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Use of Erythrocyte Sedimentation Rate and C-Reactive Protein to Predict

Osteomyelitis Recurrence

Article  in  Journal of orthopaedic surgery (Hong Kong) · May 2016

DOI: 10.1177/230949901602400118

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Journal of Orthopaedic Surgery 2016;24(1):77-83

Use of erythrocyte sedimentation rate and

C-reactive protein to predict osteomyelitis
recurrence
Ziwei Lin,1 Anupama Vasudevan,2 Paul Anantharajah Tambyah2,3
1
Department of Emergency Medicine, National University Health System, Singapore
2
Yong Loo Lin School of Medicine, National University of Singapore, Singapore
3
Division of Infectious Diseases, University Medicine Cluster, National University Health System, Singapore

aureus. The cutoff points of CRP ≥5 mg/l and ESR ≥20

ABSTRACT
Purpose. To determine the association between
both erythrocyte sedimentation rate (ESR) and
C-reactive protein (CRP) and osteomyelitis
recurrence.
Methods. Records of 81 males and 27 females aged 10
to 87 (median, 54) years who underwent antibiotic/
surgical treatment for primary (n=68) or recurrent
(n=40) osteomyelitis that was related (n=26) or
unrelated (n=82) to a prosthesis were reviewed. Of
the 40 cases of osteomyelitis recurrence followed
up for a median of 23.4 (range, 0.6–74.0) months, 7
and 33 were related and unrelated to a prosthesis,
respectively. The cutoff points of lowest ESR and
CRP for osteomyelitis recurrence were calculated.
Risk factors for osteomyelitis recurrence were
determined.
Results. Osteomyelitis recurrence was associated
with diabetes mellitus, ischaemic heart disease, non-
healing wound, infection in the lower limb, and
infection with methicillin-resistant Staphylococcus
mm/h were used for osteomyelitis recurrence. Risk
factors for osteomyelitis recurrence were ESR ≥20
mm/h, infection with methicillin-resistant S aureus,
and infection in the lower limb.
Conclusion. ESR was more sensitive, specific,
and independently associated with osteomyelitis
recurrence and should be used to guide the duration
of antibiotic treatment.
Key words: blood sedimentation; C-reactive protein;
osteomyelitis; recurrence
INTRODUCTION
Osteomyelitis is a chronic condition prone to
recurrence and is associated with morbidity and
decreased quality of life.1–3 Inflammatory markers
such as erythrocyte sedimentation rate (ESR)
and C-reactive protein (CRP) have been used to
predict osteomyelitis recurrence.4 ESR reflects the
concentration of fibrinogen and immunoglobulins in
the plasma.5 CRP is a marker for acute inflammation

Address correspondence and reprint requests to: Dr Ziwei Lin, Department of Emergency Medicine, National University Hospital,
level 1, 1 Main building, 5 Lower Kent Ridge Road, Singapore 119074. Email: ziwei.lin@mohh.com.sg
78 Z Lin et al. Journal of Orthopaedic Surgery

and is used for diagnosis of septic arthritis, acute generally over 90%, especially when combined with
rheumatic fever, and acute osteomyelitis.6 The white blood cell counts.6–9
sensitivity and specificity of ESR and CRP alone The decision to stop antibiotic therapy for
or in combination for diagnosis of osteomyelitis is osteomyelitis is based on the resolution of overlying

