Abstract
Purpose
Ultrasonography has been used increasingly in orthopaedic practice credited to its low cost, easy accessibility, non-invasiveness, reproducibility, and safety from radiation. The purpose of this study was to test the validity and efficacy of ultrasonography as an adjunct in the assessment of fracture healing in long bones treated with intramedullary interlocking devices and its predictive value in determining the need for a secondary surgical procedure.
Methods
This was a descriptive longitudinal study of 40 skeletally mature patients from November 2016 to February 2019, who sustained long bone fractures of the tibia or femur treated using intramedullary interlocking nails. Patients with comminuted and segmental fracture patterns were excluded from the study. Each patient was evaluated at 6- and 12-week post-surgery using standard orthogonal radiographs and ultrasonography to assess fracture healing. Patients were then followed up until fracture union. Quantitative data was analyzed using frequency statistics and descriptive data with inferential statistics.
Results
Ultrasonography predicted 87.5% union and 12.5% delayed or non-union as early as 6 weeks after surgery, while radiographs predicted 22.5% union as late as 3 months of follow-up. The sensitivity and specificity of ultrasonography in assessing fracture healing were 100% and 97.2%, respectively, with a positive predictive value of 80.0%. Vascular resistance index was less than 0.5 in all patients who developed delayed or non-union.
Conclusion
Ultrasonography is able to predict fracture outcomes much earlier than standardized radiographs with comparable sensitivity and specificity. Vascular resistance index is an objective parameter in assessing callus quality and predicting fracture outcomes.
Keywords: Ultrasound, Ultrasonography, Fracture, Non-union, Doppler
1. Introduction
Over the past few decades, ultrasonography has been used increasingly in orthopaedic diseases from diagnosing soft tissue disorders and intra-articular pathologies to therapeutic implementation in musculoskeletal medicine. The trend towards the increased use of ultrasonography can be attributed to its low cost, easy accessibility, non-invasiveness, reproducibility, and safety from radiation. Despite its advantages, routine implementation of ultrasonography in fracture management has not gained momentum in clinical practice. Radiographs remain the primary method of diagnosis and follow-up of fractures and their union. Although radiographs are the cheaper alternative, the increased exposure to radiation, the latency in diagnosis of delayed union and non-union go against its favor. Furthermore, the predictive value of ultrasonography in determining the prognosis of fractures (union vs. non-union) has been seldom explored. The purpose of this study was to test the validity and efficacy of ultrasonography as an adjunct in the assessment of fracture healing in long bones treated with intramedullary interlocking devices and its predictive value in determining the need for a secondary surgical procedure. We also aimed to determine whether any correlation exists between vascular resistance index and quality of callus among these patients.
2. Methods
This was a descriptive longitudinal study conducted from November 2016 to February 2019 at a tertiary hospital in south India. Institutional ethical clearance was obtained, and a convenience method of sampling was adopted. All participants were enrolled in the study after obtaining their written informed consent. Skeletally mature patients having sustained a long bone fracture treated with intramedullary interlocking nails were included and those with comminuted and segmental fracture patterns were excluded from the study. Patients were followed up at 6- and 12-week post-surgery and evaluated using ultrasonography and radiographs.
Ultrasonography was conducted by an experienced radiologist using 3 MHz–12MHz (Samsung HS70) and 18 MHz (Affiniti 70G) linear transducer at the fracture site in anterior, anteromedial, and anterolateral projections after locating the fracture site on the postoperative radiograph. Callus was assessed based on the degree to which it obscured the visibility of the underlying intramedullary device in all 3 projections. The echogenicity of callus was referenced against that of the surrounding muscle, and described as isoechoic (equal to), hypoechoic (less than), or hyperechoic (greater than) (Fig. 1). If hyperechoic callus was visualized in all 3 projections, a trend towards union would be anticipated (Fig. 2). Conversely, isoechoic callus, hypoechoic callus, or the absence of callus in any projection was taken to be suggestive of delayed (Fig. 3) or non-union (Fig. 4). Vascular resistance index was determined using doppler ultrasonography at a single point within the callus having the greatest density of vessels. The neovascular channels in the callus were visualized and referenced against periosteal vessels away from the fracture site.
Fig. 1.
Ultrasonographic findings of hypoechoic: (A) isoechoic, (B) hypoechoic, and (C) callus denoted by yellow arrows.
Fig. 2.
