Microbiological profiles and antibiotic resistance of periprosthetic joint infection after hip replacement in patients with fracture or non-fracture: A comparative study

Abstract

BACKGROUND:

Periprosthetic joint infection (PJI) is one of the worst complications following total joint arthroplasty (TJA). Unfortunately, effective prevention strategies to reduce the burden of PJI have not been fully determined in hip replacement patients with fracture and non-fracture.

OBJECTIVE:

This study aimed to analyze and compare the demographic characteristics, microbiological profiles and antibiotic resistance of PJI after hip replacement between patients with fracture and non-fracture.

METHODS:

We retrospectively analyzed the data of 132 patients who treated PJI. There were divided into two groups: non-fracture group (64 patients infected after hip replacement for fracture) and non-fracture group (68 patients infected after hip replacement for non-fracture). Microorganisms were obtained from the synovial fluid and infected necrotic tissue in the joint capsule, medullary cavity, or acetabulum in all patients, and microbiological profiles and antibiotic resistance were evaluated.

RESULTS:

Coagulase-negative staphylococci (CoNS) were the most common pathogenic microorganisms in all patients. Methicillin-resistant Staphylococcus (MRS) accounted for 25% in all pathogenic microbes. Staphylococci showed high drug resistance rates to clindamycin, levofloxacin, and all of the first- and second-generation cephalosporins. MRS isolates in non-fracture group had higher drug resistance rates to clindamycin and levofloxacin than than those in fracture group. Gram-negative bacilli (GNB) showed high drug resistance rates to Aztreonam, gentamicin and all of the third- and fourth-generation cephalosporins. Furthermore, GNB isolates in the non-fracture group showed higher resistance rates to gentamicin and all of the third- and fourth-generation cephalosporins.

CONCLUSIONS:

MRS isolates in the non-fracture group showed higher drug resistance rates to clindamycin and levofloxacin, and GNB isolates in non-fracture group showed higher drug resistance rates to gentamicin and all of the third- and fourth-generation cephalosporins.

Keywords

Periprosthetic joint infection hip replacement fracture microbiological profiles antibiotic resistance

1. Introduction

Periprosthetic joint infection (PJI) is a catastrophic complication after joint replacement that seriously affects limb function and therapeutic effects [1]. Highly accompanied by huge physical, psychological and economic burdens, it has become a research focus of orthopedic surgeons at home and abroad in recent years [2]. Meanwhile, PJI is also one of the most challenging problems for orthopedic surgeons in clinical practice. Although technological advances, strict aseptic techniques and various precautions have reduced the incidence of PJI, the actual number of PJI cases is increasing in China as a result of the increasing cases of joint replacement [3, 4, 5]. Therefore, it is critical to identify the pathogen and treat PJI with targeted antibiotic therapy.

Often, PJI results in multiple operations, prolonged use of antibiotics, extensive utilization of medical resources, and substantial social, economic, or even psychological impacts on the patients [6, 7, 8]. The microorganisms that cause PJI vary and different microbiological profiles will lead to different drug resistance, thereby affecting the treatment outcomes of diseases [9, 10, 11]. PJI may occur after hip replacement due to hip fracture or diseases that include femoral head necrosis, developmental dysplasia of the hip (DDH), tumors, tuberculosis and others [12, 13, 14, 15]. However, the microbiological profiles and drug resistance of PJI after hip replacement for fracture and non-fracture patients remain unclear. Therefore, the purpose of this study was to analyze and compare the demographic characteristics, microbiological profiles and antibiotic resistances of PJI after hip replacement patients with fracture or non-fracture.

2. Patients and methods

2.1 Patients

Between January 2001 and January 2016, a total of 187 patients could be diagnosed with PJI in Chinese PLA General Hospital, Beijing, China, according to the criteria. Due to incomplete clinical data, 55 cases were excluded, and a final study cohort size of 132 patients with PJI was obtained in this retrospective study. They had undergone initial hip replacement before coming to our hospital for treatment. Patients were divided into fracture (64 patients) and non-fracture (68 patients) groups according to the reason of infection for hip replacement. This study was approved by the Ethics Committee of The First Medical Center, Chinese PLA General Hospital (No. 20200618012).