Table 1
Patient characteristics and outcomes
Characteristic Overall osteomyelitis
Recurrence No recurrence Unadjusted HR p Value
(95% CI)
Gender 0.73 (0.37–1.43) 0.360
Male 28 (34.6) 53 (65.4)
Female 12 (44.4) 15 (55.6)
Median (range) age (years) 54 (10–87)
No. of patients whose age ≥median 22 (39.3) 34 (60.7) 1.17 (0.63–2.18) 0.624
Co-morbidities
Diabetes mellitus 28 (48.3) 30 (51.7) 2.42 (1.23–4.77) 0.011
Hypertension 22 (39.3) 34 (60.7) 1.27 (0.68–2.37) 0.450
Dyslipidaemia 12 (31.6) 26 (68.4) 0.82 (0.42–1.63) 0.585
Peripheral vascular diseases 8 (53.3) 7 (46.7) 1.65 (0.76–3.58) 0.207
Ischaemic heart disease 11 (55.0) 9 (45.0) 2.09 (1.04–4.20) 0.038
Previous osteomyelitis 7 (53.8) 6 (46.2) 1.43 (0.63–3.25) 0.387
Symptoms
Pain 24 (42.1) 33 (57.9) 1.44 (0.76–2.71) 0.261
Fever 16 (40.0) 24 (60.0) 1.25 (0.66–2.35) 0.492
Swelling 14 (38.9) 22 (61.1) 1.12 (0.58–2.17) 0.744
Warmth 7 (41.2) 10 (58.8) 1.11 (0.49–2.53) 0.808
Erythema 10 (37.0) 17 (63.0) 1.01 (0.49–2.09) 0.978
Purulent discharge 18 (46.2) 21 (53.8) 1.58 (0.84–3.00) 0.159
Non-healing wound 31 (50.0) 31 (50.0) 2.95 (1.40–6.20) 0.004
History of trauma 11 (26.2) 31 (73.8) 0.52 (0.26–1.05) 0.067
Open trauma 5 (20.8) 19 (79.2) 0.62 (0.18–2.13) 0.444
Prosthesis present 7 (26.9) 19 (73.1) 0.61 (0.27–1.38) 0.235
Site of infection
Single 37 (36.3) 65 (63.7) 0.53 (0.16–1.71) 0.284
Multiple 3 (50.0) 3 (50.0) - -
Upper limb 1 (10.0) 9 (90.0) 0.21 (0.03–1.52) 0.121
Lower limb 32 (46.4) 37 (53.6) 2.90 (1.33–6.30) 0.007
Spine 3 (23.1) 10 (76.9) 0.52 (0.16–1.68) 0.271
Others 5 (29.4) 12 (70.6) 0.67 (0.26–1.70) 0.397
Microorganism
Isolated 32 (34.8) 60 (65.2) 0.68 (0.32–1.49) 0.336
Unknown 8 (50.0) 8 (50.0)
Single microbe 20 (29.4) 48 (70.6) 0.54 (0.26–1.10) 0.089
Mixed infection 12 (50.0) 12 (50.0)
Staphylococcus aureus 6 (26.1) 17 (73.9) 0.58 (0.24–1.38) 0.216
Methicillin-resistant S aureus 11 (57.9) 8 (42.1) 2.42 (1.21– 4.85) 0.013
Other Gram-positive microbe 7 (38.9) 11 (61.1) 1.23 (0.54–2.78) 0.620
Pseudomonas aeruginosa 4 (20.0) 16 (80.0) 0.42 (0.15–1.18) 0.099
Other Gram-negative microbe 10 (37.0) 17 (63.0) 0.94 (0.46–1.92) 0.866
Antibiotic therapy
Intravenous antibiotics 40 (37.0) 68 (63.0) - -
Parenteral antibiotics ≥4 weeks 24 (54.5) 20 (45.5) 1.41 (0.75–2.65) 0.292
Surgical intervention 30 (37.5) 50 (62.5) 1.04 (0.51–2.14) 0.906
Debridement 20 (35.7) 36 (64.3) 0.95 (0.51–1.76) 0.858
Amputation 7 (41.2) 10 (58.8) 1.14 (0.50–2.58) 0.754
Removal of implant - - - -
Vol. 24 No. 1, April 2016 Use of ESR and CRP to predict osteomyelitis recurrence 79

soft tissue infection, healing of the wound, to stop antimicrobial therapy for osteomyelitis has
radiographic evidence of healing, and the decline not been established. This study aimed to determine
of inflammatory markers.4 Nonetheless, the cutoff the association between both ESR and CRP and
points for specific inflammatory markers at which osteomyelitis recurrence.

