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 ~  Abstract
 ~ Introduction
 ~  Materials and Me...
 ~ Results
 ~ Discussion
 ~ Conclusion
 ~  References
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  Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 37  |  Issue : 4  |  Page : 509-513
 

Microbiological profile of infections of the hip joint: An Indian perspective


1 Department of Orthopaedics, Christian Medical College, Vellore, Tamil Nadu, India
2 Department of Clinical Microbiology, Christian Medical College, Vellore, Tamil Nadu, India

Date of Submission06-Feb-2020
Date of Acceptance04-Mar-2020
Date of Web Publication18-May-2020

Correspondence Address:
Dr. T D Hariharan
Department of Orthopaedics, Christian Medical College, Vellore, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmm.IJMM_20_31

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 ~ Abstract 

Background: Knowledge of the local microbiological epidemiology helps in formulating protocols for appropriate treatment of hip infections. The aim of this study was to profile the organisms cultured from infected hips. Methods: The microbiological profile and sensitivity pattern of organisms in eighty infected hips were reviewed. Results: Infection was secondary to arthroplasty in 35, fracture surgery in 34 and primary septic arthritis in 11. Twenty percent of the infections were polymicrobial, whereas the rest were monomicrobial. Fifty-five percent were Gram-positive, of which 45% were Staphylococcus species (36% methicillin-sensitive Staphylococcus aureus, 20% methicillin-resistant S. aureus, and 44% coagulase sensitive Staphylococcal species). All Staphylococcus species were sensitive to vancomycin, but 20% of Enterococcus species were resistant to vancomycin. One-third of the Enterococcus species and 2% of Staphylococcus species were resistant to teicoplanin. Escherichia coli (n = 10) and Pseudomonas sp. (n = 13) were the most common Gram-negative organism. Although 18% of the Gram-negative organisms were carbapenem resistant, all were sensitive to colistin. Conclusion: Staphylococcus sp. was the most common pathogen found in hip infections. However, the high incidence of Gram-negative infection requires that prophylactic antibiotics cover these organisms as well. The high resistance to first-line antibiotics should be taken into consideration while making protocols. The knowledge of the microbial profile is especially important when considering arthroplasty for arthritis secondary to hip infections.


Keywords: Hip joint, infection, revision surgery, susceptibility profile, THR


How to cite this article:
Arunshankar A, Chandy V J, Elangovan D, Hariharan T D, Jude Prakash JA, George R, Oommen AT, Poonnoose PM. Microbiological profile of infections of the hip joint: An Indian perspective. Indian J Med Microbiol 2019;37:509-13

How to cite this URL:
Arunshankar A, Chandy V J, Elangovan D, Hariharan T D, Jude Prakash JA, George R, Oommen AT, Poonnoose PM. Microbiological profile of infections of the hip joint: An Indian perspective. Indian J Med Microbiol [serial online] 2019 [cited 2020 Jun 1];37:509-13. Available from: http://www.ijmm.org/text.asp?2019/37/4/509/284527



 ~ Introduction Top


Infections around the hip, if inadequately treated, can result in significant morbidity. Many of these patients subsequently require hip replacements to reduce pain and improve their quality of life. However, revision arthroplasty is not without risk, as patients with prior infection in the hip are at risk of developing periprosthetic infection.[1]

Adequate treatment of infections around the hip is essential before any definitive arthroplasty surgery. Luo et al. showed that adequate treatment of infections ensured that there were no infections following hip replacement in such patients.[2] The International consensus meeting on prosthetic joint infections (2013) has suggested guidelines on how to manage patients with infected prosthetic joints.[3] Two-stage revision arthroplasty is considered the gold standard in patients undergoing a revision hip replacement for an infected hip. This involves a first-stage debridement and antibiotic impregnated cement spacer followed by culture-specific antibiotics, and second-stage implantation of a total hip arthroplasty implant. A single-stage revision surgery may be considered in patients infected with a non-virulent organism, that is sensitive to first-line antibiotics.[3] There is, however, no consensus on arthroplasty following infections secondary to other implants, or primary septic arthritis.

