ, AC/~555 3 intra-peritoneal weeks collections/NEG
No
MALDI-TOF MS Conventional 16S rRNA sequencing
NR (obese)/NR/NR/NR/ exudate (suppurative hidradenitis)/NR 31.2/162/13x109/37 C/ intra-peritoneal collections/NEG
Note: WBC: white blood cells. (N x109/L). BC: Blood culture. Blood culture: negative (NEG)/positive (POS). BMI: body mass index (kg/m2). CRP: C reactive protein (mg/L). AM treatment: antimicrobial treatment. Length AM treatment. AH: arterial hypertension. DM: diabetes mellitus. NA: not available. AMX: amoxicillin. BEN PEN: benzyl penicillin. AMC: amoxicillin-clavulanic acid. FLU: flucloxacillin. CLIN: clindamycin. RFA: rifampicin. PP: phenoxymethylpenicillin. CFZ: cefazolin. CFX: cephalexin. CLOX: cloxacillin. MEM: meropenem. NR: not reported. COPD: chronic obstructive pulmonary disease; IHD: ischemic heart disease; CRF: chronic renal failure.
treated successfully with a combination of surgery and antibiotics. A consideration regarding surgery that should be taking into account is that obesity rates are rising worldwide, and some authors have suggested that prophylactic cefazolin dose should be doubled for obese patients [50]. Also, specific preoperative topical skin preparation should also be considered to diminish the colonization [51]. The true incidence of Cutibacterium infections may be underestimated because of its categorization as a low virulence microorganism, interpretation as common skin colonizer and insufficient culture time [17,23,26,32,34,52,53]. However, C. avidum may be isolated from blood in serious entities such as: infective endocarditis [32e34], osteomyelitis [20,29] and septic arthritis [35]. Although the presence of oxygen reduces the growth rate for all Cutibacterium spp., C. avidum is the best species at adapting its growth to aerobic conditions [26,54,55]. Nevertheless, some authors have described cases of C. avidum bacteremia, in which only
the anaerobic bottles yielded the microorganism [34. 35]. Blood cultures in our case were negative despite including anaerobic and aerobic bottles. Like most laboratories we routinely incubate the blood cultures for five days, but it would be advisable to extend the incubation culture time in these cases [32-34,52,53]. Cutibacterium species is seldom isolated from true infections from abdominal origin in adults [55] and never in children [56,57]. Unlike C. acnes, C. avidum was not an agent of contamination in some cases [15]. Fortunately, in our case, C. avidum grew in pure culture in three relevant samples obtain by surgical drainage. This fact was reported in several cases, which greatly facilitated the adjudication of a pathogenic role in the assessed entity [14,19,21e23,25,27e31]. According to the literature an aerotolerant gram-positive rod that showed creamy colonies with a wide zone of beta-hemolysis in aerobic and anaerobic atmosphere is suggestive of C. avidum [17,19,25]. Although C. avidum was reported to be identified using
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automated system VITEK 2 (bioMerieux, Marcy L'Etoile, France) [18] and API Coryne strip [25e28], some reports have demonstrated problems with VITEK 2 (Propionibacterium granulosum (91%)/Propionibacterium propionicus (88%), API Coryne system (Propionibacterium propionicus/avidum) [19] and no identification with VITEK MS [58]. Like other authors, we correctly identify C. avidum by phenotypic methods and MALDI- TOF MS. This method have demonstrated to be accurate [12,14,19,23,24,34] including by the Andromas matrix-assisted laser desorption ionization-time of flight mass spectrometry system [59]. Similar to other cases, the identification of our isolate as Propionibacterium avidum was confirmed by 16s rRNA sequencing [14, 25 26]. The microorganism can show the same homology percentage with Propionibacterium propionicum. However, biochemical tests can help to achieve the correct identification [21]. In general C. avidum is susceptible to penicillin and other blactams, clindamycin, rifampin, moxifloxacin, vancomycin and naturally resistant to metronidazole [14, 18, 19, 24. 25, 27, 28, 30, 32, 34, 35, 60, 61]. However, in our and some other cases, C. avidum was resistant to clindamycin [16e18,23,36]. This is very important because some guidelines and authors have used it for treatment and/or prophylaxis [14,15,18,24,62e64]. 