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1
Department of Diagnostic Radiology, Kingston General Hospital, Hotel Dieu
Hospital, Queen's University, 76 Stuart St., Kingston, Ontario, K7L 2V7
Canada.
2
Department of Diagnostic Imaging, The Hospital for Sick Children, University
of Toronto, 555 University Ave., Toronto, Ontario, M5G 1X8 Canada.
3
Department of Surgery, Division of Orthopedics, Kingston General Hospital,
Hotel Dieu Hospital, Queen's University, Kingston, Ontario, K7L 2V7
Canada.
Received October 25, 1999;
accepted after revision December 10, 1999.
Presented at the annual meeting of the American Roentgen Ray Society, New
Orleans, May 1999.
Abstract
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MATERIALS AND METHODS. We examined 707 radiographs of fractured forearms in 141 patients. Each fracture was assessed by a pediatric radiologist who was unaware of the timing of the initial injury. Assessment included the following features: fracture margins, fracture gap, periosteal reaction, callus, bridging, and remodeling. The time interval between injury and the appearance of the radiographic features and the duration of radiographic signs were determined and correlated with age, sex, angulation, displacement, and location.
RESULTS. Sclerosis at the fracture margins was evident in 85% of fractures 5 weeks after injury. Widening of the fracture gap was observed in 62% of fractures at 6 weeks. Periosteal reaction was evident on all images by 4 weeks, and after 7 weeks, periosteal reaction was separable from cortex in only 10% of fractures. Fracture callus had a density equal to or greater than that of adjacent cortex 10 weeks after injury in 90% of fractures.
CONCLUSION. A wide variation exists in the appearance and duration of the radiographic signs of bone healing. Marginal sclerosis should be an expected radiographic sign of normal bone healing. Applying maximum and minimum time spans to objective radiographic signs may aid in fracture dating.
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The mean number of radiographs per fracture was 3.7 (range, 2-8). In 205 initial fracture radiographs, 26% of patients had casts. On 1-week follow-up radiographs, 97% of patients had casts. On 4- and 5-week follow-up radiographs, 59% and 20% of patients had casts, respectively. The time interval between injury and the appearance of radiographic features and the duration of these features were determined and correlated with gender, age, displacement, and location (metaphysis, metadiaphysis, or diaphysis). The age distribution of our patients included 18% between 0 and 4 years, 21% between 5 and 7 years, 36% between 8 and 10 years, and 25% between 11 and 17 years. All radiographs were assessed by a pediatric radiologist unaware of the time interval after trauma. The radiographic features were chosen because of their common use in the radiography and histology literature [1,2,3,4].
Fractures were assessed for the presence of sharp or blunted fracture margins; a gap between fracture fragments (measured in millimeters), which was compared with earlier radiographs to determine changes in spacing; bone density (sclerosis) at the fracture margins (Fig. 1A,1B); periosteal reaction and its subsequent incorporation into the cortex (Fig. 2A,2B); callus density (compared with that of adjacent cortex) (Fig. 2A,2B); bridging (partial or whole) at the fracture site, defined as a loss of fracture margins (Fig. 2A,2B); and remodeling, determined by a loss of a focal cortical bump or an increase in the obtuse angle of new bone with cortex (Fig. 3A,3B).
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Periosteal reaction was not observed on any radiograph obtained before 2 weeks; however, only 22 patients underwent radiography between 7 and 14 days after injury, and most of these patients had a cast that limited visibility. Periosteal reaction was evident in all patients (33/33) 4 weeks after injury. After 7 weeks, periosteal new bone was separable from cortex on only 10% (14/147) of radiographs. However, it was still separable in one of nine patients who underwent imaging 13 weeks after injury. Periosteal incorporation in cortex increased from 0% (0/66) after 3 weeks to 58% (31/53) after 10 weeks (Fig. 4).
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Fracture gap widening between radiographic examinations was first noted at 2 weeks after injury on 9% (11/177) of radiographs. Between 4 and 6 weeks, the fracture gap widened in 56% of patients (84/150). Seven weeks after injury, further fracture gap widening was noted on only 1 radiograph (1/96). After 8 weeks or more after injury, 91% of fractures (86/95) imaged displayed a decrease in fracture gap.
Two weeks after injury, 6% of fractures (7/117) showed increased density (sclerosis) at the fracture margins. This density peaked from 4 to 6 weeks at 85% (128/150) of fractures. After 11 weeks, no fracture showed an increase in bone density at the fracture margin (0/18) compared with that of adjacent bone (Fig. 5).
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Calcific callus was identified at all fracture sites imaged at 4 weeks with the earliest visualization at 2 weeks after injury in 15% (18/117) of fractures. Between 8 and 10 weeks after injury, 50% (30/61) of fractures had a callus density less than that of adjacent cortex. Additionally, we noted a steady rise in density, and after 10 weeks, 90% (26/29) of calluses had a density equal to or greater than that of cortex.