Inclusion criteria: (1) PJI was diagnosed in accordance with the criteria developed by the International Consensus Meeting in Philadelphia [16]; (2) PJI was considered if one of the primary criteria were met, including the presence of a fistula communicating with the prosthesis and the same pathogen isolated at least twice from separate samples of the affected prosthetic joint; (3) PJI was also considered if at least three of the six secondary criteria were met, including elevated serum erythrocyte sedimentation rate (ESR) and serum C-reactive protein (CRP) level, elevated white blood cell count (WBC) in the synovial fluid (SF), elevated percentage of SF neutrophils, the presence of pus in the affected joint, isolation of microorganisms from periprosthetic tissues or fluids and five or more neutrophils per high power field.

Exclusion criteria: (1) patients undergoing non-primary joint replacement surgery; (2) patients undergoing joint replacement due to tumor and tuberculosis; (3) patients with primary joint infection; (4) patients with severe heart, liver, lung, kidney and other organ dysfunction; (5) patients with incomplete clinical data.

2.2 Testing and sampling methods of microorganisms

Specimens for culture were obtained from the synovial fluid and infected necrotic tissue in the joint capsule, medullary cavity, or acetabulum. Standard microbiological techniques were used to identify and test the drug susceptibility of isolates in accordance with the methods approved by the Clinical and Laboratory Standards Institute (CLSI). Briefly, the collected specimens were plated on on sabouraud glucose agar and chocolate agar plates and incubated at 25 ${}^{\circ}$ C for 4 weeks for culture of aerobic bacteria, anaerobic bacteria and fungi and to test the drug sensitivity of the isolates. The specimens were incubated in a constant temperature incubator at 37 ${}^{\circ}$ C for 18–24 h before isolation and purification. A sufficient number of pure colonies were obtained with a sterile inoculation loop and 3.0 ml of sterile saline (0.45% to 0.50% NaCl, pH 5.0 to 7.2) was added to prepare a bacterial suspension. Suspensions of gram-positive and gram-negative bacteria were prepared within the range of 0.50 to 0.63 McGill units, and an electronic turbidity metre was used to measure turbidity. The VITEK2 Compact system (BioMerieux, Marcy L’Etoile, France) was used for identification and antimicrobial susceptibility testing of the bacterial suspensions.

2.3 Data collection and statistical analysis

The demographic characteristics, comorbidities, reasons for initial hip replacement, pathogens and drug resistance of all patients were collected. If multiple pathogens were isolated from the same joint at different times, the preoperative or intraoperative results were used in this study. Polymicrobial infection was defined as two or more pathogens were isolated from one periprosthetic tissue or synovial fluid at the same time.

SPSS version 24.0 (SPSS Inc. Chicago, IL, USA) was used for the statistical analysis. Measurement data were expressed as means $\pm$ standard deviation (SD). Count data were expressed as frequency. The chi-square test, Student’s $t$ -test and Fisher’s exact test were used to compare the differences between the two groups. $p\leqslant$ 0.05 was considered statistically significant.

3. Results

3.1 Demographics of patients

There were 64 patients (34 females, 30 males) in the fracture group and 68 patients (31 females, 37 males) in the non-fracture group. The demographic characteristics are shown in Table 1. There was no significant difference in sex between the two groups ( $p=$ 0.387). However, the average age in the fracture group was significantly older than that in the non-fracture group (62.4 $\pm$ 14.8 vs. 54.3 $\pm$ 13.3; $p<$ 0.001). For comorbidities, the proportion of patients with arrhythmias was higher in the fracture group than in the non-fracture group ( $p=$ 0.03). There were no significant differences in hypertension, diabetes, ischemic heart disease (IHD) and chronic obstructive pulmonary disease (COPD) between the two groups ( $p>$ 0.05). Twenty-six patients (17.8%) presented with culture-negative infection, including 11 patients in the fracture group and 15 in the non-fracture group (15.7% vs. 19.7%, $p=$ 0.526).