Prosthesis-related osteomyelitis Prosthesis-unrelated osteomyelitis

Recurrence No Unadjusted HR p Value Recurrence No Unadjusted HR p Value
recurrence (95% CI) recurrence (95% CI)
0.27 (0.05–1.44) 0.125 0.91 (0.43–1.91) 0.803
5 (21.7) 18 (78.3) 23 (39.7) 35 (60.3)
2 (66.7) 1 (33.3) 10 (41.7) 14 (58.3)
52 (25–75) - 56 (10–87)
4 (30.8) 9 (69.2) 1.62 (0.36–7.27) 0.531 15 (36.6) 26 (63.4) 0.75 (0.38–1.49) 0.416

4 (40.0) 6 (60.0) 2.07 (0.46–9.25) 0.343 24 (50.0) 24 (50.0) 2.42 (1.12–5.22) 0.024
3 (27.3) 8 (72.7) 1.11 (0.25–4.96) 0.894 19 (42.2) 26 (57.8) 1.27 (0.64–2.53) 0.500
1 (12.5) 7 (87.5) 0.38 (0.05–3.18) 0.373 11 (36.7) 19 (63.3) 0.92 (0.44–1.89) 0.813
0 (0.0) 2 (100.0) 0.04 (0–3478) 0.585 8 (61.5) 5 (38.5) 1.91 (0.86–4.24) 0.112
2 (66.7) 1 (33.3) 4.35 (0.82–23.13) 0.085 9 (52.9) 8 (47.1) 1.80 (0.83–3.87) 0.135
0 (0.0) 3 (100.0) 0.04 (0.00–469.9) 0.500 7 (70.0) 3 (30.0) 1.88 (0.81–4.35) 0.141

3 (27.3) 8 (72.7) 1.13 (0.25–5.05) 0.873 21 (45.7) 25 (54.3) 1.43 (0.70–2.91) 0.323
2 (33.3) 4 (66.7) 1.19 (0.23–6.14) 0.836 14 (41.2) 20 (58.8) 1.17 (0.59–2.33) 0.659
1 (16.7) 5 (83.3) 0.59 (0.07–4.91) 0.625 13 (43.3) 17 (56.7) 1.15 (0.56–2.38) 0.697
2 (40.0) 3 (60.0) 1.40 (0.27–7.25) 0.685 5 (41.7) 7 (58.3) 1.05 (0.40–2.76) 0.920
3 (50.0) 3 (50.0) 3.49 (0.77–15.78) 0.105 7 (33.3) 14 (66.7) 0.71 (0.31–1.67) 0.435
4 (40.0) 6 (60.0) 2.00 (0.45–8.96) 0.363 14 (48.3) 15 (51.7) 1.51 (0.74–3.06) 0.257
6 (42.9) 8 (57.1) 5.39 (0.65–44.79) 0.119 25 (52.1) 23 (47.9) 2.64 (1.19–5.86) 0.017
5 (23.8) 16 (76.2) 0.59 (0.11–3.07) 0.533 6 (28.6) 15 (71.4) 0.56 (0.23–1.35) 0.196
2 (20.0) 8 (80.0) 0.83 (0.34–2.02) 0.674 3 (21.4) 11 (78.6) 0.71 (0.29–1.75) 0.461
- - - - - - - -

6 (24.0) 19 (76.0) 0.04 (0.003–0.65) 0.024 31 (40.3) 46 (59.7) 0.85 (0.20–3.56) 0.826
1 (100.0) 0 (0.0) - - 2 (40.0) 3 (60.0) - -
1 (20.0) 4 (80.0) 0.69 (0.08–5.74) 0.732 0 (0.0) 5 (100.0) 0.04 (0–11.5) 0.271
5 (38.5) 8 (61.5) 3.01 (0.58–15.6) 0.189 27 (48.2) 29 (51.8) 2.65 (1.09–6.42) 0.031
0 (0.0) 1 (100.0) 0.05 (0–317000) 0.702 3 (25.0) 9 (75.0) 0.50 (0.15–1.64) 0.252
2 (25.0) 6 (75.0) 0.87 (0.17–4.47) 0.863 3 (33.3) 6 (66.7) 0.71 (0.22–2.33) 0.574

