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Original Research |
1 Department of Radiology, Beth Israel Deaconess Medical Center, 330 Brookline
Ave., Shapiro 4th Fl., Boston, MA 02215.
2 Department of Radiology, Hahnemann University Hospital, Philadelphia,
PA.
3 Department of Radiology, Thomas Jefferson Medical College, Philadelphia,
PA.
4 Department of Diagnostic Radiology, Yale University, New Haven, CT.
Received September 27, 2006;
accepted after revision January 26, 2007.
Address correspondence to J. S. Wu
(jswu{at}bidmc.harvard.edu).
Abstract
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MATERIALS AND METHODS. A retrospective review was performed of 800
consecutive patients undergoing imaging-guided core bone biopsies at two
institutions. Seventy-five biopsies were performed for suspected osteomyelitis
and 41 patients had histologically proven osteomyelitis. A chart review was
performed to determine whether the following factors affected the culture
result: histologic type of osteomyelitis, antibiotic therapy before biopsy,
fever (temperature 
38.0°C), elevated WBC count ( 10 x
103 µL), elevated erythrocyte sedimentation rate (ESR) ( 10
mm/h), elevated C-reactive protein value (CRP) ( 6 mg/L), the size of the
biopsy needle, and the amount of purulent fluid obtained at biopsy.
RESULTS. Of the 41 cases of osteomyelitis, 14 (34%) had positive
cultures. Eighteen (44%) of 41 cases were chronic osteomyelitis. Seventeen
(41%) of 41 patients received antibiotics before biopsy, seven (17%) were
febrile, five (12%) had an elevated WBC count, 16 (39%) had an elevated ESR,
and six (15%) had an elevated CRP value. The biopsy needle size ranged from
11- to 18-gauge. These factors did not have any significant association with
positive or negative culture results. Purulent fluid was aspirated in 10 (24%)
of the 41 cases. In six (15%) of the cases, 2 mL of purulent fluid was
aspirated and five (83%) of the six cases were associated with positive
culture (p =0.02).
CONCLUSION. The rate of positive culture results in histologically
proven cases of osteomyelitis obtained from imaging-guided bone biopsies is
low. Aspirating 2 mL of purulent fluid is associated with a significantly
higher rate of positive cultures.
Keywords: biopsy • bone • CT • fluoroscopy • infectious diseases • osteomyelitis
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Although clinical symptoms; inflammatory markers in the blood; and findings on MRI, leukocyte scintigraphy, and PET can suggest osteomyelitis, the definitive diagnosis of osteomyelitis is made by culturing an organism directly from the site of infection [3–6]. The identification of a causative organism by culture both confirms osteomyelitis and allows tailoring of antimicrobial therapy; however, cultures from samples obtained during surgery or by imaging guidance are often negative. Several studies suggest that 40–60% of histologically proven cases of osteomyelitis at surgery or biopsy are negative at culture, but many of these studies involve small patient populations [5–8].
The factors that predict positive or negative culture results are unknown. Treatment with antimicrobial therapy around the time of tissue sampling, small biopsy tissue volume, and sampling error are factors that may affect culture results [2, 9–12]. In several studies, investigators have stressed the importance of sending both histologic and microbiologic samples at the time of biopsy given the low rate of positive culture [5–7, 11]. Clinical and laboratory factors associated with osteomyelitis include fever, elevated WBC count, elevated erythrocyte sedimentation rate (ESR), and elevated C-reactive protein value (CRP). Unfortunately, many of these factors can be negative at clinical presentation, and some studies indicate that these factors are best reserved for monitoring treatment rather than determining diagnosis [3, 5, 11].
Imaging-guided bone biopsy with CT or fluoroscopy is a useful technique in diagnosing osteomyelitis and is the preferred initial technique for obtaining both histologic and microbiologic samples. This procedure can be performed on an outpatient basis, and complication rates are low [13–15].
For this study, we determined the rate of positive culture in histologically proven cases of osteomyelitis obtained from imaging-guided biopsies and identified clinical or technical factors associated with positive or negative culture results. We hypothesized that the culture positivity rate would be low and that certain clinical and technical factors would affect the culture positivity rate.
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Musculoskeletal radiologists at the two institutions obtained samples using standard coaxial bone biopsy techniques [18–20]. Most of the biopsies were performed with either a 15-gauge needle (1.7-mm-diameter bore) (Bonopty, Radi Medical Systems) or a 14-gauge needle (2.03-mm-diameter bore) (Elson/Ackerman, Cook). At the beginning of the procedure, the target lesion was localized under CT or fluoroscopy guidance. Once the patient had received appropriate local anesthetic and was under conscious sedation, a penetration cannula was placed adjacent to the outer cortex of the lesion. Subsequently, a biopsy cannula was used to obtain core bone samples. An average of three samples were obtained at both institutions. Aspiration of the lesion for purulent fluid is attempted during each biopsy. At least one core sample was sent for microbiologic analysis.