Tibia fracture that progressed to union (A & B), hyperechoic callus (yellow arrow) formation in anteromedial (C), anterolateral (D), and posterior (E) ultrasonographic projections. (F) Doppler shows good flow with resistance index of 0.56.
Fig. 3.
Tibia fracture with radiographic evidence of delayed union (A & B), hypoechoic callus (yellow arrow) noted in anteromedial (C), anterolateral (D), and posterior (E) ultrasonographic projections. (F) Doppler shows resistance index of 0.47 with poor vascularity in the region of the fracture site.
Fig. 4.
Tibia fracture with radiographic evidence of nonunion (A & B), absent callus (yellow arrow) noted in anteromedial (C), anterolateral (D), and posterior (E) ultrasonographic projections. (F) Doppler shows resistance index of 0.39 with poor vascularity in the region of the fracture site.
Radiographs of the operated bone were taken in standard antero-posterior and lateral projections and fracture healing was defined by the presence of bridging callus and disappearance of the fracture line, similar to the radiographic union scale in tibial (RUST) criteria. Patients were followed up till fracture union, and the results of ultrasonography and radiography findings were compared. Quantitative data was analyzed using frequency statistics and descriptive data with inferential statistics.
3. Results
A total of 40 patients with long bone fractures were included in the study. Thirty (75.0%) patients had tibial fractures and the rest (25.0%) had femur fractures. Compound fractures accounted for around 15.0% of patients. The majority sustained a simple transverse fracture constituting 52.5% of the study population followed by oblique (32.5%) and spiral (15.0%) fracture configurations (Table 1).
Table 1.
Frequency distribution of patient characteristics, fracture characteristics, findings, outcomes, and secondary procedures implemented (n = 40).
| Variables | n (%) |
|---|---|
| Age (year) | |
| < 20 | 2 (5.0) |
| 21-30 | 14 (35.0) |
| 31-40 | 14 (35.0) |
| 41-50 | 5 (12.5) |
| > 50 | 5 (12.5) |
| Sex | |
| Female | 6 (15.0) |
| Male | 34 (85.0) |
| Bone | |
| Femur | 10 (25.0) |
| Tibia | 30 (75.0) |
| Fracture type | |
| Closed fracture | 34 (85.0) |
| Open fracture | 6 (15.0) |
| Fracture pattern | |
| Oblique | 13 (32.5) |
| Spiral | 6 (15.0) |
| Transverse | 21 (52.5) |
| Ultrasound interpretation at 6 weeks | |
| Callus | 35 (87.5) |
| Delayed union | 4 (10.0) |
| Non-union | 1 (2.5) |
| Ultrasound interpretation at 12 weeks | |
| Callus | 35 (87.5) |
| Delayed union | 4 (10.0) |
| Non-union | 1 (2.5) |
| Radiological interpretation at 6 weeks | |
| No callus | 1 (2.5) |
| Uniting fracture | 39 (97.5) |
| Radiological interpretation at 12 weeks | |
| No callus | 1 (2.5) |
| United fracture | 7 (17.5) |
| Uniting fracture | 32 (80.0) |
| Expected results | |
| Delayed union | 4 (10.0) |
| Union | 35 (87.5) |
| Non-union | 1 (2.5) |
| Actual results | |
| Delayed union | 3 (7.5) |
| Union | 36 (90.0) |
| Non-union | 1 (2.5) |
| Agreement | |
| Concordant | 39 (97.5) |
| Discordant | 1 (2.5) |
| Actual results | |
| Union | 36 (90.0) |
| Delayed/Non-union | 4 (10.0) |
| Secondary procedure | |
| Bone grafting | 1 (2.5) |
| Bone marrow injection | 1 (2.5) |
| Dynamization followed by exchange nailing and bone grafting | 1 (2.5) |
| Dynamization with bone marrow injection | 1 (2.5) |
| Nil | 36 (90.0) |
At 6- and 12-week post-surgery, ultrasonography was able to detect the presence of callus with sensitivity and specificity of 89.7% and 100%, respectively, when compared to radiographs as a gold standard. Ultrasonography demonstrated a positive predictive value of 100%, negative predictive value of 20.0% and diagnostic accuracy of 90.0% for anticipating fracture union (Table 2).
Table 2.