8 (33.3) 18 (66.7) 0.74 (0.26–2.14) 0.577 26 (38.2) 42 (61.8) 0.87 (0.57–1.32) 0.508
1 (50.0) 1 (50.0) 7 (50.0) 7 (50.0)
4 (22.2) 14 (77.8) 0.85 (0.36–1.99) 0.709 16 (32.0) 34 (68.0) 0.70 (0.47–1.05) 0.082
2 (33.3) 4 (66.7) 10 (55.6) 8 (44.4)
1 (11.1) 8 (88.9) 0.27 (0.03–2.28) 0.231 5 (35.7) 9 (64.3) 0.79 (0.31–2.05) 0.627
1 (20.0) 4 (80.0) 0.72 (0.09–5.96) 0.758 10 (71.4) 4 (28.6) 3.22 (1.52–6.79) 0.002
3 (60.0) 2 (40.0) 4.72 (1.02–21.9) 0.047 4 (30.8) 9 (69.2) 0.80 (0.28–2.27) 0.671
0 (0.0) 2 (100.0) 0.04 (0–3478.38) 0.585 4 (22.2) 14 (77.8) 0.42 (0.15–1.18) 0.099
1 (20.0) 4 (80.0) 0.64 (0.08–5.30) 0.677 9 (40.9) 13 (59.1) 0.96 (0.45–2.08) 0.924

7 (26.9) 19 (73.1) - - 33 (40.2) 49 (59.8) - -

6 (37.5) 10 (62.5) 4.95 (0.59–41.3) 0.139 18 (42.9) 24 (57.1) 1.17 (0.59–2.33) 0.646
6 (26.1) 17 (73.9) 0.84 (0.1–6.96) 0.868 24 (42.1) 33 (57.9) 1.17 (0.54–2.51) 0.696
6 (30.0) 14 (70.0) 2.11 (0.25–17.5) 0.490 14 (38.9) 22 (61.1) 0.95 (0.48–1.90) 0.884
0 (0.0) 0 (0.0) - - 7 (41.2) 10 (58.8) 1.00 (0.43–2.29) 0.990
5 (26.3) 14 (73.7) 0.99 (0.19–5.11) 0.990 - - - -
80 Z Lin et al. Journal of Orthopaedic Surgery

Table 2
Sensitivity, specificity, positive and negative predictive values (PPV and NPV) of lowest C-reactive protein (CRP) and eryth-
rocyte sedimentation rate (ESR) for predicting osteomyelitis recurrence

Parameter Overall osteomyelitis

Sensitivity Specificity PPV NPV OR (95% CI) p Value
CRP (mg/l)
5 62.5 58.8 47.2 72.7 2.00 (1.05–3.76) 0.036
6 60.0 66.2 51.1 73.8 2.29 (1.22–4.31) 0.010
7 57.5 72.1 54.8 74.2 2.63 (1.40–4.93) 0.003
8 57.5 75.0 57.5 75.0 2.94 (1.57–5.52) 0.001
9 55.0 76.5 57.9 74.3 2.85 (1.53–5.33) 0.001
ESR (mm/h)
20 85.0 52.9 51.5 85.7 4.67 (1.96–11.2) 0.001
25 80.0 58.8 53.3 83.3 4.22 (1.94–9.19) <0.001
30 75.0 61.8 53.6 80.8 3.71 (1.81–7.61) <0.001

