Case Report
J Bacteriol Mycol. 2021; 8(2): 1169.
Blood Stream Infection Caused by Achromobacter Xylosoxidans: Case Report and Review of Literature
Ucciferri C1,2, Caiazzo L1, Pontolillo M1, Vignale F1, Vecchiet J1 and Falasca K1*
1Clinic of Infectious Diseases, “G. D’Annunzio” University Chieti-Pescara, Italy
2Department of Medicine and Health Sciences, University of Molise, Italy
*Corresponding author: Katia Falasca, Department of Medicine and Science of Aging, “G. D’Annunzio” University Chieti-Pescara, Clinic of Infectious Diseases, Via dei Vestini, 66100 Chieti, Italy
Received: March 16, 2021; Accepted: April 09, 2021; Published: April 16, 2021
Abstract
Achromobacter xylosoxidans also known as Alcaligenes xylosoxidans is a Gram-negative bacillus found in water and soil. It is an uncommon cause of infection in immunocompetent and immunocompromised patients. This report describes a 47-year-old female diagnosed with common variable immunodeficiency with Achromobacter xylosoxidans positive blood cultures and acquired resistance to piperacillin/tazobactam during treatment. This bacterium can cause pathologies with high mortality, due to its ability to create biofilms and its particular pattern of susceptibility to antibiotics. Choosing the right antibiotic is critical because they are highly resistant to antibiotics. Due to the presence of few antibiotics with bactericidal activity, the risk of empirical treatment failure is high and therefore a correct understanding of this rare but fatal disease is important to obtain the best chance of success. For this reason we finally carried out a literature review.
Keywords: Achromobacter spp; Antibiotic resistance; Bacteremias; Common variable; Alcaligenes, immunodeficiency; Biofilm; Vascular catheter
Introduction
Achromobacter xylosoxidans ss xylosoxidans (formerly Alcaligenes xylosoxidans ss xylosoxidans) is an aerobic, catalase and oxidase positive, non-fermenting gram-negative peritrichous rod; it is found usually in aqueous environments but it is still a human host, occasionally present in the skin and gastrointestinal tract [1]. A. xylosoxidans is considered an opportunistic pathogen, causing infection in immunocompromised hosts [1].
Its pathological role has well defined in literature, among dialysis patients, either in hemodialysis or in peritoneal dyalisis [2-4].
While it has been adequately outlined, until now, that A. xylosoxidans can cause nosocomial catheter-related bloodstream infection and bacteremias (outbreak or single cases), as far as we know few reports exist that describe catheter-related bloodstream infection neither in dialysis nor in oncologic patients [5].
We describe a clinical case of a patient, afflicted by common variable immunodeficiency, ulcerative colitis and coeliac disease, with a catheter-related blood stream infection sustained by A. xylosoxidans and review another cases in literature.
Case Presentation
A 47-year-old woman was admitted to our Infectious diseases ward due to a high-grade fever, chills and weakness lasting for six days. This young woman has suffered from recurring episodes of low respiratory and gastrointestinal tract infections since her childhood. At 27 years of age she was diagnosed with Common variable immunodeficiency. She had total Ig level below 100 mg/dl and a very low level of B lymphocyte, so, started a treatment with a cycle of iv Immunoglobulin every 21 days. During her adulthood, she was diagnosed with Ulcerative colitis and Coeliac disease, that lead her to important malabsorption and weight loss. Given the fact that, no matter that medication, she had been progressing to lose weight and report gastrointestinal symptoms, in February 2014, the Medical equipe she was in charge to decided to propose her the implantation of a Groshing, a vascular catheter, for total parenteral nutrition and albumin infusion. At the end of 2014 she had been hospitalized twice, first for an episode of candidaemia and then for a bacteremia from S. capitis. In 2015, a third hospital stay, due to a new Bloodstream Infection (BSI), lead to the substitution of the vascular catheter with a new one: always a Groshong. The patient had been assisted in home care regimen, with a daily visit from a professional nurse that took care of the central venous access, disinfecting it before every use. However, she occasionally needed an hospital admission, to treat and cure episodes of gastrointestinal infection. On 2017 October 25th, she was admitted to our Infectious Disease ward for a sudden appearance of high grade fever and shivering. She noticed that the elevation of the body temperature was related to the use of the Groshong catheter. At the admission, her general