Diagnostic accuracy and clinical agreement of postoperative ultrasonography at 6- and 12-week follow-up.
| Parameter | True negative (no callus on radiograph) | True positive (callus on radiograph) | False negative (union) | False positive (delayed/non-union) | Sensitivity (%) | Specificity (%) | Positive predictive value (%) | Negative predictive value (%) | Diagnostic accuracy (%) | Gold standard | Kappa statistics | p value |
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| USG at 6 weeks | 1 | 35 | 4 | 0 | 89.7 | 100.0 | 100.0 | 20.0 | 90.0 | 6-week radiograph | 0.304 | 0.125 |
| USG at 12 weeks | 1 | 35 | 4 | 0 | 89.7 | 100.0 | 100.0 | 20.0 | 90.0 | 12-week radiograph | 0.304 | 0.125 |
USG: ultrasonography.
Ultrasonography predicted union (87.5%) and delayed or non-union (12.5%) as early as 6 weeks after surgery, while radiography was able to detect a meagre 22.5% union at 3 months of follow-up. Eventually, 36 patients (90.0%) attained union, and 4 (10.0%) had delayed or non-union. One patient who was anticipated to have delayed or non-union on ultrasonography at 6 weeks progressed to uneventful fracture union. Of the 4 patients who showed evidence of delayed or non-union, 1 underwent bone grafting, 1 underwent bone marrow injection, 1 underwent dynamization with bone marrow injection and 1 underwent dynamization with exchange nailing and bone grafting.
Vascular resistance index was found to be less than 0.5 in all patients who developed delayed/non-union and was equal to or greater than 0.5 in those who progressed to fracture union. At a cut-off of 4.9, vascular resistance index was found to be 100% sensitive and specific for predicting union as justified by the receiver operating characteristic curve (Fig. 5, Table 3) that demonstrated a linear configuration with absolute agreement. One patient who was suspected to progress to delayed or non-union based on the appearance of callus was found to have vascular resistance index of 0.5 and eventually progressed to union. At a cut-off of 0.56, vascular resistance index demonstrated 97.2% sensitivity and 100% specificity (Table 4).
Fig. 5.
The receiver operating characteristic curve analysis was carried out for the vascular resistance index. We do not see any curve because the cut-off of 0.49 gives absolute agreement for prediction of the vascular resistance index. The area of 1.000 indicates absolute agreement and 100% prediction.
ROC: receiver operating characteristic.
Table 3.
Coordinates of the receiver operating characteristic curve determined using vascular resistance index as test result variable.
| Positive if greater than or equal toa | Sensitivity | 1 - Specificity |
|---|---|---|
| 0.0000 | 1.000 | 1.000 |
| 0.4050 | 1.000 | 0.750 |
| 0.4450 | 1.000 | 0.500 |
| 0.4700 | 1.000 | 0.250 |
| 0.4900 | 1.000 | 0.000 |
| 0.5600 | 0.972 | 0.000 |
| 0.6250 | 0.944 | 0.000 |
| 0.6350 | 0.833 | 0.000 |
| 0.6450 | 0.806 | 0.000 |
| 0.6550 | 0.750 | 0.000 |
| 0.6650 | 0.667 | 0.000 |
| 0.6750 | 0.583 | 0.000 |
| 0.6850 | 0.500 | 0.000 |
| 0.6950 | 0.444 | 0.000 |
| 0.7050 | 0.417 | 0.000 |
| 0.7150 | 0.333 | 0.000 |
| 0.7250 | 0.278 | 0.000 |
| 0.7350 | 0.194 | 0.000 |
| 0.7450 | 0.139 | 0.000 |
| 0.7550 | 0.111 | 0.000 |
| 0.7800 | 0.056 | 0.000 |
| 1.0000 | 0.000 | 0.000 |
The smallest cutoff value is the minimum observed test value minus 1, and the largest cutoff value is the maximum observed test value plus 1. All the other cut-off values are the averages of 2 consecutive ordered observed test values.
Table 4.
Diagnostic accuracy and clinical agreement of vascular resistance index with a 0.5 cut off.
| Parameter | True negative (VRI > 0.5, union) | True positive (VRI ≤ 0.5, delayed/non-union) | False negative (VRI > 0.5, delayed/non-union) | False positive (VRI ≤ 0.5, no union) | Sensitivity (%) | Specificity (%) | Positive predictive value (%) | Negative predictive value (%) | Diagnostic accuracy (%) | Gold standard | Kappa statistics | p value |
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| VRI (cut off 0.5) | 35 | 4 | 0 | 1 | 100.0 | 97.2 | 80.0 | 100.0 | 97.5 | Actual results (union) | 0.875 | < 0.001 |
VRI: vascular resistance index.