We defined a positive case of osteomyelitis for this study as a histologic report indicating acute osteomyelitis, chronic osteomyelitis, or acute and chronic osteomyelitis. Cases of acute osteomyelitis showed the presence of acute inflammatory cells, congestion or thrombosis of medullary or periosteal small vessels, and necrotic bone. Cases of chronic osteomyelitis exhibited areas of woven bone and fibrosis with large numbers of lymphocytes, histiocytes, and plasma cells in the absence of neutrophils. Features of both were seen in cases of acute and chronic osteomyelitis. Forty-one of the 75 patients (55%) had a histologic diagnosis of osteomyelitis. For microbiologic analysis, we considered a culture positive if any organism grew.
We performed a chart review of the 41 histologically positive cases of
osteomyelitis to determine whether the following factors contributed to
positive or negative culture results: histologic type of osteomyelitis (acute
or chronic), antibiotic therapy before biopsy, fever (temperature
38.0°C), elevated WBC count ( 10 x 103 µL),
elevated ESR ( 10 mm/h), elevated CRP value ( 6 mg/L), biopsy needle
size, and the amount of purulent fluid obtained at biopsy. For the purposes of
this study, histology samples interpreted as "acute osteomyelitis"
or as "acute and chronic osteomyelitis" were considered to be
cases of acute osteomyelitis. A patient was considered to have received
antibiotic therapy if any dose was given within 24 hours before the biopsy.
Patients at both institutions are asked to discontinue antibiotic therapy for
at least 24 hours before biopsy, if feasible. The definition of
"fever" was a temperature of 38.0°C within 7 days of the
biopsy. A subject had an elevated WBC count, ESR, or CRP value if the values
were elevated at any time from initial presentation to the time of biopsy. We
also documented the biopsy needle gauge and the amount of purulent fluid
aspirated at biopsy.
Analyses were conducted using SAS software (version 8.02, SAS Institute). We calculated p values from the chi-square test or Fisher's exact test for categoric variables and from the Wilcoxon's rank sum test for ordinal or continuous variables. Finally, we compared the histologic and microbiologic data from the surgical biopsy or débridement with the preceding imaging-guided biopsy results.
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Of the 41 histologically positive cases of osteomyelitis, 14 (34%) cases
were positive at culture. Staphylococcus aureus was the most common
organism cultured, detected in eight (57%) of the 14. The culture positivity
rate did not vary with patient sex, by type of imaging guidance, or between
the two institutions (Table 2).
Moreover, no significant difference in the culture positivity rate was seen
with regard to acute versus chronic osteomyelitis, antibiotic therapy before
biopsy, fever, elevated WBC count, elevated ESR, elevated CRP value, or biopsy
needle size (Table 2). Purulent
fluid was aspirated in 10 (24%) of the 41 cases and five (50%) of 10 grew an
organism at culture (p = 0.22). Of the 31 cases for which no purulent
fluid was aspirated at biopsy, only nine (29%) of the 31 cultures were
positive. Of the six patients from whom 2 mL of purulent fluid was
aspirated, five (83%) had positive culture (p = 0.02)
(Table 2).
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Surgical biopsy or débridement was performed in 10 (24%) of the 41 histologically positive cases of osteomyelitis: four surgeries in patients with positive cultures and six surgeries in patients with negative cultures (Table 3). In nine of the 10 surgical cases, acute or chronic osteomyelitis was the histologic diagnosis, compatible with the imaging-guided biopsy result. In the 10th case, the surgical specimen was nondiagnostic and no histologic result was given; however, the culture specimen was positive. Of the four cases with positive culture results from the imaging-guided biopsy, two grew S. aureus, which is identical to the imaging-guided biopsy culture results. No growth occurred in the other two cases; however, both of these patients received antibiotics during the time interval between the imaging-guided biopsy and the surgical procedure. Of the six culture-negative cases at imaging-guided biopsy that underwent surgery, four cases had no growth at culture similar to the imaging-guided biopsy results. The other two cases grew organisms from the surgical specimen.
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Although imaging-guided bone biopsies are relatively safe [13–15], the referring clinician and radiologist should be aware of the low culture positivity rate. Thus, in cases in which the diagnosis of osteomyelitis is obvious, performing a biopsy for the sole purpose of attaining an organism to guide antimicrobial treatment must be performed with caution. This is most important in cases in which the risk of adjacent tissue injury or seeding of noninfected tissue is high. The most common organism found at culture was S. aureus, seen in 57% of the cultures, which is consistent with the results of other studies [1, 11, 16, 21]. Dich et al. [21] evaluated 163 cases of osteomyelitis and found S. aureus to be the most common etiologic agent, seen in 61% of cases.
