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 ~ Introduction
 ~  Materials and Me...
 ~ Results
 ~ Discussion
 ~ Conclusion
 ~  References
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  Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 37  |  Issue : 1  |  Page : 29-33
 

Microbiological profile of septic arthritis in adults: Lessons learnt and treatment strategies


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 Web Publication16-Aug-2019

Correspondence Address:
Dr. V J Chandy
Department of Orthopaedics, Christian Medical College, Vellore - 632 004, Tamil Nadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmm.IJMM_19_134

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 ~ Abstract 


Objective: The aim of this study is to characterise the clinical and microbiological profile of adult patients treated at our orthopaedic unit with septic arthritic between 2006 and 2017. Materials and Methods: A total of 70 patients who were admitted with a diagnosis of septic arthritis between 2006 and 2017 were included in the study. The patients' clinical and epidemiological characteristics were surveyed; microbiological profile and the complications relating to the patients' treatment were identified. Results: Septic arthritis was more common among males (83%). About 75% of the patients presented with a history of fever. The knee was the most commonly affected joint (71%), followed by the hip. While C-reactive protein was found to be consistently >75, total blood white blood cell (WBC) counts were found not to be reflective of the presence of infection with a mean WBC count of only 13,561/cu.mm, and Gram stain examination had a poor sensitivity of 47%. Among the co-morbidities, the most prevalent association was with diabetes mellitus. The infectious agent most frequently isolated was Staphylococcus aureus(42.85%). The antibiotic sensitivity pattern has evolved since the early years, with resistant strains becoming increasingly prevalent. Unusually, high incidence of streptococci was noted (30%), contrary to the published literature. One-third of the patients had multi-resistant organisms. Septic arthritis left 70% of the patients with a significant residual disability at 6 months follow-up and had 4.25% mortality. Conclusion: Changing sensitivity patterns of microbes in septic arthritis point to a need for reconsidering empirical antibiotic therapy. Joint damage following infection can lead to significant disability.


Keywords: Infective arthritis, microbiological profile, septic arthritis


How to cite this article:
George J, Chandy V J, Premnath J, Hariharan T D, Oommen AT, Balaji V, Poonnoose PM. Microbiological profile of septic arthritis in adults: Lessons learnt and treatment strategies. Indian J Med Microbiol 2019;37:29-33

How to cite this URL:
George J, Chandy V J, Premnath J, Hariharan T D, Oommen AT, Balaji V, Poonnoose PM. Microbiological profile of septic arthritis in adults: Lessons learnt and treatment strategies. Indian J Med Microbiol [serial online] 2019 [cited 2019 Oct 21];37:29-33. Available from: http://www.ijmm.org/text.asp?2019/37/1/29/264486





 ~ Introduction Top


Infective arthritis of joints is an orthopaedic emergency requiring prompt intervention. Early diagnosis and appropriate management are of paramount importance, owing to the significant morbidity associated with the disease, as delay in treatment could lead to complete destruction of the joint involved, and result in systemic complications.

The incidence of septic arthritis of native joints in a general population has been reported to be around two cases/100,000 people per year.[1] However, significant geographical as well as demographic variability in incidence have been reported, varying from 4 to 10 cases/100,000 population per year in Western Europe,[2],[3],[4] up to 29 cases/100,000 population per year among the aboriginal Australian population.[5] No population-based data are available from India in this regard.

The most common causative organism of septic arthritis across all age groups has been Staphylococcus aureus,[4],[6] and the empirical antibiotic therapy for septic arthritis, has conventionally been tailored to cover the same – the recommendations being β-lactamase stable penicillins (e.g., cloxacillin) and cephalosporins.[4],[7] However, increasing rates of methicillin-resistant S. aureus (MRSA) causing primary septic arthritis of native joints are being reported, with significant geographic variability.[6],[8],[9],[10] Studies from India also show a higher rate of staph aureus infections in the joints with large numbers of MRSA.[11]

In this study, we aimed to look at the clinical and microbiological profile of septic arthritis in adult patients, treated at our orthopaedic unit over 12 years.