Table 1
General characteristics in the two groups

Items	Fracture group	Non-fracture group	$p$ value
Number	64	68
Sex
Female	34 (53.1%)	31 (45.6%)	0.387
Male	30 (46.9%)	37 (54.4%)
Mean age	62.4 $\pm$ 14.8	54.3 $\pm$ 13.3	0.001 ${}^{\blacktriangle}$
Comorbidities
Hypertension	12 (18.8%)	13 (19.1%)	0.957
Diabetes	13 (20.3%)	13 (19.1%)	0.863
IHD	7 (10.9%)	4 (5.9%)	0.294
Arrhythmia	6 (9.4%)	0	0.030 ${}^{\blacktriangle}$
COPD	3 (4.7%)	0	0.222

IHD: ischemic heart disease; COPD: chronic obstructive pulmonary disease. ${}^{\blacktriangle}$ : $p\leqslant$ 0.05 was considered statistically significant.

Because the vast majority of PJI patients came from other hospitals, different THR component systems were used in the initial replacement, including cemented and non-cemented systems. There were 10% of the patients infected after primary arthroplasty in our hospital. Part of the treatment is oral or intravenous antibiotics.

Table 2

Microorganisms in patients with PJI

Items	Hip fracture		Non- fracture		Total		$p$ value
Gram-positive	47	(67.1)	47	(61.8)	94	(64.4)	0.504
CoNS	31	(44.3)	29	(38.2)	60	(41.1)	0.452
S. aureus	10	(14.3)	9	(11.8)	19	(13.0)	0.661
Streptococci	2	(2.9)	4	(5.3)	6	(4.1)	0.753
Enterococci	4	(5.7)	4	(5.3)	8	(5.5)	1.000
Other	0	(0)	1	(1.3)	1	(0.7)	1.000
Gram-negative	11	(15.7)	13	(17.1)	24	(16.4)	0.821
E. coli	3	(4.3)	4	(5.3)	7	(4.8)	1.000
P. aeruginosa	6	(8.6)	6	(7.9)	12	(8.2)	0.882
K. pneumoniae	1	(1.4)	1	(1.3)	2	(1.4)	1.000
Other	1	(1.4)	2	(2.6)	3	(2.1)	1.000
Fungus	1	(1.4)	1	(1.3)	2	(1.4)	1.000
Negative	11	(15.7)	15	(19.7)	26	(17.8)	0.526
Total	70		76		146

Table 3

Polymicrobial infections

Items	Hip fracture	Non-fracture
GPC/GPC	2	3
GPC/GNB	3	3
GNB/GNB	0	1
GPC/FUN	1	1
Total	6	8

GPC: gram-positive cocci; GNB: gram-negative bacteria; FUN: fungus.

Table 4

Antimicrobial resistance of the main gram-positive bacteria

Items	P	OX	CZ	CXM	E	CL	GM	LVX	RA	LNZ	VA	ETP
CoNS
F	19	15	9	4	10	6	6	4	1	0	0	4
( $n=$ 31)	61.3	48.4	29.0	12.9	32.3	19.4	19.4	12.9	3.2	0	0	12.9
NF	14	12	6	6	15	13	3	10	2	0	0	4
( $n=$ 29)	48.3	41.4	20.7	20.7	51.7	44.8	10.3	34.5	6.9	0	0	13.8
Total	33	27	15	10	25	19	9	14	3	0	0	8
( $n=$ 60)	55.0	45.0	25.0	16.7	41.7	31.7	15.0	23.3	5.0	0	0	13.3
$p$	0.31	0.59	0.46	0.64	0.13	0.03 ${}^{\blacktriangle}$	0.54	0.05 ${}^{\blacktriangle}$	0.95	–	–	1.00
S.aureus
F	8	5	2	2	7	7	5	5	0	0	0	0
( $n=$ 10)	80	50	20	20	70	70	50	50	0	0	0	0
NF	6	3	1	1	6	6	2	3	0	0	0	0
( $n=$ 9)	66.7	33.3	11.1	11.1	66.7	66.7	22.2	33.3	0	0	0	0
Total	14	8	3	3	13	13	7	8	0	0	0	0
( $n=$ 19)	73.7	42.1	15.8	15.8	68.4	68.4	36.8	42.1	0	0	0	0
$p$	0.63	0.65	1.00	1.00	1.00	1.00	0.35	0.65	–	–	–	–

P: penicillin; OX: oxacillin; CZ: cefazolin; CXM: cefuroxime; E: erythromycin; CL: clindamycin; GM: gentamicin; LVX: levofloxacin; RA: rifampicin; LNZ: linezolid; VA: vancomycin; ETP: ertapenem. ${}^{\blacktriangle}$ : $p\leqslant$ 0.05 was considered statistically significant.