conditions were good. She weighted 44 kg. Blood pressure was 90/60 mmHg, heart rate was 120/min, body temperature was 39°C. Laboratory findings on admissions are shown in Table 1. The Chest x-ray was normal. First of all, peripheral and Central Venous Catheters (CVC) blood cultures were performed, then we started an empiric antimicrobial therapy with Piperacillin/ tazobactam. On the third day of hospital stay, we observed a new rise of body temperature related to the use of the Groshong catheter. We took once again peripheral and CVC blood cultures. On the seventh day of admission, we performed an echocardiography that was completely normal and ruled out vegetations either of the valve or of the Groshong. A. xylosoxidans was isolated from every single culture performed both from peripheral vein and Groshong catheter. The first series of blood cultures taken showed a bacteremia from A. xylosoxidans sensible to Piperacillin/tazobactam (Table 2), so we continued to treat her with Piperacillin/tazobactam. However, she presented again a raise in body temperature at day 10th of hospital stay and in the meantime the cultures taken on the 3rd day of admission exhibited a change in bacterial sensitivity (Table 2). While the first blood cultures showed A.xylosoxidans sensible to Piperacillin/ tazobactam, the second series of cultures revealed A.xylosoxidans resistant to Piperacillin/tazobactam. It seemed that the bacteria have developed resistance during the antibiotic treatment. So, we performed a new series of blood cultures and change the antimicrobial, shifting to Meropenem 3g/day. Even though our patient did not improve so much, continuing to present sudden episodes of malaise. We decided to perform again a Transthoracic echocardiography. The exam showed an endocarditis of the vascular catheter, reinforcing the urgent need to remove it. A regimen of enoxaparin 0.4UI twice daily was added, with resolution of the episodes of malaise reported by the patient. Once again, all the blood cultures showed A.xylosoxidans strain resistant to Piperacillin/tazobactam. Eventually we continued the antimicrobial until the transfer of the patient to the Hospital in which she substituted the catheter with a new one.
Parameter
Patient 's value
Reference range
Haemoglobin
12.2 g/dL
13.0-16.0
White blood cells
3.810 cells/uL
4.000-10.000
Neutrophils
2.570 cells/uL
2.100-7.100
Lymphocytes
1.140 cells/uL
1.100-3.000
Platelets
93.000/mmc
150.000-450.000
INR
1.16
0.950-1.150
C-reactive Protein
14.70 mg/dL
0.00-0.50
Procalcitonin
21.80 ng/ml
0.00-0.50
Table 1: Laboratory results at the Hospital admission.
Day 0, before antibiotic initiation
Day 3, during empirical antibiotic therapy
Antibiotic
A.xylosoxidans
Amoxicillin/clavulanic acid
I 8.000
Amoxicillin/clavulanic acid
Piperacillin/tazobactam
S <= 4 mg/L
Piperacillin/tazobactam
R >= 64.000
Imipenem
S 1.000
Imipenem
S 1.000
Meropenem
S <= 0.25 mg/L
Meropenem
S <= 0.25 mg/L
Cefotaxime
R >= 32.000
Cefotaxime
R >= 32.000
Ceftazidime
S 2
Ceftazidime
S 4
Gentamicin
R >= 8.000
Gentamicin
R >= 8.000
Amikacina
R >= 32.000
Amikacin
R >= 32.000
Ciprofloxacin
R >= 2.000
Ciprofloxacin
R >= 2.000
Table 2: Blood cultures taken at the admission and on 3rd day of admission, both by peripheral and central vascular catheter.
To conduct the review of literature we search PubMed using the following lists of terms: “bacteremia AND xylodoxidans”, “catheter AND xylodoxidans”, catheter AND achromobacter xylodoxidans bacteremia”, “intravascular catheter AND xylodoxidans bacteremia”, “central venous catheter AND achromobacter xylodoxidans bacteremia”, “endocarditis AND xylodoxidans”, “common variable immunodeficiency AND xylodoxidans”, “groshong catheter AND xylodoxidans”.
We included all the articles fully written in english reporting: bacteremia with or without a secondary localization of infection, endocarditis and rare cases of localized non-bacteremic infection. We decided to focalize only on adult non cystic-fibrosis patients, therefore we excluded papers in cystic-fibrosis (Table 3). Also we exclude studies reporting only neonatal or infant. We included single case reports and review of literature.
Author/Publication
Year of publication
Cases
Cured
Dead
Unknown Outcome
Lofgren et al.
1981
1
0
1
0
Duggan et al.
1996
77
54
23
0
Martino et al.
1996
1
1
Knippschild et al.
1996
11
11
0
0
Manfredi et al.
1997
7
7
0
0
Wetkamp et al.
2000
1
1
0
0
Gomez-cerezo et al.
2003
54
46
8
0
Tsay RW et al.
2004
12
10
2
0
Shie et al.
2004
40
21
19
0
Aisenberg et al.
2004
46
39
7
0
Ahn et al.
2005
1
1
0
0
Tena et al.
2005
4
4
0
0
Yilmaz et al.
2006
1
1
0
0
Siebor et al.
2007
12
0
0
12
Nanuashvili et al.
2007
1
1
0
0
Van Hals et al.
2008
1
1
0
0
Moon J. Kim et al.