 ~ Materials and Methods Top


This study was designed as a retrospective case series analysis. Seventy consecutive adult patients who were treated at the orthopaedic facility with a diagnosis of acute or subacute pyogenic arthritis of native joints, during 12 years between January 2006 and December 2017 were included in the study. The diagnosis of septic arthritis was made as per the criteria described by Newman[12] – which required at least one positive criteria – (i) isolation of a pathogenic organism from an affected joint; (ii) isolation of a pathogenic organism from another source (e.g. blood) in the context of a hot red joint suspicious of sepsis; (iii) typical clinical features and turbid joint fluid in the presence of previous antibiotic treatment; and (iv) post-mortem or pathological features suspicious of septic arthritis. The exclusion criteria included age <18 years, previous surgery to the involved joint-including knee replacements, duration of symptoms >6 months and a diagnosis of tuberculous or fungal arthritis.

The demographic profile of the patients was gathered from inpatient medical records. The patients were grouped into two categories-acute pyogenic arthritis (duration of symptoms <2 weeks) and subacute pyogenic arthritis (2 weeks–6 months symptoms).

The clinical parameters assessed included the site of the involved joint, duration of local symptoms (joint pain, swelling) and the presence of fever. Laboratory parameters analysed included erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), total and differential white blood cell (WBC) counts in blood and synovial fluid counts (where available).

The microbiological profile of the infections were analysed – Gram stain, culture positivity rates, the organism identified in culture and the antibiotic susceptibility pattern. The incidence of primary joint infection with resistant strains, particularly MRSA was also analysed.

The peri-operative morbidity was reviewed, in terms of the need for a second surgical procedure, uncontrolled infection resulting in amputation, incidence of systemic bacteraemia, rate of intensive care unit (ICU) admissions and mortality.

Although no formal functional assessment was done, their ambulatory status in the community was assessed from outpatient records.


 ~ Results Top


A total of 210 patients were admitted under the orthopaedic unit with a diagnosis of septic arthritis from January 2006 to December 2017 – of whom 116 were <18 years. Of the remaining 94 patients, 12 patients had previous surgery to the involved joint and seven had symptoms of more than 6 months duration. Seventy patients (58 males, 12 females) were included in the study after the exclusion criteria were followed. The mean age of the study population was 48.8 years.

Forty-five patients presented with symptoms of duration ≤2 weeks (acute group) and 25 patients presented between 2 weeks and 6 months (subacute group). The median duration of symptoms in the acute group was 5 days (interquartile range [IQR] = 3–7 days) and in the subacute group was 30 days (IQR = 21–60 days).

Seventy-five percent (53/70) of patients presented with a history of fever-82% (37/45) in the acute group and 64% (16/25) in the subacute group. About 74.2% (52/70) of the patients had no pre-existing local or systemic infection before the onset of the acute symptoms of septic arthritis. 21.4% (15/70) patients had a history of pre-existing local soft tissue or bony infection in the same limb as the affected joint. 4.29% (3/70) had other systemic foci of infection at the time of diagnosis of septic arthritis. 32.9% (23/70) patients were diabetic, and an additional 4.29% (3/70) patients were immunocompromised-one with HIV and two on chronic steroids.

71.42% of patients (50/70) had infection involving the knee joint. The other joints involved were: Hip 10% (7/70), ankle 7.14% (5/70), shoulder 7.14% (5/70) and one case each involving the sternoclavicular, sacroiliac and elbow joints [Figure 1].
Figure 1: Distribution of involved joints

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The median WBC counts of the patient were 13561/cu.mm at presentation (n = 62).

In the acute group (n = 39), the median WBC count was 14,400/cu.mm (IQR = 11,450–18,600/cu.mm) and 10,700/cu.mm (IQR = 9050–14,000/cu.mm) in the subacute group (n = 23). Leucocytosis >11,000/cu.mm was noted only in 66% of patients. Blood neutrophilia averaged to 75.88% in the overall study population (81.5% in the acute and 66.3% in the subacute groups).

Average ESR at presentation was 77.6 mm at 60 min (n = 38): ESR of 84 mm (n = 18) in the acute and 71.8 (n = 20) in the subacute groups. The CRP level at presentation (n = 36) was 132.5 (IQR = 79.38–190): 185 (IQR = 100.02–192) in the acute group (n = 19) and 122 (IQR = 121.5–122.5) in the subacute group (n = 17). In the 19 patients who had synovial fluid counts done, the average synovial fluid WBC counts was 74,855/cu.mm with an average 93% neutrophils.