Table 5

Antimicrobial resistance of gram-negative bacteria

Items	GM	CPX	LVX	ATM	C	SCF	TZP	AMC	CARBA
GNB
F	2	3	1	5	2	3	0	4	0
( $n=$ 11)	18.2	27.3	9.1	45.5	18.2	27.3	0	36.4	0
NF	8	4	3	7	8	4	1	3	0
( $n=$ 13)	61.5	30.8	23.1	53.8	61.5	30.8	7.7	23.1	0
Total	10	7	4	12	10	7	1	7	0
( $n=$ 24)	41.7	29.2	16.7	50.0	41.7	29.2	4.2	29.2	0
$p$	0.047 ${}^{\blacktriangle}$	1.000	0.596	1.000	0.047 ${}^{\blacktriangle}$	1.000	1.000	0.659	–

GM: gentamicin; CPX: ciprofloxacin; LVX: levofloxacin; ATM: aztreonam; C: cephalosporin III/IV; SCF: cefoperazone and sulbactam; TZP: piperacillin-tazobactam; AMC: amoxicillin/clavulanic acid; CARBA: carbapenems. ${}^{\blacktriangle}$ : $p\leqslant$ 0.05 was considered statistically significant.

3.2 Results of bacterial infection in patients with PJI

Results of bacterial infections including monobacterial infection (Table 2) and polybacterial infection (Table 3) were evaluated. As shown in Table 2, a total of 146 microorganisms were isolated from the patients with PJI. The most common pathogen was coagulase-negative staphylococci (CoNS) isolates ( $n=$ 60, 41.1%), including 31 isolates in the fracture group and 29 isolates in the non-fracture group (44.3% vs 38.2%, $p=$ 0.452). There were 94 (64.4%) gram-positive cocci (GPC) isolates, including 47 isolates in the fracture group (31 CoNS, 10 staphylococcusaureus, 2 streptococci, 4 enterococci) and 47 isolates in the non-fracture group (29 CoNS, 9 S. aureus, 4 streptococci, 4 enterococci, 1 other) (67.1% vs. 61.8%, $p=$ 0.504). Furthermore, there were 24 gram-negative bacilli (GNB) isolates (16.4%), including 12 Pseudomonasaeruginosa, 7 Escherichia coli, 2 Klebsiellapneumoniae, 1 Acinetobacterbaumannii, 1 Citrobacter and 1 Proteus. Among them, P. aeruginosa was the most common GNB isolates, followed by Escherichia coli. The number of GNB isolates were not notably significant between fracture and non-fracture groups (15.7% vs. 17.1%, $p=$ 0.821). In addition, one patient in the fracture group was infected with Candida parapsilosis and one patient in the non-fracture group was infected with Candida albicans. Those two patients were not exclusively infected with fungus.

Additionally, Polymicrobial infectionsthere were 14 patients (10.6%) with polymicrobial infections, including 6 patients in the fracture group and 8 patients in the non-fracture group (Table 3). Five patients were infected with two kind of GPC, including 2 patients in the fracture group and 3 in the non-fracture group. Six patients were infected with both GPC and GNB, including 3 patients in the fracture group and 3 in the non-fracture group. One patient in the non-fracture group was infected with two kinds of GNB, and one patient in each group was infected with a GPC and a fungus (Table 3).