A partial bridge was noted as early as 3 weeks after injury with 50% of fractures having evidence of bridging at 8 weeks. The fracture line was not visible (full bridge) on 40% (12/30) of radiographs obtained after 10 weeks.
Remodeling was noted as early as 4 weeks in one patient. At 8 weeks after injury and beyond, 95% (91/96) of fractures continued to show evidence of remodeling.
Using the chi-square test, we found no statistically significant difference in the development or duration of radiographic changes based on sex, age, fracture displacement, or fracture site (metaphysis versus diaphysis) in injuries of the radius or ulna.
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Bone healing represents a continuum, often divided into five overlapping histologic stages [1, 2]. The induction stage lasts for 3 weeks from the time of injury. Osteoblastic activity is stimulated at the area of blood flow disruption [5]. Radiographically, soft-tissue edema and hematoma characterize this stage. These features were not observed in our study. In the review by O'Connor and Cohen [1], resolution of these changes was noted as early as 2-5 days.
The inflammatory phase is characterized by inflammatory exudate and follows local necrosis and cellular proliferation. Osteoblasts become active 7 days after injury with bone resorption occurring at areas of necrosis. According to some reports [1, 2], this stage peaks at 2-3 weeks after injury and is defined by a loss of fracture line definition. Bone resorption at this time would result in a widened fracture gap, which in our study plateaued at 4 and 6 weeks. Widening of the fracture gap was seen in more than 60% of patients and was unrelated to either inadequate immobilization or repetitive trauma.
The third stage, the reparative stage, is characterized by periosteal and endosteal calcium deposition and the growth of new osteoid tissue. Calcium deposition begins within a few days of fracture and reaches a peak at several weeks [6]. According to some reports, this stage is called the soft-callus stage and lasts 2-6 weeks [1, 2]. During this stage, we observed increased density at the fracture margins, which was seen in nearly 90% of fractures at 6 weeks. An increase in density at fracture margins was not seen after 11 weeks, which may be an important feature in fracture dating. This histologic stage would also encompass our radiographic visualization of periosteal reaction and callus, first observed at 2 weeks after injury [1, 2].
The fourth histologic stage, called the hardcallus stage, is characterized by the conversion of periosteal and endosteal new bone to lamellar bone with bridging of the fracture line. Radiographically, this stage corresponds to periosteal new bone becoming inseparable from the adjacent cortex and callus density becoming equal to that of adjacent bone. Previous reports stated that the periosteal new bone is incorporated and inseparable from the cortex by 1-3 months [2, 7]. In our study, no periosteal new bone became incorporated before 6 weeks after injury. This may be another important feature in fracture dating. Likewise, periosteal new bone was separable from cortex in 10% of fractures after 7 weeks. Another feature that may be useful in dating is fracture callus density. In our study, fracture callous density was equal to or greater than that of cortex after 10 weeks (90% of fractures). The presence of a partial or whole bridge in 75% of fractures imaged at 10 weeks or more after injury is similar to data published in the literature [1].
The fifth histologic stage is called the remodeling stage. Radiographically, this stage is characterized by slow changes in callus and bone shape. According to one study [3], this stage lasts from 3 months to 2 years after injury. Our study showed remodeling beginning as early as 4 weeks with 95% of fractures continuing to show remodeling after 8 weeks.
Figure 6 summarizes and correlates our study data with histologic changes [1]. Emphasis has been placed on healing characteristics that may be useful in fracture dating.
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Using a constellation or absence of radiologic signs is important when dating fractures. An injury less than 5-7 days old would not show any of the radiographic features described. An injury more than 14 days old, but less than 3 weeks old, would probably show periosteal reaction (separable from cortex) without sclerosis at the fracture margins. A fracture with periosteal reaction separable from cortex and marginal sclerosis is probably between 3 and 11 weeks old. An injury that shows periosteal new bone that is incorporated in underlying cortex is usually older than 6 weeks.
Important limitations of our study include the differences in radiography time intervals. The number of patients or radiographs available has been noted whenever a percentage has been expressed. The presence of a cast for immobilization often limits bone detail and the value of distinct versus indistinct (blunted) fracture margins on radiographs. We focused on a specific location, and bone healing may vary in other skeletal sites [8].
A major limitation of our study was the low number of patients 4 years old or younger (23 patients). Typically, one third of all abuse cases occur in children who are younger than 1 year old, with approximately half of abused children less than 2 years old [4]. Fewer than 10% of abused children are older than 5 years [9]. In children younger than 4 years old, the repair process may proceed more rapidly than in older children [1].
The abused child may be subject to repetitive injury and may not have adequate immobilization, which will alter healing patterns. Additionally, systemic factors such as malnutrition, especially vitamin D or calcium deficiency, and other comorbid illnesses that may affect the bone healing process may be present in an abused child.
In conclusion, the appearance and duration of radiographic signs of bone healing vary. Applying maximum and minimum time limits to objective radiographic signs of healing may aid in dating. Using a constellation or radiographic signs, or the absence thereof, is important when dating fractures.
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