4. Conclusions To our knowledge, this is the first documented case of nonprosthetic intra-peritoneal infection by a clindamycin resistant C. avidum and the second one in a female patient with obesity and previous abdominal surgical intervention. C. avidum should be suspected as the etiologic agent in clinically relevant samples with pure culture, especially from obese patients with surgical incision site close to areas colonized with the bacteria and despite the absence of foreign material and other comorbidities. C. avidum was rapidly identified by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS). For the resolution, both, antimicrobial treatment and surgical intervention may be required. Although rare, monitoring antibiotic resistance in members of Cutibacterium spp. is necessary because clindamycin could be a therapeutic option. References [1] M. Rosenthal, D. Goldberg, A. Aiello, E. Larson, B. Foxman, Skin microbiota: microbial community structure and its potential association with health and disease, Infect. Genet. Evol. 11 (2011) 839e848, https://doi:10.1016/ j.meegid.2011.03.022. [2] G.J. Christensen, H. Bruggemann, Bacterial skin commensals and their role as host guardians, Benef. Microbes 5 (2014) 201e215, https://doi.org/10.3920/ BM2012.0062. [3] K. Szabo, L. Erdei, B.S. Bolla, G. Tax, T. Biro, L. Kemeny, Factors shaping the composition of the cutaneous microbiota, Br. J. Dermatol. 176 (2017) 344e351. https://doi:10.1111/bjd.14967. [4] Y. Achermann, E.J.C. Goldstein, T. Coenye, M.E. Shirtliff, Propionibacterium acnes: from commensal to opportunistic biofilm-associated implant pathogen, Clin. Microbiol. Rev. 27 (2014) 419e440. https://doi.org/10.1128/CMR.0009213. [5] H.C. Douglas, S.E. Gunter, The taxonomic position of Corynebacterium acnes, J. Bacteriol. 52 (1946) 15e23. [6] G.G. Aubin, P. Bemer, S. Kambarev, N.B. Patel, O. Lemenand, J. Caillon, P.A. Lawson, S. Corvec, Propionibacterium namnetense sp. nov., isolated from a human bone infection, Int. J. Syst. Evol. Microbiol. 66 (2016) 3393e3399, 2016, https://doi.org/10.1099/ijsem.0.001204. [7] S.M. Butler-Wu, D.J. Sengupta, W. Kittichotirat, F.A. Matsen, R.E. Bumgarner, Genome sequence of a novel species, Propionibacterium humerusii. J. Bacteriol. 193 (2011) 3678. https://doi.org/10.1128/JB.05036-11. [8] C.F.P. Scholz, M. Kilian, The natural history of cutaneous propionibacteria, and reclassification of selected species within the genus Propionibacterium to the proposed novel genera Acidipropionibacterium gen. nov., Cutibacterium gen. nov. and Pseudopropionibacterium gen. nov, Int. J. Syst. Evol. Microbiol. 66 (2016) 4422e4432. https://doi.org/10.1099/ijsem.0.001367. [9] N.K.M. Nordstrom, W.C. Noble, Colonization of the axilla by Propionibacterium avidum in relation to age, Appl. Environ. Microbiol. 47 (1984) 1360e1362.
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Clinical microbiology
Intra-peritoneal abscess after an abdominal hysterectomy involving Cutibacterium avidum (former Propionibacterium avidum) highly resistant to clindamycin M.C. Legaria a, *, C. Barberis a, J. Camporro b, G.M. Traglia a, A. Famiglietti a, D. Stecher b, C.A. Vay a tedra de Universidad de Buenos Aires, Facultad de Farmacia y Bioquímica, Hospital de Clínicas Jos e de San Martín, Departamento de Bioquímica Clínica, Ca Microbiología Clínica, Buenos Aires, Argentina Universidad de Buenos Aires. Facultad de Medicina, Hospital de Clínicas Jos e de San Martín, Servicio de Infectología, Buenos Aires, Argentina
a
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 24 April 2019 Received in revised form 20 June 2019 Accepted 24 June 2019 Available online 26 June 2019
Cutibacterium avidum is a gram-positive anaerobic rod belonging to the cutaneous group of human bacteria with preferential colonization of sweat glands in moist areas. The microorganism rarely cause disease, generally delayed prosthetic joint infections (PJIs). We describe the second case of intraperitoneal abscess by C. avidum after an abdominal surgery in an obese female patient and the first case after a non-prosthetic abdominal surgery due to a highly clindamycin resistant strain in a patient with underling conditions. The patient was successfully treated with surgical drainage and beta-lactam antibiotics. Although rare and apparently non-pathogenic, C. avidum may be involved in infections, especially in some high-risk patients with obesity who have undergone surgical incision involving deep folder of the skin. The microorganism was identified by phenotypic methods, MALDI-TOF MS and 16S rRNA gene sequencing. Susceptibility test should be performed in C. avidum because high level resistance to clindamycin could be present. We present a literature review of C. avidum infections. © 2019 Published by Elsevier Ltd.
Handling Editor: Vincent Rotimi Keywords: Cutibacterium avidum Cutibacterium spp. Propionibacterium avidum Propionibacterium spp. Abscess Clinical infections Antimicrobial resistance
Contents 1.
2.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1. Case presentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction On the skin surface, the anaerobic microbial community is mostly constituted by species belonging to the genera Propionibacterium. While these commensal microorganisms, are critical in
* Corresponding author. E-mail address: [email protected] (M.C. Legaria). https://doi.org/10.1016/j.anaerobe.2019.06.013 1075-9964/© 2019 Published by Elsevier Ltd.