2008
12
12
0
0
Malek-Marin et al.
2009
1
1
0
0
Teng et al.
2009
1
1
0
0
Ahmed et al.
2009
1
0
1
0
Storey et al.
2010
1
0
1
0
Derber et al.
2011
1
1
0
0
Turgutalp et al.
2011
1
0
1
0
Beherens-Muller et al.
2012
9
9
0
0
Tokuyasu et al.
2012
11
4
7
0
Sawant et al.
2013
1
1
0
0
Lee et al.
2014
1
0
1
0
Rafael et al.
2014
1
1
0
0
Dai et al.
2015
1
0
1
0
Tugcu et al.
2015
1
1
0
0
Patel et al.
2015
1
0
1
0
Raghuraman et al.
2015
1
0
1
0
Liu et al.
2016
15
10
5
0
Kumar et al.
2017
1
0
0
1
Al jasser et al.
2017
1
0
1
0
Rodrigues et al.
2017
1
1
0
0
Donderski et al.
2018
1
1
0
0
Jananthanan et al.
2019
1
1
0
0
Xiaoxia et al. 2019
2019
32
0
32
Total
367
243
79
45
Table 3: Articles included in the review and number of cases.
Discussion
A. xylosoxidans is a very uncommon human pathogen. As well described in literature, infection from these bacteria are commonly seen in immunosuppressed patients [6-8].
We have considered 367 events reported in literature from 1996 to 2019. Within these cases, we report 243 cases (66.21%) with favorable outcome and 79 (21.52%) deaths. There were 45 cases with unknown outcome.
232 cases were related to a nosocomial infection, emphasizing that A. xylodoxidans is an opportunistic pathogen that rarely causes community diseases [4,9,10].
On the other hand, Aisenberg pointed out a conspicuously low frequency of nosocomial infections caused by A. xylodoxidans [7]. Also Shie et al, in their series of clinical bacteremias from A. xylodoxidans in Taiwan, exhibited how more than a quarter of cases were community acquired [8].
The clinical syndromes are mainly represented by bacteriemia (36.2%); followed by vascular catheter infection (25%), pneumonia (11.7%), endocarditis (6.8%), UTI (2.4%), SSTI (1.9%) (Table 4).
Clinical Syndrome
Number of cases
Bacteremia
133
Catheter-related bacteremia
92
Endocarditis
25
Pneumonia
43
UTI
9
SSTI
7
Meningitis
4
Surgical wound infection
5
Septic arhritis
3
GI/BI tract infection
7
Empyema
1
Renal stones
1
Sinusitis
1
Other
4
Unknown
10
Table 4: Clinical syndromes.
We have observed that 99 patient had a venous catheter. This is a risk factor especially for immunosuppressed people (who often have these devices to infuse chemotherapy or nutrition). Also, on these devices A.xyodosidans easily creates biofilms. Associated clinical syndromes can be simple catheter infections, but also endocarditis. The associated symptoms are generally subtle and nuanced, with intermittent and long lasting fever. In his work, Duggan identified, for 26 patients, contaminated solution or hospital equipment as the source of infection [11]. A particular cluster of infections resides in patients on hemodialysis or in peritoneal dialysis [2-4]. A series of report show that A. xylosoxidans could be an opportunistic pathogen in dialysis setting, colonizing fluids (didecyldimethylammonium chloride, saline, chlorhexidine and deionized water in hemodialysis systems) and health care workers’ hands [11,12].
Furthermore, in an outbreak in a hemodialysis unit, Tena characterized specifically the source of infection, isolating the causative pathogen in an atomizer containing diluted 2.5% chlorhexidine [9].
In our review the most frequent underlying conditions are neoplasms, that are present in almost half of cases (46.8%); of which 38.5% solid tumors and 61.5% hematological malignancies) (Table 5).
Comorbid condition
Number of cases
Solid tumor
66
Haematologic malignancies
105
Major surgery
23
Diabetes
45
HIV
13
CKD/ESRD
35
Intravascular catheter
99
COPD
19
Cardiovascular disease
57
Neutropenia
52
High dose steroids
23
Chemotherapy
16
Liver Cirrhosis
9
Abbreviations: AUC: Area Under the Curve; LS: Least Squares; NE: Not Estimable
Table 5: Most common comorbidities reported.
Duggan et al. too, reported as the most frequent underlying condition malignancies (23%), solid or hematologic, followed by cardiovascular diseases (16%), renal failure (6%) and diabetes (3%) [13]. These data has been confirmed in subsequent studies, especially reinforcing the major role of Neoplasms as risk factor [7,8,10,13-24].