With regard to clinical, laboratory, and biopsy-related factors associated
with culture positivity or negativity, we found only one significant
association: the aspiration of 2 mL of purulent fluid at biopsy.
Histologic type of osteomyelitis (acute or chronic), antibiotic therapy before
biopsy, fever, elevated WBC count, elevated ESR, elevated CRP value, and
biopsy needle size did not have a significant association with positive or
negative cultures. These results have several implications.
First, the aspiration of 2 mL of purulent fluid at biopsy was the only
factor associated with a higher culture positivity rate. When no purulent
fluid was obtained, only 29% of cases were positive at culture. The culture
positivity rate increased to 50% if any purulent fluid was aspirated and rose
to 83% if 2 mL of purulent fluid was obtained. Intuitively, this
finding—that culture yield would increase as the amount of organisms
obtained at biopsy increases—seems reasonable. This finding suggests
that performing biopsies in suspected cases of intraosseous or periosseous
abscess is useful, especially if the abscess is large. Thus, if fluid
collections can be seen on imaging, the culture yield from these biopsies may
be higher and may warrant the procedure, especially in more hazardous
situations.
Second, radiologists commonly request that patients discontinue antimicrobial therapy for at least 24 hours before biopsy to have the highest chance of isolating an organism. Although this difference was not statistically significant, we did detect a lower culture positivity rate in the patients on antimicrobial therapy before biopsy versus the patients off therapy. Of the patients who received antibiotic therapy within 24 hours of the biopsy, 24% had a positive culture, whereas the patients who did not receive antibiotics had a 42% culture positivity rate. Larger prospective studies are needed to further investigate this finding. Given our results, we have maintained our requests to referring clinicians to discontinue antibiotics for at least 24 hours before biopsy.
Third, although one may hypothesize that a larger biopsy needle size would lead to a higher likelihood of culture positivity due to a larger sample volume, our results suggest no difference in culture positivity rates between the two predominant needle sizes used, 14- and 15-gauge. Unfortunately, the two main needles used did not differ much in size.
Finally, there was good correlation of both the histologic and microbiologic results from the imaging-guided biopsies and surgical procedures. Aside from one nondiagnostic surgical specimen, all surgical samples were positive for osteomyelitis and were histologically identical to the imaging-guided biopsy results. In no cases did organisms isolated from the imaging-guided biopsy differ with those attained at surgery. These results suggest that imaging-guided bone biopsies are accurate procedures, which is similar to the results of past studies [2, 5, 6, 9].
Despite the strengths of our study, a few limitations deserve mention. Our sample size may not be large enough to detect a significant difference in histologic type of osteomyelitis, antibiotic therapy before biopsy, WBC count, ESR, CRP value, or size of biopsy needle in the groups who had positive and negative cultures. Although osteomyelitis is common, requests for imaging-guided biopsies for osteomyelitis are relatively uncommon. Our study consists of 800 bone biopsies over a 7- and an 8-year period at two large tertiary care centers, with only 75 biopsies performed for suspected osteomyelitis. This is only 3–7 cases per year for each institution. Often patients with clear clinical or laboratory data suggesting osteomyelitis are treated with antibiotics or are taken directly to surgery without undergoing an imaging-guided biopsy. For instance, a patient with diabetes who has a draining foot ulcer with exposed bone is unlikely to need imaging-guided biopsy to diagnosis osteomyelitis. The cases referred for biopsy are often in patients for whom the diagnosis is difficult. Despite the low numbers, the similar culture positivity rates between the two institutions (31% and 36%) suggest that the 34% combined culture positivity rate is accurate.
In addition, the 24-hour antibiotic-free interval used in this study is somewhat arbitrary, considering some patients with chronic renal failure in whom the serum level of antibiotics may be high. Nevertheless, we consider this parameter to be acceptable because it is current practice at both institutions is to discontinue antibiotics at least 24 hours before biopsy.
Another limitation of the study pertains to using positive histology as the diagnostic standard in the study. Although this may not be optimal, we are likely underdiagnosing, not overdiagnosing, cases of osteomyelitis. Sampling error will reduce the accuracy of histology by increasing the number of false-negatives; however, the positive cases at histology are likely true cases of osteomyelitis. The histologic definition of acute osteomyelitis is fairly specific; thus, it is unlikely that there is an alternative diagnosis, such as metastasis or myeloma, if the histologic result is osteomyelitis. Our study focuses on these positive histology cases; thus, we believe using positive histology as the diagnostic standard is reasonable.
In conclusion, the rate of positive culture of osteomyelitis obtained from
imaging-guided core biopsy is low. We found that aspiration of 2 mL of
purulent fluid at biopsy is associated with a higher culture positivity rate.
Clinicians and radiologists should be aware that the likelihood of isolating
an organism with imaging-guided biopsies is low, but it is significantly
higher in cases of intraosseous abscesses.
Acknowledgments
We thank A. C. Wu for statistical support and manuscript review.
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