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the regulation of skin homeostasis and prevents colonization from other harmful pathogens, they can also act as an opportunistic pathogen [1e3]. In 1946, Douglas and Gunter proposed the Propionibacterium genus [4,5], and recently, after a significant taxonomic revision the Propionibacterium species from the skin microbiota were replaced for Cutibacterium for Propionibacterium avidum, Propionibacterium acnes, Propionibacterium granulosum, and the more recently discovered species Propionibacterium namnetense [6] and
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Propionibacterium humerusii by Scholz and Kilian [6e8]. The skin Cutibacterium spp. composition varies with the site of the body. C. avidum lives mainly in moist areas, like the groin, axillae, perianal region and nares, and appeared during puberty while Cutibacterium acnes inhabits mainly sebum-rich areas, like the back, chest, face and scalp. It seems that water is the dominant environmental force for C. avidum, like sebum is for C. acnes [9e13]. C. avidum has been reported in a few cohort studies on PJIs [14e18], others derived from individual case reports [17,19e35] and a recently published series of skin and soft-tissue infections cases [36]. Here we present the case of intra-peritoneal abscess after an abdominal hysterectomy involving a high-level clindamycin resistant C. avidum isolate not previously described. A literature review was carried out. 2. Case presentation A 47-year-old female with history of HIV infection, with no detectable viral load, CD4: 680/mm3 (46%), follicular lymphoma in remission, obesity (body mass index (BMI) 38.7 kg/m2), steatosis and type II diabetes. She had undergone hysterectomy secondary to myomas that caused severe metrorrhagia and anemia. After 96 h, she started with fever (38.5 C), pain in hypogastrium and left flank with local erythema and induration. Physical examination revealed diffuse abdominal pain, predominantly in hypogastrium and in left flank, induration, erythema and swelling. On admission, hematocrit was 28%, hemoglobin 9,2 g/L, WBC 8.4 109/L, glycemia 79 mg/dl, normal blood clotting tests. Abdominal computed tomography scans showed a hydroaeric collection between the oblique and left transverse muscles, with extension to the rectus abdominis and a hyperdense effusion in the supravesical space that required surgical evacuation (Figs. 1e3). The samples obtained from the wound, abdominal wall and prevesical effusion, blood and urine were cultured. Blood (aerobic and anaerobic bottles, BACTEC™Media, Becton Dickinson) and urine cultures were negative. The three intraoperative samples were processed aseptically within 2 h after surgery. Gram stain showed leucocytes and small number of short gram-positive rods (Fig. 4). Aliquots were inoculated onto chocolate agar, blood agar plates (incubated under 5% CO2), Levine EMB agar eosin methylene blue agar plates (incubated under aerobic atmosphere), Brucella agar plates supplemented with 5% sheep blood, hemin, vitamin K (incubated under anaerobic atmosphere) and into anaerobic enrichment broths. C. avidum grew in pure culture. The microorganism was aerotolerant and showed colonies creamy,
Fig. 2. CT scan coronal plane.
Fig. 3. CT scan sagittal plane. Fluid collection with extension to the rectus abdominis muscle.
Fig. 1. CT scan, axial plane. Fluid collection with air bubble inside, between left transverse muscle and the oblique muscle and a supravesical fluid collection.
yellowish, and convex with wide zone of beta-hemolysis (Figs. 5 and 6). The identification was performed by conventional methods and by MALDI-TOF MS (Microflex LT Bruker Daltonics, Bremen, Germany) using MALDI Biotyper 3.1. The phenotypic identification included a positive reaction for catalase, CAMP factor, and esculin hydrolysis, and a negative test for urea and indole to
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Fig. 6. C. avidum on blood agar showing beta-hemolysis.
Fig. 4. Gram stain of material from the intraabdominal abscess showing numerous polymorphonuclear cells and gram-positive coccobacilli in clusters.
strands, using an ABIPrism 3100 BioAnalyzer equipment. The nucleotide sequences were analyzed using the Blast V2.0 software. The result showed a 99% nucleotide identity with Propionibacterium avidum DSM 4901 (GenBank accession number NR118647). The sequences for the 16S RNA ribosomal of C. avidum 825 were assigned GenBank accession number MK618585. The antibiotic susceptibility testing was performed using E-test rieux). A bacterial suspension adjusted to strips (AB Biodisk, Bio-Me a McFarland standard of 0.5 was inoculated onto brucella agar plates that were incubated under anaerobic conditions for 48 h. The minimal inhibitory concentration (MIC) were interpreted in accordance with Clinical Laboratory Standards Institute (CLSI) criteria for anaerobic organism in CLSI Document M100 [38]. C. avidum showed susceptibility to (MIC in mg/ml): ampicillin (0.125), ampicillin-sulbactam (0.125), piperacillin-tazobactam (0.75) and cefoxitin (1.5), and resistance (mg/ml) to metronidazole (256) and clindamycin (256). The patient was treated with vancomycin (1gr/12 h) and imipenem (500 mg/6 h) that was adjusted after bacteriological results to piperacillin-tazobactam (4.5gr/6 h). She completed 14 days of this last treatment with amoxicillin-clavulanic acid. There has been no evidence of recurrence to date. 3. Discussion
Fig. 5. C. avidum in Brucella blood agar plate.
