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. 2016 Jan 12;89(1058):20150384. doi: 10.1259/bjr.20150384

Standard-b-value vs low-b-value DWI for differentiation of benign and malignant vertebral fractures: a meta-analysis

Zhanpeng Luo 1,2, Li Litao 2, Suxi Gu 2, Xiaobo Luo 2, Dawei Li 2, Long Yu 2, Yuanzheng Ma 1,2,✉
PMCID: PMC4985191  PMID: 26612466

Abstract

Objective:

To determine the comparative diagnostic performance of standard-b-value (≥500 mm2) vs low-b-value (<500s mm−2) diffusion-weighted imaging (DWI) for discriminating malignant from benign vertebral compression fractures.

Methods:

12 studies with a total of 350 malignant and 312 benign vertebral fractures were included.

Results:

The apparent diffusion coefficient (ADC) value of benign vertebral compression fractures was lower than that of malignant vertebral compression fractures (SMD = 1.81, 95% CI 0.98 to 2.64 Z = 4.27, p < 0.05). ADC value difference was more pronounced in the group of low-b-value DWI (SMD = 2.31, 95% CI 1.02 to 3.60 Z = 3.51, p < 0.05) than in the group of standard-b-value DWI (SMD = 1.38, 95% CI 0.18 to 2.59 Z = 2.25, p < 0.05). Ethnicity stratified analysis demonstrated higher ADC values in benign vertebral compression fractures in comparison to malignant tissues in both the Asian and Caucasian subgroups (Asians: SMD = 2.400, 95%CI 1.45 to approximately 3.35, p<0.05; Caucasians: SMD = 0.592, 95 % CI −0.848 to approximately 2.032, p < 0.05). And the ADC value difference was more pronounced in the Asian subgroup.

Conclusion:

ADC value appears to be a reliable method to differentiate benign from malignant fractures. Low-b-value DWI was more a valuable parameter than standard-b-value DWI for discriminating malignant from benign vertebral compression fractures. And the diffusion characteristics of the benign vertebral fractures such as osteoporosis, trauma and infection have rarely been investigated separately.

Advances in knowledge:

The use of low-b-value DWI for differentiation of benign and malignant vertebral fractures is recommended.

Metastases to the spine occur in up to 10% of patients with primary neoplasms. However, it has been estimated that up to one-third of vertebral compression fractures in patients with known malignancies are benign.1–5 Although diagnostic imaging has made remarkable progress in recent years, it remains difficult to differentiate benign and malignant vertebral fractures. Appropriate treatment of vertebral fractures requires knowledge of the cause of the fracture.6,7

Diffusion-weighted imaging is a sensitive technique that allows for noninvasive characterization of biological tissues on the basis of the diffusion of water molecules.8 Diffusion-weighted imaging (DWI) and apparent diffusion coefficients (ADCs) have been studied in variable clinical situations, including grading of tumours and assessment of tumour response.9 Theoretically, DW imaging with a higher b-value yields better contrast with its reflection of more tissue diffusivity and less T2 shine-through effect.9 Perfusion effects which occur at low b values, so a technique which focuses more on low b value information will have correspondingly more perfusion information.10

DWI has proven to be a useful method in the differential diagnosis of benign and malignant vertebral compression fractures.11–15 However, the results varies across studies. The present systematic review and meta-analysis aim to summarise and combine the published data on diffusion-weighted imaging for discriminating malignant from benign vertebral compression fractures. We conducted a subgroup meta-analysis of b-value ≥500 and b-value < 500 used for ADC calculation. Ethnicity stratified analysis was also performed.

METHODS AND MATERIALS

Search strategy

The initial database (the Chinese Biological Medicine, Pubmed, MEDLINE and EMBASE databases) search identified 1518 relevant articles that were published including till Jan 2015. The literature search was performed with the following terms: vertebral compression fractures and diffusion-weighted imaging, vertebral compression fractures and DWI, fractures and diffusion-weighted imaging, fracture and diffusion-weighted imaging, fractures and DWI, fracture and DWI. The research was limited to articles concerning humans with an abstract in English and Chinese.