Even if, in our records, other conditions have been described as predisposing to infection by A. xylodoxidans, like diabetes (12.2%), CV disease (15.5%); neutropenia (14.1%), chemotherapy (4.3%); high dose steroids therapy (6.2%), HIV (3.5%), renal failure (9.5%), COPD (5.1%); liver cirrhosis (2.4%), ours is the first report of BSI in a patient with common variable immunodeficiency . In our scenario, the patient had not been admitted to hospital during the previous three months, but a professional nurse, who provided the management of the Groshong catheter, assisted her in a daily home care regimen. Therefore, we cannot be certain about the community origin of the infection.
On the contrary, the catheter infection has been indirectly proved by the sudden comparison of fever with every use of the Groshong and by the positivity of all the blood cultures performed, from either the catheter or peripheral vein. We can suppose that the aqueous environment and the glucose contained in the nutrient solution facilitated infections with A. xylosoxidans. Another element that confirmed the infection of the catheter was the presence of the endocarditis. In literature, the infective endocarditis sustained by A.xylosoxidans are quite rare as it is the demonstration of the vegetations directly on the Groshong catheter [3,13,20,25-32].
A particular element of interest consists in the antimicrobial susceptibility pattern. In works collected, A.xylosoxidans is often resistant to aminoglycosides (231 cases). Only Weitkamp et al. in 1999 reports that all isolates were susceptible to amikacin and tobramycin [16].
Regardless of the type of molecule, quinolones exhibit a variable sensitivity model. This uniform resistance observed among aminoglycosides is due to an effux pumps33 and fluoroquinolone seems to be secondary to alteration of the DNA gyrase or defective transport of the agents through the cell envelope [34]. A.xylodoxidans, is frequently resistant to cephalosporins, with exception for cefriaxone which is effective in most cases. Among beta-lactams, Piperacillin/tazobactam is the most active against A.xylodoxidans, while carbapenems are always effective.
In our case, the first series of blood cultures (Table 2), taken at hospitalization, demonstrates a pathogen sensitive to piperacillin/ tazobactam (the empirical treatment started at his hospitalization), while the culture was repeated on day 3 of hospitalization. hospital shows resistance to piperacillin/tazobactam. In literature, Sawant et al. showed a shift in the sensitivity pattern toward piperacillin/ tazobactam [32]. The rapid switch of sensitivity in our case and the data from Sawant, suggest that the A.xylodoxidans has the ability to quickly render piperacillin/tazobactam ineffective, making the choice of this therapeutic option a choice at risk of therapeutic failure. Also in this case A.xylodoxidans, caused endocarditis from biofilm on the right ventricular pacemaker lead.
As outlined in a recent review by the group of Didelot, the acquisition of a resistance profile within the host is not uncommon for bacterial pathogens, and several mechanisms have been listed to mediate this phenomenon, most notably horizontal gene transfer, hitchhiking, heteroresistance and selective sweep [35].
A.xylosoxidans in particular, shows genomic and phenotypic features that make it a reservoir for transferable elements, like plasmids and integrons, carrying antimicrobial resistance-associated genes, as described in the paper by Traglia et al. [36].
The resistance to Piperacillin/tazobactam has been rarely reported to date; browsing literature, we have found a small percentage of resistance reported in the case series of Shie et al. [8].
Probably the presence of cultures with different antibiotic resistance profiles is due to the presence of biofilm in the catheter. In medical device-related infections, the subsequent failure of antimicrobial therapy regularly requires the removal of the colonized biomaterial, leading to substantial morbidity and mortality. Antimicrobial concentrations sufficient to destroy planktonic organisms are generally inadequate to destroy biofilm organisms, especially those deep within the biofilm, potentially selecting for resistant subpopulations [37]. Biofilm physiology contributes to tolerance to antimicrobial agent, so biofilm bacteria are physiologically distinct from planktonic bacteria, expressing specific protective factor, such as multidrug efflux pumps and stress response regulation [38]. A. xylosoxidans has been shown to form robust biofilms both in vivo and in vitro, improving the intrinsic resistance to biofilm cell [32,39].
Conclusion
Our review show that A. xylosoxidans is a troublesome human pathogen causing nosocomial or community related, hard to treat, infection in immunocompromise patient. The most frequent underlying conditions are represented by malignancies, immunodepression, or the presence of vascular catheters. Due to the high mortality of pathologies caused by A. xylosoxidans and the presence of few antibiotics with bactericidal activity, the risk of treatment failure is high (especially in empirical therapy). Furthermore, the particularity of this germ and its ability to create biofilms can render antibiotic therapy ineffective, requiring the mechanical removal of the source of infection to be considered.
Acknowledgment
We are in debt to Dr. A. Gambi and Dr A. Occhionero for helping us.
ICMJE Statement: CL and CU contributed to the writing the manuscript; MP and FV was responsible for the organization and coordination of the trial. JV and FK contributed to the management and analysis of data.
All authors contributed to the writing of the final manuscript.
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