MATERIALS AND METHODS
This study was approved by the National Healthcare
Group Domain Specific Review Board. Records of
81 males and 27 females aged 10 to 87 (median, 54)
years who underwent antibiotic/surgical treatment
for primary (n=68) or recurrent (n=40) osteomyelitis
that was related (n=26) or unrelated (n=82) to a
prosthesis between January 2005 and January 2012
were reviewed. Of the 40 cases of osteomyelitis
recurrence followed up for a median of 23.4 (range,
0.6–74.0) months, 7 and 33 were related and unrelated
to a prosthesis, respectively.
The diagnosis of osteomyelitis was made when
the patients presented signs and symptoms of bone
and/or joint infection of <2 weeks, and at least
one of the following: (1) positive blood or tissue
culture, (2) typical radiological findings (deep soft-
tissue swelling, periosteal reaction, and/or bony
destruction), and (3) surgical finding of pus in bone
and/or joint.10 Osteomyelitis recurrence was defined
as re-admission for antibiotic/surgical treatment for
osteomyelitis of the same site as the index admission.
This was differentiated from persistent osteomyelitis
in which antibiotics were continued and had not been
stopped. Patients with fewer than 2 CRP and ESR
readings were excluded.
The date of initial presentation of osteomyelitis
was defined as time 0, whereas the end of follow-
up was defined as the date of the last attendance
or the date of re-admission (for recurrence). Patient
age, gender, comorbidities, symptoms, site of
osteomyelitis, microbiological results, and treatment
options were recorded for analysis.
The cutoff points for osteomyelitis recurrence
were determined separately for the lowest ESR and
CRP using the area under the curve (AUC) in the
receiver operating characteristic analysis. Risk factors
for osteomyelitis recurrence were determined using
the multivariable Cox regression analysis. Variables
were found not to violate the proportional hazards
assumption. All tests were 2-sided. A p value of <0.05
was considered statistically significant.
RESULTS
In univariate analysis, overall osteomyelitis
recurrence was associated with diabetes mellitus
(48.3% vs. 51.7%, unadjusted HR=2.42, 95% CI=1.23–
4.77, p=0.011), ischaemic heart disease (55.0% vs.
45.0%, unadjusted HR=2.09, 95% CI=1.04–4.20,
p=0.038), non-healing wound (50.0% vs. 50.0%,
unadjusted HR=2.95, 95% CI=1.40–6.20, p=0.004),
infection in the lower limb (46.4% vs. 53.6%,
unadjusted HR=2.90, 95% CI=1.33–6.30, p=0.007),
and infection with methicillin-resistant Staphylococcus
aureus (57.9% vs. 42.1%, unadjusted HR=2.42, 95%
CI=1.21–4.85, p=0.013) [Table 1].
The cutoff points that had high sensitivity
and specificity were CRP 5, 6, 7, 8, and 9 mg/l and
ESR ≥20, 25, and 30 mm/h (Table 2). For overall
osteomyelitis recurrence, the cutoff points of CRP
≥5 mg/l (sensitivity=62.5%, specificity=58.8%) and
ESR ≥20 mm/h (sensitivity 85.0%, specificity 52.9%)
were used because their sensitivity was highest. For
prosthesis-related osteomyelitis recurrence, the cutoff
points of CRP ≥5 mg/l (AUC=0.820, sensitivity=71.4%,
specificity=84.2%) and ESR ≥20 mm/h (AUC=0.782,
sensitivity=85.7%, specificity=73.7%) were used.
For prosthesis-unrelated osteomyelitis recurrence,
the cutoff points of CRP ≥8 mg/l (AUC=0.603,
Vol. 24 No. 1, April 2016 Use of ESR and CRP to predict osteomyelitis recurrence 81

Prosthesis-related osteomyelitis Prosthesis-unrelated osteomyelitis

Sensitivity Specificity PPV NPV OR (95% CI) p Value Sensitivity Specificity PPV NPV OR (95% CI) p Value

71.4 84.2 62.5 88.9 6.73 (1.30–34.9) 0.023 60.6 49.0 44.4 64.9 1.42 (0.71–2.85) 0.328
71.4 89.5 71.4 89.5 8.70 (1.67–45.3) 0.010 57.6 57.1 47.5 66.7 1.62 (0.81–3.24) 0.171
57.1 89.5 66.7 85.0 5.81 (1.28–26.2) 0.022 57.6 65.3 52.8 69.6 2.11 (1.06–4.22) 0.034
57.1 89.5 66.7 85.0 5.81 (1.28–26.2) 0.022 57.6 69.4 55.9 70.8 2.43 (1.22–4.87) 0.012
57.1 94.7 80.0 85.7 8.31 (1.82–37.9) 0.006 54.5 69.4 54.5 69.4 2.19 (1.10–4.35) 0.026

85.7 73.7 54.5 93.3 11.1 (1.33–93.2) 0.026 84.8 44.9 50.9 81.5 3.46 (1.33–8.98) 0.011
71.4 73.7 50.0 87.5 5.73 (1.10–29.9) 0.038 81.8 53.1 54.0 81.3 3.69 (1.52–8.96) 0.004
71.4 73.7 50.0 87.5 5.73 (1.10–29.9) 0.038 75.8 57.1 54.3 77.8 3.18 (1.43–7.06) 0.005