Kapadia et al. suggested that the epidemiology of microbiological and drug resistance patterns in prosthetic joint infections varies between countries and regions.[4] As the abuse of antibiotics has changed the resistance spectrum, it is imperative to be aware of the regional microbiological and antibiotic resistance profile. This information is especially important in situ ations where empirical antibiotics are necessary or when treating culture-negative cases. In addition, the choice of antibiotics mixed in the cement spacer used in the first stage of revision arthroplasty for infected hips is determined by the microbiological profile of the organisms found in the local region. In this study, we aim to profile the organisms in the hips of patients who presented to our unit, following a primary or secondary hip infection.


 ~ Materials and Methods Top


All patients who presented to the orthopaedic unit during the period 2007–2018, with a history of having had an infection of the hip – either primary or secondary to an implant fixation/arthroplasty were considered. Patients who had a history of tuberculosis arthritis and those who had a replacement for other pathologies were excluded from the study. All patients had an implant exit/debridement, as appropriate as part of the treatment of the infection. Those who required an arthroplasty had either a single-stage revision arthroplasty, or a two-stage revision. The decision to do a single or two-stage arthroplasty was based on the criteria set by the international consensus group and was dependent on the clinical and surgical findings, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), and where appropriate, joint fluid counts/culture and frozen section analysis.[3],[5] Tissue from the deep tissues close to the implant was collected at the time of implant removal and sent for culture, as per standard operating protocols. In the two-stage revision, following the first stage debridement, antibiotic spacers with teicoplanin and gentamicin were left in the hip joint for an interval of 3 months. At the second stage, the spacer was removed, and a revision arthroplasty was done. Some patients had implant removal/debridement and did not proceed to replacement. All patients with positive cultures were treated with appropriate intravenous antibiotics for 6 weeks following the initial debridement. The organisms were cultured using media such as Blood agar, MacConkeyagar and Thioglycollate broth (Aerobic and anaerobic condition) for an extended period of 1 week. The microbiological profile of the organisms cultured at the time of debridement was studied, and the sensitivity pattern analysed.


 ~ Results Top


Of patients presented to the orthopaedic unit with infection of the hip – either primary or secondary to an implant, eighty patients were culture positive. The mean age of the patients was 57 years (range 24–84 years), with 65 males and 15 females. All patients had been treated with antibiotics elsewhere for varying durations, before review at our institution.

The most common cause for revision of the implant was the failure of a previous hip replacement hemi-arthroplasty (n = 29) or total hip replacement (n = 6). Twenty-six had a fracture implant removed following infection, while four had debridement with retention of the implant. Four had infected implants removed from the acetabulum. There were 11 patients who presented with a history of septic arthritis of the hip.

Of the eighty patients with positive cultures, 24 had a revision hip arthroplasty – either single stage (6) or two-stage (18). Another 29 patients had an excision arthroplasty but did not proceed to a second stage, 21 of them with antibiotic laden hip spacers. The remaining 27 had a simple debridement of the hip with the removal of the infected implant if required.

Of the eighty patients with positive cultures, 64 hips (80%) had monomicrobial infection, while 16 (20%) had polymicrobial infection [Figure 1]. Overall, 55% (54) were Gram-positive, and 45% (44) were Gram-negative organisms. Staphylococcus species (45%) was the most common Gram-positive organism, with 36% being methicillin-sensitive Staphylococcus aureus (MSSA), 20% methicillin-resistant S. aureus (MRSA), and 44% coagulase-negative Staphylococcus species (CONS).
Figure 1: Distribution of monomicrobial (Gram-positive and negative) and polymicrobial infections of the hip joint

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[Figure 1] shows the distribution of Gram-negative organisms. The most common Gram-negative organisms were Escherichia coli and Pseudomonas species.

Twenty percent of the infections were polymicrobial in nature, with slightly more Gram-positive organisms than Gram-negative. Most commonly, there were two organisms cultured except in one case, which grew a combination of two Gram-positive organisms (CONS and Enterococcus species) and two Gram-negative organisms (E. coli and Klebsiella species). The most common dual pathogen was the CONS, which was cultured along with coliforms (4 in number), MRSA (2 in number) and non-fermenting Gram-negative bacilli (NFGNB) (2 in number), respectively. There were two other cases of Enterococcus species infection one with coliform and the other with NFGNB. There were two cases infected with MRSA and coliform.