distinguish from other Cutibacterium spp. Identification by MALDITOF MS showed a spectral score of 2.223 for Cutibacterium avidum. In order to confirm the identification, 16S rRNA gene sequencing was performed. PCR reactions were carried out using the “Kit T-Plus ADN polimerasa SIEMBRA DIRECTA” according to manufacturer's instructions (INBIO HIGHWAY Inc, Argentine). PCR products of the 16S rRNA gene were obtained with the primers described by Weisburg et al. [37]. Sequencing was performed on both DNA
The present report presented differences and similarities with respect to C avidum infections previously reported. There is a paucity of published data on C. avidum infections, specially outlining factors associated with risks, diagnosis and management of these entities and the vast majority of these cases are prosthetic joint infections (PJIs). It is striking that the majority corresponded to late post-surgical infections in areas colonized by C. avidum. Most of them related to foreign bodies, mainly after implantation of arthroplasties. Direct inoculation is the main mechanism of the C. avidum infection, from groin skin folds [12,14e16,18,20,35]. Unlike Cutibacterium acnes which mainly causes shoulder PJIs [18,39], C. avidum is predominantly associated with hip arthroplasty [16,40], in patients with higher BMIs [15]. Indeed, patients
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colonized with C. avidum have higher BMI than those with C. acnes and Cutibacterium granulosum [12,14,16,18,35]. PJIs in the hip were associated to colonization of sweat glands in the groin, perianal regions and skin folds typically found in obese individuals which may facilitate their entry into the surgical wound [10,16,41]. C. avidum was also isolated in cases other than PJIs. (Table 1). The microorganism has been recovered also as a commensal from the axilla of adolescents, which probably increase with age [9]. Breast infections are the most common described [36], mainly in patients who had undergone a surgery [17,21e25], and also in cases without previous surgery [25,26]. C. avidum is also capable of causing infections in other sites than breast [17] such as buttock abscess [2], abscess of the root of the thigh [28], splenic abscess as a complication of cardiac catheterization [30,31], sacroiliitis with ilio-psoas muscle abscess and osteomyelitis [20], and others [36]. Finally, an abdominal wall and intraperitoneal abscess after a prosthetic parietoplasty like our case [19]. However, it is remarkable that in our patient the infection occurred after a surgery not associated with prostheses. It is notable that C. avidum cause mostly delayed infections (i.e. presenting one month and later after surgery) [16,25,27,32,34]. In fact, the microorganism can remain intracellular in a dormant state for weeks and months, which explains the long incubation period [32]. The re-isolation of the same strain causing a PJI 18 months later, suggest the persistence and long-term colonization capacity of C. avidum [14]. By contrast, the infection in our patient manifested within 96 h after an abdominal hysterectomy. As suggested by other authors, this difference may be explained, in part, because soft tissue compared to the joint prosthesis made local signs of inflammation earlier visible [18]. However, this was not the case either in C. avidum infections different from PJIs, such as: breast abscess after a mastectomy or mammoplasty [22,23,25]. intraperitoneal abscess by C. avidum after a prosthetic parietoplasty [19], infective endocarditis after cardiac surgeries [32,34], splenic abscess as a complication of cardiac catheterization [30,31], a buttock abscess after haemorrhoidectomy [27], in which the incubation period lasted several weeks or months after the aforementioned surgeries or interventions. Indeed, it is important to note that in the series of cases reported by Tena D. et al., an infection was defined a postoperative surgical infection if it was acquired within 30 days after the surgical procedure, thus the cases of breast infections included maybe occurred in patients with an older surgery [36]. Despite the fact that C. avidum infections developed mainly after surgery, it was important to take into account that other routes of infection are also feasible and can show similar findings (Table 1) such as bacteremia and arthritis of the hip after intraarticular glucocorticoid injection [35], cervical osteomyelitis presumably by hematogenous spread [29], a root of a thigh abscess in a patient with seborrhic dermatitis associated with maceration of the skin at the level of inguinal fold [28], a recurrent breast abscess that resulted from mammary duct ectasia [26], two cases of splenic abscess after cardiac catheterization [30,31], a perianal abscess associated with a primary skin and soft tissue lesion containing dead cells and tissues that attracted bacteria after hemorrhoidectomy [27] and other similar cases [36]. Underlying conditions apart from obesity, presence of foreignbody and previous surgery were noted in rare occasions of C. avidum infections. (Table 1). For example, in monoclonal gammopathy [35], longstanding history of hepatitis B virus induced liver cirrhosis [27], ductal carcinoma in situ [25], rheumatoid arthritis and obstructive lung disease under corticoid therapy [14], and diabetes mellitus [29,34,36]. Moreover the smoker patients, such as a heavy smoker patient, in which tobacco have likely increased the pathogen's morbidity and affected wound healing [24,36]. The patient with an infected seroma had a chronic
179