Only 33 out of the 70 patients (47.14%) had a positive smear with either Gram-positive or Gram-negative organisms: 53.3% (24/45) in the acute group and 36% (9/25) in the subacute group. Seventy percent of patients (49/70) grew at least one organism in synovial cultures, 73% (33/45) in the acute and 64% (16/25) in the subacute groups. Polymicrobial infection (maximum of two organisms) was seen in six patients (8.5%), five in the acute group and one in the subacute group. Thirty percent of the patients (21/70) did not have a positive culture. In these 21 patients, the diagnosis of septic arthritis was made based on typical clinical features and turbid synovial fluid, as per the criteria described by Newman.[12]

S. aureus was the most common organism identified in culture – 38.1% (21/55). Streptococci were isolated in 27.2% (15/55), Gram-negative bacilli in 30.9% (17/55). There was one joint with enterococcus infection, and another with anaerobic Gram-positive cocci infection [Figure 2]. Among the 21 S. aureus-positive cultures, 13 were methicillin susceptible and 8 were methicillin resistant (38.09%). The incidence of methicillin resistance in the acute group was 50% (6/12) and in the subacute group was 22.2% (2/9). Overall, of the 49 positive cultures, 8 (16.3%) were MRSA. 30.6% (15/49) of cultures grew organisms that were not susceptible to first-line antibiotics. Eight of the 17 Gram-negative bacilli isolated in cultures (54%) were resistant to first-line antibiotics. All the Streptococcus species isolated were susceptible to penicillin.
Figure 2: Distributions of isolates in synovial fluid culture. (MRSA: Methicillin-resistant Staphylococcus aureus, MSSA: Methicillin-sensitive Staphylococcus aureus, NFGNB: Nonfermenting Gram-negative bacilli, STREPT: Streptococcus)

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Eighteen patients included in this study were elderly (age >60). Ten (55%) of these 18 patients grew at least one organism in culture. Of the 10 culture-positive cases, 5 (50%) grew Streptococcus species and 5 (50%) grew S. aureus. Two of the five staphylococcal strains were methicillin resistant. One patient had polymicrobial infection with Staphylococcus and Gram-negative bacteria.

About 8.57% (6/70) of patients required a second surgical procedure in view of uncontrolled infection after the initial arthrotomy and washout, of which two patients required amputation for disease control. Systemic bacteraemia was detected in 3 out of 70 patients on blood culture, with 2 patients growing the same organism in synovial fluid and blood. Eight patients required ICU admission in view of systemic complications including septicaemia, coagulopathy, liver failure or multi-organ dysfunction. Four of these eight patients were >60 years of age, but there was no death in this population as a direct result of septic arthritis. The mortality rate in the study group was 4.28% (3/70 patients). Septic arthritis was associated with significant residual morbidity in 70% of patients at 6 months follow-up in that they were not able to walk outside their homes without aids.


 ~ Discussion Top


The importance of early diagnosis and prompt management of pyogenic arthritis of joints cannot be ignored, considering the significant morbidity associated with the disease. The diagnosis of septic arthritis is primarily clinical. A four-point criteria has been described by Newman,[12] of which at least one should be present to make a diagnosis of septic arthritis – (i) isolation of a pathogenic organism from an affected joint; (ii) isolation of a pathogenic organism from another source (e.g., blood) in the context of a hot red joint suspicious of sepsis; (iii) typical clinical features and turbid joint fluid in the presence of previous antibiotic treatment; and (iv) post-mortem or pathological features suspicious of septic arthritis.

Majority of patients with septic arthritis were males (82.8%), which is similar to the demographics in other studies.[13] We also noted a high incidence of co-morbidities in patients with septic arthritis, with a third of all patients having diabetes.[4],[6] About a quarter of the patients in our series had a history of prior infection in the same limb or sepsis elsewhere, which is lower than stated in other studies, where the incidence has been reported to be up to 47%.[6]

Seventy-five percent of patients in this study sample presented with a history of fever. There has been a wide range reported in literature from 36% to 90%[3],[9] regarding the presence of fever at the time of presentation. Clinical suspicion of septic arthritis should be considered even in the absence of a typical history of high-grade fever, especially in high-risk groups that include the elderly, patients with diabetes mellitus, rheumatoid arthritis, recent joint surgery, haemodialysis, skin infections, corticosteroid injection into joints and immunosuppression.[4],[14],[15]