The sensitivity pattern of the common organisms is listed below:

  • Staphylococcus species (n = 45): CONS (n = 20), S. aureus (n = 25)


    • There was a higher level of sensitivity to methicillin seen in S. aureus − 64%(16/25) – MSSA, as compared to CONS - 40% (8/20)
    • Erythromycin susceptibility was 44% for S. aureus (11/25) and 60% for CONS (12/20)
    • There was a high-level susceptibility for co-trimoxazole of around 80% for both the species (22/25 and 15/20)
    • All MRSA and methicillin-resistant CONS were sensitive to both vancomycin and linezolid, while 98% were sensitive to teicoplanin.


  • Enterococcus species (n = 9)


    • 4/9 (44%) were moderately susceptible to ampicillin and gentamicin
    • 6/4 (66%) were sensitive to teicoplanin
    • 2/9 (20%) were vancomycin-resistant.


  • E. coli (n = 10)


    • There was very low susceptibility to gentamicin 15% (2/10), and cefpodoxime–15%(2/10) with 78% extended-spectrum beta-lactamases (ESBL) producers
    • Only 25% (3/10) were sensitive to cotrimoxazole
    • Sixty percent (9/10) were sensitive to amikacin and levofloxacin, and 61%(8/10) were sensitive to ciprofloxacin
    • Ninety percent were sensitive to both meropenem and ertapenem.


  • Pseudomonas species (n = 13)


    • There was 90% sensitivity to both ceftazidime and cefepime
    • Eighty percent were sensitive to the piperacillin-tazobactam combination
    • Only 60% was sensitive to gentamicin, while 50% were sensitive to amikacin
    • Fifty percent were sensitive to levofloxacin, and 70% were sensitive to ciprofloxacin
    • Seventy percent were sensitive to meropenem, and the three carbapenem-resistant organisms were sensitive to colistin
    • There was no resistance to colistin.


All the Klebsiella species (n = 1) and NFGNB (n = 4) were carbapenem-resistant, but sensitive to colistin.

Considering the antibiotic sensitivity of the Gram-positive organisms, all Staphylococcus species were sensitive to vancomycin; but 20% of Enterococcus species were resistant to vancomycin. One-third of the Enterococcus species and 2% of Staphylococci species were resistant to teicoplanin. Among the 44 Gram-negative organisms, 18% (8) were carbapenem-resistant, but all were sensitive to colistin.


 ~ Discussion Top


Millions of orthopaedic implants are used every year across the world, and in spite of many advances, many of the implants become colonised by bacteria and become the focus of implant-related infection. Infections lead to implant failure or loosening, necessitating revision surgery. This can be extremely expensive, and cause a lot of morbidities.

Infections can occur due to contamination at the time of surgery, or a spread from concurrent infections elsewhere in the body. Associated factors such as diabetes mellitus, advanced age, HIV infection, malnutrition and inflammatory arthritis can pre-dispose the patients to infections. Other risk factors include operating time, concurrent urinary or respiratory tract infection at the time of surgery. Post-operative complications including wound haematoma and suture abscess could also contribute to deep-seated hip joint infection.[3] The implant forms a base onto which the pathogens bind, often forming a biofilm.