obstructive pulmonary disease, an ischemic heart disease, a chronic renal failure and an abdominal surgery [36}. Our patient presented HIV infection, follicular lymphoma in remission, obesity, steatosis and type II diabetes. It is noteworthy that C. avidum infections in immunocompetent patients also were reported [14,22,25,26,28,36]. C. avidum may be more virulent [15,18] and show higher hemolytic activity than C. acnes [16, 35. 42, 43]. This last event could have implications for potential side effects in the host and -like the hemolytic phenotype of C. acnes-may represent a more pathogenic strain [42,44,45]. Moreover, this characteristic was very striking at the time of the phenotypic identification in our strain. An exopolysaccharide-like structure seems to play a role in bacterial adherence and biofilm formation [14], such as in the presence of implanted foreign materials [46]. In cases like ours, in which prosthetic materials were absent, sutures may host bacteria during their resorption phase favoring the infection after surgery [24,47e49]. Only one case of C. avidum intra-peritoneal infection have been described [19]. In this case the patient was referred to the hospital two months after prosthetic parietoplasty, while in our case the infection manifested 96 h after an abdominal hysterectomy without prostheses. Similarly, the patients were female, and had similar age (46 and 47 years, respectively), high BMI (30.1 and 38.7 kg/m2, respectively), previous abdominal surgery, hydroaeric and multiple collected intra-peritoneal effusions. In both patients, the infection sites were surgically evacuated yielding purulent fluid that showed gram-positive rods and pure growth of C. avidum. Also, both received antibiotic treatment and presented favorable evolution. Unfortunately, the case of post abdominal surgery infection included in the series reported by Tena D et al., have not complete data available to be compared [36]. If we observe the reported cases of C. avidum infections other than PJIs (n ¼ 30, Table 1), 73% (22/30) were female and the median age was 53 (range: 23e85 years). Three patients had prosthetic valve endocarditis, two died, but the other had a favorable outcome. Of the remaining 27 patients, 22 (73%) resulted in cure of the infection, 4 presented recurrence, 1 unknown, and 1 presented lowgrade inflammation, and a mastectomy was being considered. Sixteen patients (53%) had a history of previous surgery (15) or catheterization (1), six of them with foreign body. Fourteen (47%) had a breast infection, 6 after breast surgery. Surprisingly, obesity was observed in all cases the BMI/obesity was reported (5). Blood cultures were positive in 5/11 (45.5%) reported cases, sacroilitis (n ¼ 1), septic arthritis (n ¼ 1) and endocarditis (n ¼ 3). Surprisingly, C. avidum grew in pure culture in 25/30 (83%) of cases. There is not treatment consensus for Cutibacterium infections. However, it seems that eradication is best achieved by a combination of both appropriate antimicrobial and surgical treatment [18,19,32]. The extracellular factors produced by C avidum are considered important factors that contribute to limitation of antibiotic access to the site of infection. Although in some cases, of C. avidum infections antimicrobial monotherapy was used [19] the combination of antibiotics is more frequently reported as treatment of choice [14,28]. In most of them rifampicin has been associated with cefazolin [35], penicillin, ciprofloxacin [32], clindamycin [14], daptomycin, penicillin [32], vancomycin, gentamicin [33], or amoxicillin and levofloxacin [18,29,33]. Some authors have reported that a rifampin-containing treatment should be considered in some serious infections like Cutibacterium prosthetic infective endocarditis due to its activity against planktonic and biofilm Cutibacterium, the very low MIC, the excellent oral bioavailability and the high tissue penetration [32]. Surgery is needed in a high proportion of patients, mainly due to infection extension and abscess formation [27]. Our patient was
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Table 1 Main features of reported cases of C. avidum infections other than PJIs. Author Gender/Age (year)/ Publication date Country
Comorbities/Predisposing condition
Braun DL F/70/ Biological aortic valve replacement surgery 2013 Switzerland
Site/Previous surgery/ BMI/CRP/WC/ Outcome Surgery, drainage Length from surgery Temperature ( C) or treatment/AM to infection fever/Isolation source/BC treatment/Length of AM treatment Prosthetic valve endocarditis/Aortic valve surgery/3 months
Prosthetic valve endocarditis/Aortic valve surgery/8 months Prosthetic valve endocarditis/c/ Cardiac surgery/~6 months Cervical Rodrigues F M/ DM/8 kg weight loss in 3 months, intra-muscular quinine osteomyelitis/Gluteal 77/2018 abscess (Streptococcus injection (Malaria) France pneumoniae) surgically drained/-2 months Osteomyelitis, psoas Estoppey O M/ Surgical repair of an inguinal hernia abscess, sacroiliitis/ 67/1997 hernia surgery/10 Switzerland days Right breast abscess/ Werno AM F/ Right total mastectomy and mastectomy and transverse rectus abdominis 53/2004 muscle flap reconstruction for a rectus abdominis New multicentric ductal carcinoma in muscle flap Zealand reconstruction/1 situ month Left breast abscess/ Werno AM F/ Left breast abscess, granulomatous mastitis No/33/2004 New Zealand Bilateral breast Levin B. F/56/ Bilateral breast reduction surgery infections/breast 2008 reduction surgery/1 Australia month Bradbury RS F/ Recurrent breast abscess, history Breast abscess/-/of puerperal mastitis, mammary 44/2011 duct ectasia Australia Bilateral breast reduction Bilateral breast Kritikos A F/ surgery abscess/breast 37/2015 reduction surgery/7 Switzerland weeks Panagea S F/ Bilateral breast reduction Bilateral breast 40/2005 UK surgery abscess/breast reduction surgery/3 weeks Unilateral breast di Summa PG Bilateral breast reduction abscess/breast F/36/2015 surgery/tobacco smoker reduction surgery/3 Austria weeks Splenic abscess/ Dunne WM M/ Placement of four coronary coronary bypass bypass grafts, malaria. during 61/1986 surgery/8 weeks World War II USA LoureiroAmigo J F/ 85/2016 Spain Vetromile F M/ 67/2001 Argentina
Permanent pacemaker implantation, HA, DM, bioprosthetic aortic valve, weight loss. Prosthetic mitral valve, weight loss
Vohara A M/ 79/1998 USA
Cardiac catheterization with angioplasty. DBT. AHT
Bentorki AA M/26/2013 Algeria
Depressive episode, seborrheic dermatitis associated with maceration of the skin at the level of inguinal fold. Intraarticular (hip) glucocorticoid treatment, steoarthritis, overweight, weight loss (5 kg), ynphoma.