Not all patients with septic arthritis have a raised WBC count in the blood analysis. Significant leucocytosis (>11,000/cu.mm) was noted only in 66% of patients, and the average WBC count was 13,561/cu.mm. This finding is similar to previous studies.[16] CRP levels were found to be a better predictor of the infective process than leucocytosis in this study, even though, previous studies have failed to establish the predictive value of any inflammatory marker (leucocytosis, ESR or CRP) in septic arthritis.[4],[17]

Gram stain of the synovial fluid in our series was positive in <50% of the cases as compared to 70% culture positivity. This is similar to what has been previously reported by Weston et al., where he noted that Gram stain was positive in 50% of cases, as compared to 67% culture positivity.[3] With such a low-negative predictive value, Gram stain result should not be considered in isolation when a decision whether to do an arthrotomy is made, especially when the clinical features are suggestive of septic arthritis.

S. aureus was found to be the most common organism, as has been reported in other studies.[4],[18] We also noted a significant number of joint infections with other microbes like streptococci which were isolated in 27% of the positive cultures. This is much higher than the existing data, which varies from 1% to 16%.[4],[6] Among the Staphylococcus isolated in cultures, we noted a significant proportion of methicillin-resistant strains (MRSA), which is in keeping with the global trend.[19],[20],[21] A varied incidence of methicillin resistance among the Staphylococcus infections have been reported from different geographical areas between 15% in a European population,[8] up to 36%[9] and 42%[10] in the Latin American and Asian populations, respectively. In India, Sreenivasan et al. reported a 35% MRSA among 17 S. aureus-infected knees in their series of 26 patients with acute septic arthritis. A retrospective review on the incidence of MRSA in adult septic arthritis in an American population showed an alarming 50% incidence of MRSA among all culture-positive cases, and 60% methicillin resistance among all the S. aureus isolated in culture.[22] In this study, the incidence of MRSA among all culture-positive cases was only 16%. The rate of methicillin resistance among the staphylococci-infected joints (38%) was similar to the previously reported Asian data.[10],[11] The increased resistance to first-line antibiotics at presentation is also of concern.

Empirical antibiotic therapy for septic arthritis has conventionally been tailored to cover methicillin-sensitive S. aureus. However, with the growing incidence of MRSA strains and increased resistance to first-line antibiotics, this needs to be reconsidered, as previously suggested by Mathews et al.[4] MRSA should be empirically covered in high incidence geographical zones as well for vulnerable patient populations.

There was significant morbidity associated with septic arthritis, with over 70% of the patients reporting difficulty in walking even after 6 months. This could partly have been because of the late presentation, but could also represent the chondral damage caused by the infection. The high mortality rate of 4.25% is also of concern, and elderly patients with risk factors should be treated aggressively in order to reduce morbidity and mortality.

There are several limitations in this study. As the hospital is a tertiary care centre, it is possible that the study population may not be representative of the general population. It is also possible that some of the patients may have had partial treatment before admission, and this may have altered the microbiological profile. As the study was retrospective in nature, it is possible that all relevant clinical data were not entered. As regards long-term follow-up, though we were able to ascertain if the patients were community ambulant at 6 months, we did not formally assess their functional status with appropriate tools.


 ~ Conclusion Top


S. aureus is the most common pathogen in acute septic arthritis, with a high percentage of MRSA. All patients do not present with fever or raised WBC counts. The sensitivity of Gram stain is low, but CRP and ESR are usually raised. Changing sensitivity patterns of microbes point to a need for reconsidering empirical antibiotic therapy, especially in the elderly. Joint damage following infection can lead to significant disability and hence needs to be treated aggressively.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 ~ References Top

1.
Cooper C, Cawley MI. Bacterial arthritis in an English health district: A 10 year review. Ann Rheum Dis 1986;45:458-63.  Back to cited text no. 1
    
2.
Kaandorp CJ, Dinant HJ, van de Laar MA, Moens HJ, Prins AP, Dijkmans BA. Incidence and sources of native and prosthetic joint infection: A community based prospective survey. Ann Rheum Dis 1997;56:470-5.  Back to cited text no. 2
    
3.
Weston VC, Jones AC, Bradbury N, Fawthrop F, Doherty M. Clinical features and outcome of septic arthritis in a single UK health district 1982-1991. Ann Rheum Dis 1999;58:214-9.  Back to cited text no. 3
    
4.
Mathews CJ, Weston VC, Jones A, Field M, Coakley G. Bacterial septic arthritis in adults. Lancet 2010;375:846-55.  Back to cited text no. 4
    