The aim of debridement for hip infections is to eradicate the infection. However, in spite of adequate treatment and removal of the implant, the hip joint is often destroyed. This necessitates a total hip replacement. The Fixation using Alternative Implants for the Treatment of Hip fractures trial-also suggests that infection is one of the main causes for revision fixation or revision arthroplasty.[6] If the infection is treated well, the outcome of arthroplasty is good. Luo et al., in their series of 101 post-septic hip joint arthritis that underwent a total hip replacement, had no post-operative joint infection at a mean of 24 years follow-up.[2] Kim et al. published their results from a retrospective analysis of 170 post-childhood septic arthritis hips that had a total hip replacement and none developed infection or septic loosening following the arthroplasty.[7] From India, Hariharan et al. documented good results following two-staged hip replacement in 22 patients who had a significant infection of the hips.[8] Often, in a loose hip prosthesis, it is difficult to make a diagnosis of infection. The diagnosis of prosthetic infection is based on the criteria as defined by the International Consensus Meeting on the prosthetic joint infection. Any patient with one major criterion or 3 out of 5 minor criteria was considered positive for prosthetic infection. The two major criteria were (a) A sinus tract communicating with the prosthesis; or (b) A pathogen is isolated by culture from two separate tissue or fluid samples obtained from the affected prosthetic joint. Minor criteria included were (a) Elevated serum ESR (30 mm/h) or CRP levels (10 mg/L), (b) Elevated synovial fluid white blood cells count (>3000 cells/ml), (c) Elevated synovial neutrophils percentage (80%), (d) Isolation of a microorganism in one culture of periprosthetic tissue or fluid (e) Greater than five neutrophils per high-power field in five high-power fields observed for the histology analysis of periprosthetic tissue at ×400.[3]

According to the International Consensus Meeting on Periprosthetic Joint infection, the current gold standard of treatment is a two-staged revision surgery – a debridement and antibiotic cement spacer at the first stage, followed by 6 weeks of appropriate antibiotics. This is then followed by the second stage revision hip arthroplasty. In cases where the pathogen is not known before the debridement, the choice of antibiotic to be mixed with the polymethacrylate acetate (PMMA) cement depends on the local microbiological epidemiology. The most common antibiotic mixed in the spacer is vancomycin or tobramycin. Antibiotics for Gram-negative cover are not added as a routine unless the pathogen is known.[3] Li et al. in their series of revision total knee replacement following two-staged revisions showed infection-free survival of at least 5 years except in one patient.[9]

Rafiq et al. studied 337 single-stage revision surgeries and observed a high incidence of staphylococcus infection, with 67% of them being CONS.[10] Phillips et al. in their study of infection following hip and knee arthroplasty, found an incidence of 71% Staphylococcus species infection, with 4% being MRSA.[11] Papanna et al., in their series of 18 cases that had two-stage revision had 11 patients (61.1%) infected with Staphylococcus species of which only one patient had resistance to methicillin.[12] From India, Hariharan et al. in their series of 22 patients who had a two-stage hip replacement for infection, found S. aureus to be the most common organism with 25% resistance to methicillin.[8] George et al., in their analysis of isolates from patients with a diagnosis of septic arthritis, found Staphylococcus species to be the most common isolate though only 10% of the joints studied were hips.[13]

Even though most of the infections around the hip joint are monomicrobial, the incidence of polymicrobial infections is on the rise, with multidrug resistance.[14] It is estimated that 80% of the prosthetic joint infection involves a single bacterium, while a small subset ranging from 15% to 20% is polymicrobial.[15] The eradication of these infections can impose a great challenge to the treating surgeon.

From our study, it appears that most infections are monomicrobial, with Staphylococcus species (S. aureus and CONS) being identified in 45% of the cases. Methicillin sensitivity was 64% in S. aureus, but only 40% among the CONS. While all Staphylococcus species were sensitive to vancomycin, we observed 20% vancomycin resistance in Enterococcus species. Another observation was that a third of the Enterococcus species were resistant to teicoplanin. This suggests that for Gram-positive cover, one should probably choose vancomycin over teicoplanin to be mixed with the antibiotic spacer.

There was a significant percentage of Gram-negative infections in this study, especially E. coli and Pseudomonas species. ESBL organisms far outnumbered the sensitive organisms among both E. coli and Pseudomonas species – at about 78%. While the sensitivity to cotrimoxazole, gentamicin, amikacin and cephalosporins was low, there was 82% sensitivity to carbapenem. None of the organisms were resistant to colistin. As the incidence of Gram-negative infection was about 45% in our study, it would be prudent to add a Gram-negative cover in the PMMA spacer, and meropenem would seem to be the ideal choice.