Million M F/ 78/2008 France
NR/208/NR/37.6 C/Aortic Prosthetic valve Favorable vegetation þ BC/POS replacement/AMC, PEN þ GEN, PEN þ RIF, CIP þ RIF/ 12 weeks NR/86/14 109/38.3 C/ Yes/ Fatal BC/POS DAP þ AMP þ CRO, PEN/13 days
Co-infection
Identification
No
NR
No
MALDI-TOF MS
NR/NR/NR/NR, fever/BC/ POS
-/VAN þ GEN þ RIF/ Fatal 99 days
No
NR
NR (obese)/68/NR/ afebrile/Two vertebral discs/NEG
Surgery/AMX þ RIF/ Favorable 6 weeks
No
NR
NR/NR/16.6 109/ afebrile/abscess, bone biopsy, BC/POS
Surgery-/CIP þ AC/- Favorable
No
NR/NR/12.0 109/ afebrile/abscess/NR
Drainage/ flucloxacillin, penicillin/NR
Favorable
No
API Coryne Conventional 16S rRNA sequencing
NR/103/12.9 109/ 37.2 C/abscess, wound, tissue/NR
Drainage/AMC, doxycycline
No Low-grade inflammation. Mastectomy?
API Coryne Conventional 16S rRNA sequencing
NR/7.1/10.3 109/NR/ necrosic area (nipples) and deep swab from both breasts/NR NR/NR/NR/NR/breast tissue/NR
Debridement/MEM, Favorable MOX augmentin/~8 weeks
No
Surgery/ND/-
Favorable
No
API Coryne 16S rRNA sequencing
Favorable
No
MALDI-TOF MS
NR/135/22.5 109/ 37.2 C/abscess/NEG
Drainage/FLU þ BEN Favorable PEN, AMC/~5 weeks
No
API Coryne Conventional 16S rRNA sequencing
NR/6/11 109/afebrile/ abscess/NR
Drainage/AMC, AMX/~6 week
Favorable
No
NR
Favorable
No
Surgery/NR/-
Favorable
No
Conventional Gas chromatographic analysis of volatile acids NR
Drainage/CIP, MTZ þ CFZ, CFX/2 weeks
Favorable
No
API Coryne Conventional
Favorable
No
Conventional
NR/16/9.1 109/afebrile/ -/AMC, AMX/6 abscess/NR weeks
NR/NR/5.6 109/38.0 C/ Surgery/NR/splenic abscess/NEG
NR/NR/13.1 109/ Splenic abscess/ cardiac 38.9 C/splenic abscess/ catheterization/6 NEG weeks Abscess of the root of NR/26/11.1 109/ the thigh/-/afebrile/abscess/NR
Septic arthritis of the 30.5/185e218/6.5 109/ Surgery/CFZ þ RIF/ hip/-/12 weeks 38.5 C/joint fluid þ acetabulum þ BC/ POS
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Table 1 (continued ) Author Gender/Age (year)/ Publication date Country
Comorbities/Predisposing condition
Site/Previous surgery/ BMI/CRP/WC/ Outcome Surgery, drainage Length from surgery Temperature ( C) or treatment/AM to infection fever/Isolation source/BC treatment/Length of AM treatment
Wang TKF M/ 70/2002 Hong Kong
Hemorrhoidectomy. Hepatitis B carrier, chronic liver failure, ascites, splenomegaly, testicular atrophy, primary skin and soft tissue lesion Breast cancer, breast surgery
Perianal subcutaneous abscess/ Hemorrhoidectomy/ 17 month Surgical wound infection, necrotizing infection/NR/-
Series of 11 cases: Tena D 1-F/43/ 2019 Spain 2-F/66/2019 No
NR/NR/NR/NR/breast exudate/NR
NR/NR/NR/NR/Breast abscess/NR Breast abscess/No/NR/NR/NR/NR/Breast abscess/NR Breast abscess, NR/NR/NR/NR/Breast necrotizing infection/ abscess, aspirate/NR No/-
No
4-F/49/2019
Depression
5-F/46/2019
No
Breast abscess/No/-
6-F/23/2019
No
Breast abscess/No/-
7-F/47/2019
Smoking
Breast abscess/No/-
8-M/39/2019
Smoking, dyslipemia
9-M/33/019
Smoking, hidradenitis (axilla)
Infected sebaceous cyst (retroauricular)/ No/Axillary abscess/No/-
10-M/77/2019 AH, COPD, IHD, CRF, abdominal Infected seroma surgery (abdominal)/ abdominal surgery/11-F/51/2019 DM, obesity, hidradenitis Suppurative hidradenitis (pubis)/ No/Abdominal wall, Janvier F F/46/ Prosthetic parietoplasty/ 2013 France abdominal wall eventration 14 intra-peritoneal abscess/prosthetic months after an abdominal parietoplasty/2 hysterectomy months Present case F/ Hysterectomy. HIVþ, follicular Intra-peritoneal lymphoma, DBT, steatosis. collections/ 47 Abdominal Argentina hysterectomy 96 h.