Table 3
Independent risk factors for osteomyelitis recurrence
Risk factor Adjusted hazard ratio (95% CI) p Value
Overall osteomyelitis
Erythrocyte sedimentation rate ≥20 mm/h 4.17 (1.73–10.0) 0.001
Methicillin-resistant Staphylococcus aureus 2.64 (1.31–5.33) 0.007
Lower limb osteomyelitis 2.44 (1.12–5.34) 0.025
Prosthesis-related osteomyelitis
C-reactive protein ≥5 mg/l 10.7 (1.67–68.6) 0.012
Other Gram-positive microorganisms 9.09 (1.39–59.4) 0.021
Prosthesis-unrelated osteomyelitis
Erythrocyte sedimentation rate ≥25 mm/h 3.89 (1.60–9.47) 0.003
Methicillin-resistant S aureus 3.46 (1.63–7.34) 0.001

sensitivity=57.6%, specificity=69.4%) and ESR DISCUSSION

≥25 mm/h (AUC=0.659, sensitivity=81.8%,
specificity=53.1%) were used.
In multivariable Cox regression analysis, risk
factors for overall osteomyelitis recurrence were ESR
≥20 mm/h (adjusted HR=4.17, 95% CI=1.73–10.0,
p=0.001), infection with methicillin-resistant S aureus
(adjusted HR=2.64, 95% CI=1.31–5.33, p=0.007), and
infection in the lower limb (adjusted HR=2.44, 95%
CI=1.12–5.34, p=0.025) [Table 3]. Risk factors for
prosthesis-related osteomyelitis were CRP ≥5 mg/l
(adjusted HR=10.7, 95% CI=1.67–68.6, p=0.012) and
infection with gram-positive microorganisms other
than S aureus (adjusted HR=9.09, 95% CI=1.39–
59.4, p=0.021). Risk factors for prosthesis-unrelated
osteomyelitis were ESR ≥25 mm/h (adjusted
HR=3.89, 95% CI=1.60–9.47, p=0.003) and infection
with methicillin-resistant S aureus (adjusted HR=3.46,
95% CI=1.63–7.34, p=0.001).
Inflammatory markers have been used to monitor
treatment progress. In a study investigating the
efficacy of inflammatory markers (CRP, ESR, white
blood cell counts, and procalcitonin) in diagnosis
and monitoring patients with foot osteomyelitis, only
ESR remained elevated in the presence of persistent
osteomyelitis at one week post-treatment until 3
months.9 Failure of ESR to normalise suggested
a need for re-evaluation and may be associated
with recurrence despite initial clinical resolution.11
In a study of 16 patients with contiguous pedal
osteomyelitis, failure of ESR to decline predicted
treatment failure.12 ESR >55 mm/h and CRP >27.5
mg/l at 4 weeks after antibiotic treatment was
associated with a higher rate of treatment failure
(defined as disease progression and recurrence) (odds
ratio [OR]=5.2, 95% CI=1.00–26.6, p=0.04) in pyogenic
82 Z Lin et al. Journal of Orthopaedic Surgery

vertebral osteomyelitis.13 In a study involving 122
patients with diabetic foot osteomyelitis, stagnating
trajectories of CRP and ESR were reported to be
associated with recurrence and readmission over a
follow-up period of one year.14
Bone and joint infection with methicillin-resistant
S aureus is reported to be associated with failure of
initial prescription of outpatient parenteral antibiotic
therapy (OR=3.3, 95% CI=1.2–9.5, p=0.03) and failure
of initial therapy defined as recurrence or death
after a median of 60 weeks (HR=2.2, 95% CI=1.1–3.3,
p=0.009).15
Prosthesis-related osteomyelitis is difficult to treat,
owing to adherence of bacteria to biomaterials and
tissues within biofilms.16 ESR and CRP are effective in
determining the presence of peri-prosthetic infection;
using both can reduce the chance of false-negative
results.17–20 Nonetheless, recurrence may occur years
later.21
There were limitations to the study. The study
was retrospective, and 25 patients were excluded
because of inadequate readings of CRP and ESR.
Patient selection may have been biased because
only patients in the inpatient setting were included.
The number of patients with prosthesis-related
osteomyelitis was insufficient for further analysis.
The distinction between persistent and recurrent
osteomyelitis may not have been absolute; some sub-
clinical persistent osteomyelitis cases may have been
counted as recurrent osteomyelitis. Owing to the
retrospective nature of the study, patients were not
clinically examined to confirm the resolution of the
osteomyelitis.
CONCLUSION
ESR was more sensitive, specific, and independently
associated with osteomyelitis recurrence and
should be used to guide the duration of antibiotic
treatment.
DISCLOSURE
No conflicts of interest were declared by the authors.

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