Similar patterns of infections were observed in the study done by Kavolus et al. which shows S. aureus (13%) and coagulase-negative staphylococci (41%) to be the most common pathogen isolated among the monomicrobial joint infection. This was closely followed by Gram-negative pathogens such as Pseudomonas species and E. coli.[16] Similar to our study, Tornero et al. found that 9.3% of prosthetic joint infections were caused by Enterococci, with Enterococcus faecalis and Enterococcus faecium being the most common though often associated with polymicrobial joint infection.[17] We also observed the same proportion of Enterococcus species (10%) among the monomicrobial infection and in the case of polymicrobial infections, Enterococcus species were found with coliforms and NFGNB. Ortega-Peña et al. suggest that they could be associated with poor pre-surgical hygiene or proximity to the genital area.[15]

Regarding Gram-negative bacilli in revision hip surgery, Zmistowski et al. observed that the Gram-negative bacilli associated with prosthetic joint infection were those that were commonly associated with urinary tract infections, such as E. coli, Klebsiella species, Proteus species and Enterobacter species.[18] Rodríguez Pardo et al. isolated E. coli and Enterobacter species in 78% of the samples, while Pseudomonas aeruginosa was only 20%.[19] However, in this study, the incidence of Pseudomonas species and E. coli species infections were almost the same. There was one isolate of Salmonella.

One of the limitations of this study is that we have not used techniques such as sonication cultures of the retrieved implants to improve bacterial load and improved pathogen isolation as shown in the study by Lass et al.[20] Although all samples were processed in media with ambient conditions adequate for bacteria, including anaerobes and fungi with prolonged incubation to grow, we did not isolate any anaerobes or fungal organisms in this study. Further, molecular methods were not used for the identification of pathogen which would have increased the yield of culture and speciation of the CONS and Enterococcus species adding greater value to the study. Another limitation of this study is that all the cases are from a single tertiary care centre, where patients are often referred. Most have been treated with a variety of antibiotics before review at the centre. The spectrum of organisms may not be representative of that found at other smaller centres. Since the study incorporates data from 2007, it should be noted that there have been minor changes in the method of interpretation of antibiotic susceptibility based on the Clinical and Laboratory Standards Institute, and the antibiotics tested over the years. Further, this study does not assess the outcome of the debridement.

However, the strength of this study is that it provides a detailed analysis of the microbiological characteristics and antimicrobial resistance patterns in patients with infected hip implants. It provides us with data that could help in formulating protocols for antibiotic prophylaxis and in choosing antibiotics to be mixed in the PMMA spacer for infected hips.


 ~ Conclusion Top


Successful treatment of infections related to implants is dependent on local debridement, local antibiotic-loaded cement and appropriate intravenous antibiotics for an adequate duration before implantation of the new implant. The knowledge of local microbiological epidemiology helps in formulating protocols for appropriate antibiotic treatment. The profile of the organisms is ever-evolving and needs to be monitored regularly. The increase of polymicrobial infections and antibiotic resistance require prolonged multi-drug antibiotic therapy, often with a multidisciplinary approach.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 ~ References Top

1.
Kuiper JW, Willink RT, Moojen DJ, van den Bekerom MP, Colen S. Treatment of acute periprosthetic infections with prosthesis retention: Review of current concepts. World J Orthop 2014;5:667-76.  Back to cited text no. 1
    
2.
Luo Y, Yang Z, Yeersheng R, Li D, Kang P. Clinical outcomes and quality of life after total hip arthroplasty in adult patients with a history of infection of the hip in childhood: A mid-term follow-up study. J Orthop Surg Res 2019;14:38.  Back to cited text no. 2
    
3.
Parvizi J, Gehrke T, Chen AF. Proceedings of the International Consensus on Periprosthetic Joint Infection. Bone Joint J 2013;95-B: 1450-2.  Back to cited text no. 3
    
4.
Kapadia BH, Berg RA, Daley JA, Fritz J, Bhave A, Mont MA. Periprosthetic joint infection. Lancet 2016;387:386-94.  Back to cited text no. 4
    
5.
Parvizi J, Tan TL, Goswami K, Higuera C, Della Valle C, Chen AF, et al. The 2018 definition of periprosthetic hip and knee infection: An evidence-based and validated criteria. J Arthroplasty 2018;33:1309-400.  Back to cited text no. 5
    