Study inclusion criteria

Two independent reviewers reviewed the abstracts from all the citations. Inclusion criteria were applied to the retrieved articles independently by the reviews. Studies were included in this analysis (1) if the diagnostic criteria of the malignant or benign vertebral compression fractures were clearly reported; (2) if DWI imaging was obtained to evaluate malignant or benign vertebral compression fractures; (3) if DWI acquisition procedures were clearly stated; (4) by the presence of ADC value [mean ± standard deviation (SD)], which could be extracted from the original study.

Data collection

The following data were extracted from all the studies that met the inclusion criteria: the study name, published year, MR modalities used (GE, Siemens and Philips), pulse, repetition time (TR, ms), echo time (TE, ms), the number of b factors, b-value (min) and b-value (max) (s mm−2), number of malignant and benign vertebral compression fractures, ADC value of malignant and benign vertebral compression fractures, ADC SD of malignant and benign vertebral compression fractures (Tables 1 and 2).

Table 1.

Main characteristics of the studies evaluating the performance of diffusion-weighted imaging for the differentiation of vertebral compression fractures

Number Study name Patient population Published year MRI unit Field (T) Pulse TR TE b factors, No b factor (Max) b factor (Min) FS b factor (Max) b value used for ADC calculation
1 Chan et al14 Asians 2002 GE 1.5 SS-SE-EPI 8000 92 4 1000 200 yes 1000 1000
2 Zhou et al11 Caucasians 2002 Philips 1.5 SS-SE-EPI 1648 63 3 250 150 NA 250 <250
3 Maedaet al13 Asians 2003 GE 1.5 LS-EPI 2093–3498 70.5 2 1000 5 NA 1000 1000
4 Tang et al12 Asians 2007 Philips 1.5 SS-SE-EPI 1400 100 8 800 100 yes 800 300
5 Balliu et al15 Caucasians 2009 Philips 1.5 multishot SE-EPI 1600 95 2 500 0 yes 500 500
6 Lu lu and Song-bai16 Asians 2013 GE 3.0 SS-SE-EPI 2800 57 6 800 300 NA 800 300
7 Zengxu and Zhou 17 Asians 2012 GE 1.5 SS-EPI 3000–4000 53–80 1 300 300 yes 300 300
8 Chunlong18 Asians 2013 GE 1.5 SE-EPI 11500 88.8 5 1000 200 NA 1000 400
9 Jiu-ming 19 Asians 2013 GE 1.5 SE-EPI 1500 30 1 1000 1000 NA 1000 1000
10 Yan20 Asians 2008 Philips 1.5 SE-EPI 2000 65 1 500 500 NA 500 500
11 Pozzi21 Caucasians 2012 Siemens 1.5 SS-SE-EPI NA NA 1 800 800 NA 800 800
12 Geith et al22 Caucasians 2014 Siemens 1.5 SS-SE-EPI 3000 72 4 600 100 yes 600 100/400
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ADC, apparent diffusion coefficient; EPI, echo planar imaging; FS, fat suppression; NA, not available; SE, single echo; SS, single shot; TE, echo time; TR, repetition time.

Table 2.

Main characteristics of the studies evaluating the performance of diffusion-weighted imaging for the differentiation of vertebral compression fractures