3.3 Antibiotic resistance

Antibiotic resistance in PJI patients was evaluated, as demonstrated in Tables 4 and 5. Results in Table 4 suggested that Staphylococci was highly drug resistant against methicillin or oxacillin. Thirty-five of the 79 staphylococcal isolates were methicillin-resistant (MR), including 27 MR-CoNS isolates and 8 MR S. aureus (MRSA) isolates. Approximately 45% of the CoNS isolates and 42.1% of the S. aureus isolates were MR staphylococci (MRS), accounting for 24% of all isolates. The detection rates for MR-CoNS and MRSA were similar between the two groups ( $p>$ 0.05). CoNS also showed a high drug resistance to clindamycin, the first- and second-generation cephalosporins and levofloxacin. There were higher drug resistance rates to clindamycin and levofloxacin in the non-fracture group than that in the fracture group ( $p<$ 0.05).

As shown in Table 5, there were 8 CoNS isolates resistant against ertapenem, with no significant difference between the two groups ( $p>$ 0.05). All CoNS isolates were sensitive to linezolid and vancomycin. Three of 24 GNB isolates (12.5%) were extended $\beta$ -lactamase (ESBL)-producing enterococcus profiles, including one in the fracture group and two in the non-fracture group. No carbapenemase-producing bacteria were detected. There were 12 GNB isolates (50%) with high drug resistant rates to aztreonam, 11 isolates (41.7%) with the third- and fourth-generation cephalosporins, and 10 isolates with gentamicin. There were higher drug resistance rates to all of the third- and fourth-generation cephalosporins and gentamicin in the non-fracture group than fracture group (Table 5).

4. Discussion

PJI is a severe complication for the patient and the health care providers with an incidence of approximately 1% [1, 2]. Infecting microorganism is a strong predictor of treatment success for PJI [17]. There are several studies exploring the microorganism profiles of PJI. Aggarwal et al. investigated the microorganism profiles of PJI at two arthroplasty infection referral centers in Europe and in the United States [18]. Bjerke-Kroll et al. conducted a single-center study to investigate the microbiology profiles of PJI [8]. Kheir et al. conducted a multicenter cohort study to investigate the etiology of PJI [19]. Drago et al. and Tsai et al. investigated microbiological profiles and antibiotic resistance in PJI of the knee and hip, respectively [20, 21]. This study showed that there are no significant differences in the microbiological profiles in PJI patients between the fracture and non-fracture groups. CoNS are the most common pathogens of PJI, accounting for 41.1% of all isolates. The prevalence of S. aureus is approximately 13%, which is similar to that in Europe [17]. However, it is lower than that in the United States and Taiwan [18, 21]. The prevalence of other GPC (such as enterococci and streptococci) is lower in this study.

Patients with PJI due to GNB have a significantly higher risk of aseptic loosening than those caused by GPB, indicating that GNB play an important role in PJI of the hip. Studies have shown that GNB infection is responsible for 5–20% of PJI, which is difficult to treat [15, 22, 23]. A recent multicenter study in Spain reported an increasing prevalence of GNB in PJI [19]. This study showed that GNB isolates are responsible for 16.4% of PJI, and there is no significant difference between fracture and non-fracture groups. P.aeruginosa is one of the most common GNB, followed by E. coli. Fungal infection is rare in PJI, and the incidence is as low as 1% [24]. Some studies have shown that the incidence of polymicrobial infection is not high (5–20%) for PJI of the hip [25, 26]. However, the treatment response rate was low [11, 27]. It also has been reported that the rate of polymicrobial infection is as high as 47% [11]. In this study, the rate of polymicrobial infection in patients with PJI of the hip is 10.6%, showing no significant differences between the fracture group and the non-fracture group. GPC were the most common pathogen, which is consistent with a previously published report [28]. In this study, the negative culture rate is 17.8%, which is consistent with one previous report that shows an annual negative rate of 11.9–33.3% over 15 years [29]. The reason may be that most patients have received some treatments such as antibiotic therapy for PJI before admission to our hospital, and they did not discontinue antibiotics for two weeks prior to the microorganism culture. This study found that the MRS isolates are numerous, accounting for 45% of CoNS isolates, 42.1% of S. aureus isolates, and approximately 25% of all PJI cases. This finding is consistent with the general (high) prevalence of MRS in China [30], which is related to the national antibiotic management policy [18]. The differences in incidence rates of MR-CoNS and MRSA in the fracture group and the non-fracture group are not significant in this study. Similarly, we identified two fungal isolates that accounts for 1.4% of all isolates. Both fungal isolates were detected in patients with polymicrobial infections, and no simple fungal infections were identified. However, the reliability may be doubt due to the small sample size.