6.
Fixation using Alternative Implants for the Treatment of Hip fractures (FAITH) Investigators, Nauth A, Creek AT, Zellar A. Fracture fixation in the operative management of hip fractures (FAITH): An international, multicentre, randomised controlled trial. Lancet 2017;389:1519-27.  Back to cited text no. 6
    
7.
Kim YH, Oh SH, Kim JS. Total hip arthroplasty in adult patients who had childhood infection of the hip. J Bone Joint Surg Am 2003;85:198-204.  Back to cited text no. 7
    
8.
Hariharan TD, Chandy VJ, George J, Mathew AJ, Premnath J, Pragasam AK, et al. Microbiological profile and outcomes of two-stage revision hip arthroplasty. Indian J Med Microbiol 2019;37:67-71.  Back to cited text no. 8
[PUBMED]  [Full text]  
9.
Li H, Ni M, Li X, Zhang Q, Li X, Chen J. Two-stage revisions for culture-negative infected total knee arthroplasties: A five-year outcome in comparison with one-stage and two-stage revisions for culture-positive cases. J Orthop Sci 2017;22:306-12.  Back to cited text no. 9
    
10.
Rafiq I, Gambhir AK, Wroblewski BM, Kay PR. The microbiology of infected hip arthroplasty. Int Orthop 2006;30:532-5.  Back to cited text no. 10
    
11.
Phillips JE, Crane TP, Noy M, Elliott TS, Grimer RJ. The incidence of deep prosthetic infections in a specialist orthopaedic hospital: A 15-year prospective survey. J Bone Joint Surg 2006;88:943-8.  Back to cited text no. 11
    
12.
Papanna MC, Chebbout R, Buckley S, Stockley I, Hamer A. Infection and failure rates following total hip arthroplasty for septic arthritis: A case-controlled study. Hip Int 2018;28:63-7.  Back to cited text no. 12
    
13.
George J, Chandy VJ, Premnath J, Hariharan TD, Oommen AT, Balaji V, et al. Microbiological profile of septic arthritis in adults: Lessons learnt and treatment strategies. Indian J Med Microbiol 2019;37:29-33.  Back to cited text no. 13
[PUBMED]  [Full text]  
14.
Marculescu CE, Cantey JR. Polymicrobial prosthetic joint infections: Risk factors and outcome. Clin Orthop Relat Res 2008;466:1397-404.  Back to cited text no. 14
    
15.
Ortega-Peña S, Colín-Castro C, Hernández-Duran M, López-Jácome E, Franco-Cendejas R. Microbiological characteristics and patterns of resistance in prosthetic joint infections in a referral hospital. Cir Cir 2015;83:371-7.  Back to cited text no. 15
    
16.
Kavolus JJ, Cunningham DJ, Rao SR, Wellman SS, Seyler TM. Polymicrobial infections in hip arthroplasty: Lower treatment success rate, increased surgery, and longer hospitalization. J Arthroplasty 2019;34:710-6.  Back to cited text no. 16
    
17.
Tornero E, Senneville E, Euba G, Petersdorf S, Rodriguez-Pardo D, Lakatos B, et al. Characteristics of prosthetic joint infections due to Enterococcus sp. and predictors of failure: A multi-national study. Clin Microbiol Infect 2014;20:1219-24.  Back to cited text no. 17
    
18.
Zmistowski B, Karam JA, Durinka JB, Casper DS, Parvizi J. Periprosthetic joint infection increases the risk of one-year mortality. J Bone Joint Surg Am 2013;95:2177-84.  Back to cited text no. 18
    
19.
Rodríguez-Pardo D, Pigrau C, Lora-Tamayo J, Soriano A, del Toro MD, Cobo J, et al. Gram-negative prosthetic joint infection: Outcome of a debridement, antibiotics and implant retention approach. A large multicentre study. Clin Microbiol Infect 2014;20:O911-9.  Back to cited text no. 19
    
20.
Lass R, Giurea A, Kubista B, Hirschl AM, Graninger W, Presterl E, et al. Bacterial adherence to different components of total hip prosthesis in patients with prosthetic joint infection. Int Orthop 2014;38:1597-602.  Back to cited text no. 20
    


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