Number N (benign) Osteoporosis Trauma Infection ADC mean (benign) ADC SD (benign) N (malignant) Metastases Multiple myeloma ADC mean (malignant) ADC SD (malignant)
Chan et al14 2002 31 25 0 6 1.94 0.35 18 18 0 0.82 0.2
Zhou et al11 2002 12 NA NA NA 0.32 0.05 15 15 0 0.19 0.03
Maeda et al13 2003 20 NA NA 0 1.21 0.17 16 16 0 0.92 0.2
Tang et al12 2007 18 4 14 0 2.23 0.21 27 27 0 1.04 0.03
Balliu et al15 2009 30 0 16 14 1.46 0.64 15 15 0 0.92 1.3
Lu lu and Song-bai16 2013 23 NA NA 0 1.75 0.41 22 18 4 1.11 0.33
Zengxu and Zhou17 2012 47 NA NA NA 0.7 0.2 100 NA NA 0.45 0.11
Chunlong18 2013 21 0 0 21 1.42 0.58 43 43 0 1.46 0.5
Jiu-ming19 2013 30 NA NA 0 1.8 0.312 20 20 0 1.3 0.241
Yan et al20 2008 44 NA NA 0 1.42 0.26 31 31 0 0.91 0.17
Pozzi21 2012 10 10 0 0 0.646 0.368 23 23 0 1.241 0.4
Geith et al22 2014 26 26 0 0 1.76 1.84 20 20 0 1.31 1.42
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ADC, apparent diffusion coefficient; SD, standard deviation.

Statistical analysis

All meta-analyses were performed using Stata® (v. 12.0; StataCorp, College station, TX). We pooled and statistically compared ADC data from malignant or benign vertebral compression fractures. Meta-analysis of continuous outcomes uses weighted mean difference (SMD). This heterogeneity was assessed by using Cochran Q test and the I-square test. When the Cochran Q test was significant or I-square value was >50%, the heterogeneity exists and random effect model (DerSimonian–Laird method) should be selected instead of fixed effect model (Mantel–Haenszel method) for calculation of pooled data. Forest plots were drawn to show a visual representation of the amount of variation between different groups. Publication bias was assessed. For all tests, p-values <0.05 were regarded as significant.

RESULTS

Study selection and data extraction

The literature search and study selection flow chart is displayed in Figure 1. The initial database search identified relevant articles that were published including till Jan 2015. The literature search from our previous study yielded 1518 articles, of which 112 were reviewed in abstract, and from them 29 were further reviewed in full text. Of these, 12 studies were eligible for inclusion.11–22

Figure 1.

Figure 1.

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Selection process of the articles. Pooled analysis. ADC, apparent diffusion coefficient; SD, standard deviation.

Description of studies

12 studies with a total of 350 malignant vertebral compression fractures and 312 benign vertebral compression fractures were included in this meta-analysis (# 1–12) Figures 2 and 3.

Figure 2.

Figure 2.

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The apparent diffusion coefficient (ADC) value of benign vertebral compression fractures (a) was lower than that of malignant vertebral compression fractures (SMD = 1.81, 95% CI 0.98 to 2.64, p < 0.05). Subgroup meta-analysis of b-value ≥500 (b) and b-value < 500 (c) was used for ADC calculation. ADC value difference was more pronounced in the group of b-value < 500 (SMD = 2.31, 95% CI 1.02 to 3.60 p < 0.05) than in the group of b-value ≥500 (SMD = 1.38, 95% CI 0.18 to 2.59 p < 0.05).

Figure 3.

Figure 3.

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Publication bias was not present (t=1.51, p=0.162).

Eleven studies used 1.5-T field strength (# 1–5, 7–12) while one study used 3.0 T (# 6). The TE of the DWI varied considerably in the studies ranging from 30 (# 9) to 100 (# 4). One study did not provide information on TE (# 11). The TR of the DWI varied considerably in the studies ranging from 1500 (# 9) to 11,500 (# 6). One study did not provide information on TR (# 11). Six studies used SSEPI sequence studies (# 1–2, 4, 6–7, 11–12). Six studies (# 1, 3–6) used a sequence with maximum of b factor in the range of 500–1000 ms. Ten studies (# 1, 3, 4–6, 8–12) used a sequence with maximum of b factor in the range of 500–1000 ms. Nine studies (# 1–8,12) used a sequence with minimum of b factor in the range of 0–500 ms. Six studies (# 2, 4, 6–8, 12) used a sequence with b factor in the range of 0–500 ms for ADC calculation while six studies (# 2, 4, 6–8, 12) used a sequence with b factor in the range of ≥500 for ADC calculation (# 1, 3, 5, 9–11). Seven studies did not provide information on fat-suppressed technique (# 2–3, 5 and 7–10). The results of all analyses are reported in Tables 1 and 2.