Antibiotics are proved to significantly reduce PJI rates after hip and knee arthroplasty [31]. It is suggested that vancomycin combined with ciprofloxacin or a third generation cephalosporin provids the highest antimicrobial coverage of all responsible pathogens identified in early PJI [32]. There are higher drug resistance rates to clindamycin and levofloxacin in the non-fracture group than fracture group. The first- or second-generation cephalosporins (cefazolin or cefuroxime) were used in routine perioperative antibiotic prophylaxis. Clindamycin or levofloxacin may be used in patients who are allergic to cephalosporins. This regimen is usually appropriate because GPC is the most common bacteria in PJI. However, in this study, staphylococci showed high resistance rates to clindamycin, all of the first- and second-generation cephalosporins and levofloxacin. Further research is necessary to investigate the use of vancomycin particularly in hip replacement for non-fracture patients. The antibiotic resistance of GNB is a challenging issue during PJI treatment, and the response rate is low [21]. In this study, although only a small number of GNB were identified, they showed high resistance rates to aztreonam, all of the third- and fourth-generation cephalosporins, and gentamicin. The prevalence of ESBL-producing enterococci is 12.5%, which is consistent with a previous report [5]. Previous studies have identified the resistance of GNB to ESBL [33] and fluoroquinolones [34] as a major concern. However, in this study, GNB shows high drug resistance rates to aztreonam, all of the third- and fourth-generation cephalosporins, and gentamicin. Moreover, there are higher drug resistance rates to all of the third- and fourth-generation cephalosporins and gentamicin in non-fracture group than fracture group. Therefore, during antibiotic prophylaxis for initial hip replacement, the above antibiotics should be avoided in empirical antibiotic therapy, particularly in hip replacement due to non-fracture. The drug resistance rate of non-fracture group is higher than that of fracture group, but the reason for this difference is unclear.

There are also some limitations. First, this is a retrospective study with a potential selection bias. Second, some patients underwent hip replacement at other hospitals and received treatment for PJI, resulting in confounding factors. Third, the sample size is small, and large multicenter study is necessary to further validate the results of this study.

5. Conclusions

This study showed that there were no significant differences in the microbiological profiles of PJI patients between fracture and non-fracture groups. CoNS was the most common pathogen in both groups. CoNS isolates were more resistant to clindamycin and levofloxacin in the non-fracture group than fracture group, whereas GNB isolates were more resistant to all of the third- and fourth-generation cephalosporins and gentamicin in the non-fracture group than fracture group. Therefore, prophylactic or empiric antibiotic therapy should be optimized according to local conditions.

Ethics statement

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. The study was approved by the Ethics Committee of The First Medical Center, Chinese PLA General Hospital (No. 20200618012).

Availability of data and materials

The dataset that support the conclusions of this article is included in the article.

Funding

This work was supported by the grants from the Beijing Municipal Natural Science Foundation (No. 7192199) and Youth Support Project of Chinese PLA General Hospital (No. QNF19015).

Author contributions

LF performed the study and analyzed the results. JF and YZ helped in the drafting and revising of the manuscript. WC and GZ contributed to the collection of the cases. LB provided revision for intellectual content. JC made some meaningful suggestions. All authors reviewed and approved the final submitted version.

Footnotes

Acknowledgments

The authors thank Chi Xu, Rui Li, and Baozhan Yu for their contribution toward the analysis and interpretation of data involved in drafting the manuscript.

Conflict of interest

The authors declare that they have no competing interests.

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Microbiological profiles and antibiotic resistance of periprosthetic joint infection after hip replacement in patients with fracture or non-fracture: A comparative study

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Introduction

2. Patients and methods

2.1 Patients

2.2 Testing and sampling methods of microorganisms

2.3 Data collection and statistical analysis

3. Results

3.1 Demographics of patients

Table 1 General characteristics in the two groups

3.3 Antibiotic resistance

4. Discussion

5. Conclusions

Ethics statement

Availability of data and materials

Funding

Author contributions

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
General characteristics in the two groups