4. Discussion
The first published research of ultrasonography in fracture diagnosis was in 1988 when Katz et al.1 studied 41 newborns with clavicle fractures following delivery. All newborns were subjected to ultrasonography and radiographs for evaluation and no significant difference was found between the 2 modalities.1 A similar study by Blab et al.2 of 49 newborns not only concluded that ultrasonography and radiographs were comparable in diagnostic accuracy, but also found that ultrasonography was better at assessing fracture healing. Several subsequent studies have applied the same technique to diaphyseal fractures, foot and ankle fractures, and sternal and rib fractures with good diagnostic accuracy.3, 4, 5, 6, 7, 8, 9
Ricciardi et al.10 was the first to describe the sonographic appearance of callus at various stages of fracture healing in 239 patients. This study, however, was considered to be limited in its clinical application due to the lack of individual patient data and no reporting of delayed union or non-union.10 Maffulli and Thornton11 not only found that ultrasonography was more sensitive in identifying early callus and its progression to bridging callus, but were also able to comment on the appearance of an established non-union by the absence of a bony bridge within maturing soft callus.
Based on the different densities, ultrasonography relies on capturing reflected high-frequency sound waves to delineate structures. When ultrasonography is applied to bone, intact cortical bone appears as a dense continuous white line due to the complete reflection of ultrasound waves from the surface of the bone. In the case of fractures, a break is visible on this white line and the ultrasound waves are reflected by the far cortex. When fractures are treated using an intramedullary nail, there are 2 distinct lines on the white line, of which the first one is the break in the continuity denoting the cortex and the second one is thin and distant due to the waves reflected by the implant. Superficial bones like the tibia are better studied using a high-frequency transducer that provides high-resolution imaging with limited depth penetration. Conversely, bones with extensive soft tissue cover like the femur require a low-frequency transducer that permits greater depth of penetration at the expense of image resolution.12
During fracture healing, the periosteal soft callus grows in size and density ultimately bridging the fracture gap. This callus appears in various shades of grey depending on its density and can be easily delineated from surrounding soft tissue. Ultrasound waves were progressively obscured as callus bridged the fracture gap, which decreased the visibility of the intramedullary implant until it was completely covered.13
Although ultrasonography has the advantages of safety, non-invasiveness, affordability, and real-time delivery of results, it has not been widely used in the assessment of fracture healing. The most commonly employed method of assessing the progression of fracture healing persists to be standard orthogonal radiographs. While standardized scoring systems such as the RUST criteria are helpful in objectively assessing fracture healing, callus takes at least 6 – 8 weeks to be visible on radiographs and more than 10 weeks to be seen bridging the fracture gap.14,15
Moed et al.16 found that bridging callus was detected at a mean of 38 days on ultrasonography as opposed to 127 days by plain orthogonal radiographs in their pilot study of 14 tibia diaphyseal fractures managed with unreamed and statically locked intramedullary nails. In their subsequent study of 47 patients, each subject underwent ultrasonographic examination at 6 weeks post-surgery. If there were no features of fracture healing, a subsequent scan would be done at 9 weeks to determine whether dynamization or bone grafting is needed. According to their studies, fracture healing could be seen in the 6- or 9-week scans and positive predictive values achieved 97% and 100% sensitivity for fracture union respectively, which were similar to the results in our study. Evidence of fracture healing was seen on ultrasonography at a mean of 6.5 weeks as opposed to 19 weeks using radiographs, thereby justifying the use of ultrasonography in predicting delayed union. A single falsely reported scan at 6 weeks resulted in the false positive finding and the patient developed symptomatic non-union that required intervention. Thus, they concluded that ultrasonography predicted early callus formation and reliably predicted fracture union before being radiographically apparent.
In this study, 87.5% of union and 12.5% of delayed or non-union were predicted by ultrasonography as early as 6 weeks postoperatively, while 22.5% of radiographs were able to detect union at 3 months of follow-up. Eventually, 90.0% of patients attained fracture union with 10.0% having delayed union. Moreover, we were able to establish the need for a secondary procedure with an 80.0% positive predictive value. One patient in our study had delayed or non-union on ultrasonography at 6 weeks progressed to fracture union.