5.
Morgan DS, Fisher D, Merianos A, Currie BJ. An 18 year clinical review of septic arthritis from tropical Australia. Epidemiol Infect 1996;117:423-8.  Back to cited text no. 5
    
6.
Ross JJ. Septic arthritis of native joints. Infect Dis Clin North Am 2017;31:203-18.  Back to cited text no. 6
    
7.
Coakley G, Mathews C, Field M, Jones A, Kingsley G, Walker D, et al. BSR & BHPR, BOA, RCGP and BSAC guidelines for management of the hot swollen joint in adults. Rheumatology (Oxford) 2006;45:1039-41.  Back to cited text no. 7
    
8.
Dubost JJ, Couderc M, Tatar Z, Tournadre A, Lopez J, Mathieu S, et al. Three-decade trends in the distribution of organisms causing septic arthritis in native joints: Single-center study of 374 cases. Joint Bone Spine 2014;81:438-40.  Back to cited text no. 8
    
9.
Helito CP, Noffs GG, Pecora JR, Gobbi RG, Tirico LE, Lima AL, et al. Epidemiology of septic arthritis of the knee at hospital das clínicas, universidade de São Paulo. Braz J Infect Dis 2014;18:28-33.  Back to cited text no. 9
    
10.
Chao CM, Lai CC, Hsueh PR. Bacteriology of septic arthritis at a regional hospital in Southern Taiwan. J Microbiol Immunol Infect 2013;46:241-2.  Back to cited text no. 10
    
11.
Sreenivas T, Nataraj AR, Menon J. Acute hematogenous septic arthritis of the knee in adults. Eur J Orthop Surg Traumatol 2013;23:803-7.  Back to cited text no. 11
    
12.
Newman JH. Review of septic arthritis throughout the antibiotic era. Ann Rheum Dis 1976;35:198-205.  Back to cited text no. 12
    
13.
Mue D, Salihu M, Awonusi F, Yongu W, Kortor J, Elachi I. The epidemiology and outcome of acute septic arthritis: A hospital based study. J West Afr Coll Surg 2013;3:40-52.  Back to cited text no. 13
    
14.
Kaandorp CJ, Van Schaardenburg D, Krijnen P, Habbema JD, van de Laar MA. Risk factors for septic arthritis in patients with joint disease. A prospective study. Arthritis Rheum 1995;38:1819-25.  Back to cited text no. 14
    
15.
Geirsson AJ, Statkevicius S, Víkingsson A. Septic arthritis in Iceland 1990-2002: Increasing incidence due to iatrogenic infections. Ann Rheum Dis 2008;67:638-43.  Back to cited text no. 15
    
16.
Goldenberg DL, Cohen AS. Acute infectious arthritis. A review of patients with nongonococcal joint infections (with emphasis on therapy and prognosis). Am J Med 1976;60:369-77.  Back to cited text no. 16
    
17.
Söderquist B, Jones I, Fredlund H, Vikerfors T. Bacterial or crystal-associated arthritis? Discriminating ability of serum inflammatory markers. Scand J Infect Dis 1998;30:591-6.  Back to cited text no. 17
    
18.
Murillo O, Grau I, Lora-Tamayo J, Gomez-Junyent J, Ribera A, Tubau F, et al. The changing epidemiology of bacteraemic osteoarticular infections in the early 21st century. Clin Microbiol Infect 2015;21:254.e1-8.  Back to cited text no. 18
    
19.
Arnold SR, Elias D, Buckingham SC, Thomas ED, Novais E, Arkader A, et al. Changing patterns of acute hematogenous osteomyelitis and septic arthritis: Emergence of community-associated methicillin-resistant Staphylococcus aureus. J Pediatr Orthop 2006;26:703-8.  Back to cited text no. 19
    
20.
Dubost JJ, Soubrier M, De Champs C, Ristori JM, Bussiére JL, Sauvezie B. No changes in the distribution of organisms responsible for septic arthritis over a 20 year period. Ann Rheum Dis 2002;61:267-9.  Back to cited text no. 20
    
21.
Gupta MN, Sturrock RD, Field M. A prospective 2-year study of 75 patients with adult-onset septic arthritis. Rheumatology (Oxford) 2001;40:24-30.  Back to cited text no. 21
    
22.
Frazee BW, Fee C, Lambert L. How common is MRSA in adult septic arthritis? Ann Emerg Med 2009;54:695-700.  Back to cited text no. 22
    


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