Identification
Favorable
No
API Coryne Conventional
Debridement/AMC, Favorable VAN LNZ/17 days
No
MALDI-TOF MS
Drainage/CLIN/15 days Drainage/AMC/13 days Drainage, debridment/ IMP,Cefditoren/15 days Drainage/AMC/7 days Drainage/AMC/7 days No (spontaneous dranage)/LEV,CLIN/ 22 days Drainage/AMC/7 days
Finegoldia MALDI-TOF MS magna Finegoldia MALDI-TOF MS magna Peptoniphilus MALDI-TOF MS harei
NR/NR/7.5 109 Drainage/ (baseline level 4.9 109) AMP þ CLOX/1 week afebrile/abscess/NR
Breast abscess/No/-
3-F/41/2019
Co-infection
NR/NR/NR/NR/Breast abscess/NR NR/NR/NR/NR/Breast abscess/NR NR/NR/NR/NR/Breast abscess/NR NR/NR/NR/NR/abscess sebaceous cyst retroauricular/NR NR/NR/NR/NR/axillary abscess/NR NR/NR/NR/NR/seroma/ NR
Favorable Favorable Recurrence
Favorable
No
MALDI-TOF MS
Favorable
No
MALDI-TOF MS
Recurrence
Actinotignum MALDI-TOF MS shaalii
Recurrence
No
MALDI-TOF MS
Drainage/AMC/10 days No/AMC/10 days
Favorable
No
MALDI-TOF MS
Recurrence
No
MALDI-TOF MS
No/CIP, CLIN NR
Unknown
Actinomyces neuii
MALDI-TOF MS
Surgery/AMC/4 weeks
Favorable
No
MALDI_TOF MS API Coryne 16S rRNA sequencing
38.7/NR/8.5x109/38.5 C/ Surgery/VAN þ IMP, Favorable TAZ, AC/~555 3 intra-peritoneal weeks collections/NEG
No
MALDI-TOF MS Conventional 16S rRNA sequencing
NR (obese)/NR/NR/NR/ exudate (suppurative hidradenitis)/NR 31.2/162/13x109/37 C/ intra-peritoneal collections/NEG
Note: WBC: white blood cells. (N x109/L). BC: Blood culture. Blood culture: negative (NEG)/positive (POS). BMI: body mass index (kg/m2). CRP: C reactive protein (mg/L). AM treatment: antimicrobial treatment. Length AM treatment. AH: arterial hypertension. DM: diabetes mellitus. NA: not available. AMX: amoxicillin. BEN PEN: benzyl penicillin. AMC: amoxicillin-clavulanic acid. FLU: flucloxacillin. CLIN: clindamycin. RFA: rifampicin. PP: phenoxymethylpenicillin. CFZ: cefazolin. CFX: cephalexin. CLOX: cloxacillin. MEM: meropenem. NR: not reported. COPD: chronic obstructive pulmonary disease; IHD: ischemic heart disease; CRF: chronic renal failure.