Synthesis of general diagnostic parameters

The ADC value of benign vertebral compression fractures was lower than that of malignant vertebral compression fractures (SMD = 1.81, 95% CI 0.98 to 2.64 Z = 4.27, p < 0.05). Significant heterogeneity between studies was noted (all p < 0.05). Publication bias was not present (t = 1.51, p = 0.162).

Subgroup meta-analysis of standard-b-value DWI (b value ≥500) and low-b-value DWI (b value < 500) used for ADC calculation

We conducted a subgroup meta-analysis of b factor ≥500 used for ADC calculation based on 6 studies, including 123 malignant vertebral compression fractures and 165 benign vertebral compression fractures. The ADC value of benign vertebral compression fractures was lower than that of malignant vertebral compression fractures (SMD = 1.38, 95% CI 0.18 to 2.59 Z = 2.25, p < 0.05).

We conducted a subgroup meta-analysis of b factor < 500 used for ADC calculation based on 6 studies, including 227 malignant vertebral compression fractures and 147 benign vertebral compression fractures. The ADC value of benign vertebral compression fractures was lower than that of malignant vertebral compression fractures (SMD = 2.31, 95% CI 1.02 to 3.60 Z = 3.51, p < 0.05).

ADC value difference was more pronounced in the group of low-b-value DWI (SMD = 2.31, 95% CI 1.02 to 3.60 Z = 3.51, p < 0.05) than in the group of standard-b-value DWI (SMD = 1.38, 95% CI 0.18 to 2.59 Z = 2.25, p < 0.05).

Subgroup meta-analysis of patient population (Asians and Caucasians)

Patient population (ethnicity) stratified analysis demonstrated higher ADC values in benign vertebral compression fractures in comparison to malignant tissues in both the Asian and Caucasian subgroups (Asians: SMD = 2.400, 95% CI 1.447–3.354, p < 0.05; Caucasians: SMD = 0.592, 95% CI −0.848–2.032, p < 0.05). ADC value difference was more pronounced in the Asian subgroup.

DISCUSSION

Vertebral compression fractures are common, and it is sometimes difficult to determine whether the cause is benign or malignant.23,24 Accurate diagnosis linked to appropriate treatment is important. Preliminary data using diffusion-weighted imaging of vertebral compression fractures showed a reduced water mobility in pathological fractures. Based on calculations of the relevant data available in the currently published articles, our systematic review and meta-analyses showed that the ADC value of benign vertebral compression fractures was lower than that of malignant vertebral compression fractures. ADC value difference was more pronounced in the group of b-value < 500 than in the group of b-value ≥500. All these demonstrated that DWI and ADC value was useful for differentiation between malignant and benign vertebral compression fractures.

We need to admit that if a meta-analysis can give a best cut-off level, the results might be more informative. The reported mean ADC values of malignant and benign vertebral fractures in our meta-analysis ranged from 0.19 to 1.46 and 0.32 to 2.23 × 10−3 mm2 s−1, respectively. Unfortunately, a threshold level was not proposed by any study using DW imaging in our meta-analysis. Under such circumstance, a best cut-off level could not be identified by meta-analysis. This is an intrinsic deficiency of meta-analysis for diagnostic accuracy test.25 Based on individual raw data in our meta-analysis, a reasonable threshold for malignancy seems to be an ADC value of 1.4 × 10−3 mm2 s−1 or less (OR = 7.13). Further prospective studies need to be completed in larger scales to validate our results.

The high cellularity of malignant vertebral compression fractures increases intracellular volume fraction relative to the interstitial space. Because the water diffusion coefficient is approximately 10 times lower in the intracellular than in the extracellular space, this should lower ADC values of malignant vertebral compression fractures. However, the cellularity of benign fractures can be lower than that of malignant vertebral compression fractures, because of the increased interstitial space associated with oedema in the acute phase. Correspondingly, we found that the ADC value of benign vertebral compression fractures was lower than that of malignant vertebral compression fractures.