Vascular resistance index determines the quality of callus by referencing the neovascular channels in the callus against the periosteal vessels at a location away from the fracture site.17,18 In the immediate postoperative period, the fracture hematoma lacks vascularity. As the callus develops, new blood vessels arise, and the vessels become increasingly dense. These immature vessels with gaps in the endothelium cause a leak, resulting in low vascular resistance and increased blood supply to the fracture site. Low resistive index implies continuous flow in the cardiac cycle with no diastolic reversal or absence. While it is calculated automatically during ultrasonographic examination, it can be calculated manually using the formula:
| Resistive index = (peak systolic velocity – end-diastolic velocity)/peak systolic velocity. |
Vessels like the internal carotid artery that supply blood to vital organs require low resistive indices (0.55 – 0.7) to ensure continuous flow. Vessels that supply the extremities, however, have high vascular resistive indices (> 0.7) due to relatively low flow during the diastolic phase of the cardiac cycle which is compensated by high peak systolic velocity. As the callus matures, ossification occurs, and the vessel density gradually decreases, which results in gradual increase in vascular resistance index that can be seen in the second ultrasonography examination at 12-week. Therefore, persistence of low resistance vessels in the fracture is taken as an indicator that the callus is not maturing and eventually results in delayed union or non-union.18, 19, 20, 21
Bottinelli et al.19 found that patients with positive fracture evolution demonstrated an increase in the caliber of afferent vessels, a decrease in their total number, and the appearance of branches. The vascular resistance index of these vessels progressively increased to values comparable to the nutrient vessels and by the second month of fracture healing, a telesystolic notch could be seen which was credited to the development of a muscular tunic in a finally mature vessel. Caruso et al.18 demonstrated that new vessel formation decreased after approximately 100 days in those patients who progressed to fracture union. Conversely, high vascularity persisting beyond 3 months with an absence of bridging callus was observed in patients with delayed union. Compared to other studies, vascular resistance index in our study was less than 0.5 in all cases of delayed union and non-union and more than 0.5 in cases that progressed to union.11,19
With the development of ultrasonography techniques and increasing expertise of radiologists, the potential of the imaging modality continues to grow. Being comparable to ex-vivo microangiography computed tomography, the results of 3-dimensional high-frequency power doppler eliminated the variability and artifacts of multiple 2-dimensional slices that often lead to erroneous reporting.22 Although a pilot study using 3-dimensional ultrasonography in the assessment of fracture healing showed good promise, further research is needed with a larger cohort.23 While contrast-enhanced ultrasonography using microbubble agents has improved accuracy in assessing vascularity in Achilles tendinopathy and rotator cuff injuries, its application in fracture healing has not been explored.24, 25, 26
The limitation of this study is that we did not expand the scope of our research to more complex fracture patterns thereby limiting the use of this technique and the cut-offs to simple fracture types. We believe that further research considering complex fractures will help establish whether these cut-offs are applicable in those clinical scenarios to establish reliable guidelines for assessment.
Non-union is a significant contributor to disability and morbidity among patients with fractures. The delay in diagnosis of this condition on radiographs results in prolonging the anguish endured by the individual and further delaying the institution of necessary treatment. Vascular resistance index was proved to be a useful and objective parameter in assessing callus quality and predicting fracture outcomes. Ultrasonography is as sensitive and specific as standard radiographs in detecting callus and predicting fracture union in the fracture healing process. Despite its advantages, ultrasonography is not widely implemented in routine fracture diagnosis and follow-up, which could be attributed to the learning curve and expertise required in accurate musculoskeletal ultrasonography. Moreover, the literature review failed to uncover an objective standardized scoring system for assessing callus during ultrasonography being similar to the RUST criteria used in radiographs. The development of a suitable scoring system will improve the prognostic and predictive value of ultrasound in fracture healing and reduce inter-observer variability during follow-up thereby ensuring early diagnosis and prompt intervention.
CRediT authorship contribution statement
Tilak Rommel Pinto: Conceptualization, Writing – Original Draft, Writing – Review & Editing. Kiyana Mirza: Writing - Original Draft, Writing – Review & Editing. Anston Vernon Braggs: Visualization. Aravinda Hegde K: Conceptualization, Writing – Original Draft. Chiranjeevi Srinivasa Gowda: Writing – Original Draft, Writing – Review & Editing.
Ethical statement
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional ethical committee.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.
Declaration of competing interest
The authors have no relevant financial or non-financial interests to disclose.
Footnotes
Peer review under responsibility of Chinese Medical Association.
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