treated successfully with a combination of surgery and antibiotics. A consideration regarding surgery that should be taking into account is that obesity rates are rising worldwide, and some authors have suggested that prophylactic cefazolin dose should be doubled for obese patients [50]. Also, specific preoperative topical skin preparation should also be considered to diminish the colonization [51]. The true incidence of Cutibacterium infections may be underestimated because of its categorization as a low virulence microorganism, interpretation as common skin colonizer and insufficient culture time [17,23,26,32,34,52,53]. However, C. avidum may be isolated from blood in serious entities such as: infective endocarditis [32e34], osteomyelitis [20,29] and septic arthritis [35]. Although the presence of oxygen reduces the growth rate for all Cutibacterium spp., C. avidum is the best species at adapting its growth to aerobic conditions [26,54,55]. Nevertheless, some authors have described cases of C. avidum bacteremia, in which only
the anaerobic bottles yielded the microorganism [34. 35]. Blood cultures in our case were negative despite including anaerobic and aerobic bottles. Like most laboratories we routinely incubate the blood cultures for five days, but it would be advisable to extend the incubation culture time in these cases [32-34,52,53]. Cutibacterium species is seldom isolated from true infections from abdominal origin in adults [55] and never in children [56,57]. Unlike C. acnes, C. avidum was not an agent of contamination in some cases [15]. Fortunately, in our case, C. avidum grew in pure culture in three relevant samples obtain by surgical drainage. This fact was reported in several cases, which greatly facilitated the adjudication of a pathogenic role in the assessed entity [14,19,21e23,25,27e31]. According to the literature an aerotolerant gram-positive rod that showed creamy colonies with a wide zone of beta-hemolysis in aerobic and anaerobic atmosphere is suggestive of C. avidum [17,19,25]. Although C. avidum was reported to be identified using
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automated system VITEK 2 (bioMerieux, Marcy L'Etoile, France) [18] and API Coryne strip [25e28], some reports have demonstrated problems with VITEK 2 (Propionibacterium granulosum (91%)/Propionibacterium propionicus (88%), API Coryne system (Propionibacterium propionicus/avidum) [19] and no identification with VITEK MS [58]. Like other authors, we correctly identify C. avidum by phenotypic methods and MALDI- TOF MS. This method have demonstrated to be accurate [12,14,19,23,24,34] including by the Andromas matrix-assisted laser desorption ionization-time of flight mass spectrometry system [59]. Similar to other cases, the identification of our isolate as Propionibacterium avidum was confirmed by 16s rRNA sequencing [14, 25 26]. The microorganism can show the same homology percentage with Propionibacterium propionicum. However, biochemical tests can help to achieve the correct identification [21]. In general C. avidum is susceptible to penicillin and other blactams, clindamycin, rifampin, moxifloxacin, vancomycin and naturally resistant to metronidazole [14, 18, 19, 24. 25, 27, 28, 30, 32, 34, 35, 60, 61]. However, in our and some other cases, C. avidum was resistant to clindamycin [16e18,23,36]. This is very important because some guidelines and authors have used it for treatment and/or prophylaxis [14,15,18,24,62e64]. 4. Conclusions To our knowledge, this is the first documented case of nonprosthetic intra-peritoneal infection by a clindamycin resistant C. avidum and the second one in a female patient with obesity and previous abdominal surgical intervention. C. avidum should be suspected as the etiologic agent in clinically relevant samples with pure culture, especially from obese patients with surgical incision site close to areas colonized with the bacteria and despite the absence of foreign material and other comorbidities. C. avidum was rapidly identified by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS). For the resolution, both, antimicrobial treatment and surgical intervention may be required. Although rare, monitoring antibiotic resistance in members of Cutibacterium spp. is necessary because clindamycin could be a therapeutic option. References [1] M. Rosenthal, D. Goldberg, A. Aiello, E. Larson, B. Foxman, Skin microbiota: microbial community structure and its potential association with health and disease, Infect. Genet. Evol. 11 (2011) 839e848, https://doi:10.1016/ j.meegid.2011.03.022. [2] G.J. Christensen, H. Bruggemann, Bacterial skin commensals and their role as host guardians, Benef. Microbes 5 (2014) 201e215, https://doi.org/10.3920/ BM2012.0062. [3] K. Szabo, L. Erdei, B.S. Bolla, G. Tax, T. Biro, L. Kemeny, Factors shaping the composition of the cutaneous microbiota, Br. J. Dermatol. 176 (2017) 344e351. https://doi:10.1111/bjd.14967. [4] Y. Achermann, E.J.C. Goldstein, T. Coenye, M.E. Shirtliff, Propionibacterium acnes: from commensal to opportunistic biofilm-associated implant pathogen, Clin. Microbiol. Rev. 27 (2014) 419e440. https://doi.org/10.1128/CMR.0009213. [5] H.C. Douglas, S.E. Gunter, The taxonomic position of Corynebacterium acnes, J. Bacteriol. 52 (1946) 15e23. [6] G.G. Aubin, P. Bemer, S. Kambarev, N.B. Patel, O. Lemenand, J. Caillon, P.A. Lawson, S. Corvec, Propionibacterium namnetense sp. nov., isolated from a human bone infection, Int. J. Syst. Evol. Microbiol. 66 (2016) 3393e3399, 2016, https://doi.org/10.1099/ijsem.0.001204. [7] S.M. Butler-Wu, D.J. Sengupta, W. Kittichotirat, F.A. Matsen, R.E. Bumgarner, Genome sequence of a novel species, Propionibacterium humerusii. J. Bacteriol. 193 (2011) 3678. https://doi.org/10.1128/JB.05036-11. [8] C.F.P. Scholz, M. Kilian, The natural history of cutaneous propionibacteria, and reclassification of selected species within the genus Propionibacterium to the proposed novel genera Acidipropionibacterium gen. nov., Cutibacterium gen. nov. and Pseudopropionibacterium gen. nov, Int. J. Syst. Evol. Microbiol. 66 (2016) 4422e4432. https://doi.org/10.1099/ijsem.0.001367. [9] N.K.M. Nordstrom, W.C. Noble, Colonization of the axilla by Propionibacterium avidum in relation to age, Appl. Environ. Microbiol. 47 (1984) 1360e1362.
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