According to imaging mechanism, diffusion-weighted images are obtained by acquiring T2W images with the addition of diffusion-weighting gradient known as the “b-value”, which represents diffusion gradient strength, duration of the gradient and interval between diffusion gradients.26 This lowering of ADC in response to a larger maximal b-value is a fundamental property of DWI because of the impact on ADC not just of true molecular diffusion but of any source of incoherent motion. In particular, capillary perfusion is a source of perceived diffusion at lower b-values that artifactually elevates ADC value.27 In our current study, we found ADC value difference of malignant and benign vertebral compression fractures was more pronounced in the group of b-value < 500 than in the group of b-value ≥ 500. Therefore, b-value < 500 was more a valuable parameter than b-value ≥ 500 for discriminating malignant from benign vertebral compression fractures.

Heterogeneity is a potential problem when interpreting the results of all meta-analyses.26 In this meta-analysis, we did find significant heterogeneity between studies. And studies were stratified by patient population to explore potential sources. Ethnicity-stratified analysis demonstrated higher ADC values in benign vertebral compression fractures in comparison to malignant tissues in both the Asian and Caucasian subgroups. ADC value difference was more pronounced in the Asian subgroup. In addition, the benign group consisted of 312 vertebral fractures. The benign vertebral fractures included osteoporosis (n = 65), trauma (n = 30), infection (n = 41), osteoporosis or trauma (n = 117) and osteoporosis or trauma or infection (n=59). The diffusion characteristics of the benign vertebral fractures such as osteoporosis, trauma and infection have rarely been investigated separately. Publication bias was not present in our current study.28,29

Conventional MR techniques are the imaging test of choice in the diagnosis of pathological fractures. However, conventional MR is very sensitive but not always specific.15 Bone single photon emission CT may be comparable with MRI for differentiating malignant from benign vertebral fractures.30 Discrimination based on the signal intensity ratio (SIR) of opposed-phase/in-phase was reported to be useful for differential diagnosis between malignant and benign vertebral compression fracture.31 High cellularity in tumour tissue yields lower ADC values than oedematous marrow in benign fractures.4 However, our study was not designed to explore the accuracy of ADC in the differentiation of benign and malignant vertebral fractures, since our data were not available to fill out cross-tabs in order to assess true positive (TP), true negative (TN), false positive (FP) and false negative (FN) cases.

There were several limitations to our study. Firstly, variable diffusion-weighting techniques were utilized among studies, such as steady-state free precession (which lacks the ability to absolutely quantify diffusion, thus not accounting for T2 shine-through), fast spin echo, line scan and echo planar imaging, as well as inconsistent diffusion pulse length.1,32 Secondly, interestingly, the mean ADC values varied significantly between study groups.1,32 The standardization of the acquisition protocol for diffusion-weighted imaging across the multicentre studies should be performed to further validate our results. Thirdly, our study was not designed to explore the accuracy of the ADC in the differentiation of benign and malignant vertebral fractures. Further studies with a larger sample size to determine the sensitivity, specificity, positive- and negative-predictive values of ADC in this aspect would certainly be useful.4 Fourthly, the diffusion characteristics of the benign vertebral fractures such as osteoporosis, trauma and infection have not been fully investigated separately.

In conclusion, even though the literature has been inconsistent, ADC value appears to be a reliable method to differentiate benign from malignant fractures. Low-b-value DWI was a more valuable parameter than standard-b-value DWI for discriminating malignant from benign vertebral compression fractures. Therefore, the use of low-b-value DWI for differentiation of benign and malignant vertebral fractures is recommended.

Contributor Information

Zhanpeng Luo, Email: luozp2009@126.com.

Li Litao, Email: lltop_1@sina.com.

Suxi Gu, Email: dr.gusuxi@qq.com.

Xiaobo Luo, Email: luoxiaobo_309@163.com.

Dawei Li, Email: ldw301@126.com.

Long Yu, Email: yulong1860@126.com.

Yuanzheng Ma, Email: xl1537323096@sina.com.

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