Segmental Femoral Fracture Malunion: Evidence and Prognostic Analysis of Medical Intervention in the 3rd Century BC

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Segmental Femoral Fracture Malunion: Evidence and Prognostic Analysis of Medical Intervention in the 3rd Century BC

https://doi.org/10.21203/rs.3.rs-3234503/v1

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We examined the remains of an individual who was unearthed from the Tuchengzi site and was believed to be from the Warring States period in China. The remains exhibited segmental femoral fracture. We aimed to deduce the cause of fracture, medical interventions, healing process, and motion behavior after fracture healing using several techniques, including macroscopic observation, computed tomography, and finite element analysis. The findings suggested that the segmental nature of the fracture was likely caused by the same occupational activity. The morphology of the healed fracture indicated that the individual underwent medical intervention. The fracture healing process signified that the lower extremity underwent adequate fixation, while bone callus remodeling suggested the recovery of lower-extremity load-bearing capacity. The finite element analysis demonstrated that the fracture healed to such a degree that it could withstand the load of standing, but not the load of normal walking. We suggest that medical practitioners in the Warring States period possessed a good knowledge of thigh anatomy, enabling them to guide fracture reduction and fixation. Reasonable medical intervention facilitated fracture healing and load recovery. Although the individual was able to stand, walking necessitated compensatory movement or instrumental assistance due to femur deformity resulting from fracture healing.

Fracture

Medical intervention

Femur

Segmental

Finite element analysis

Human remains serve as the most authentic and direct evidence to aid the understanding of ancient human life(Biers, 2023). They provide vital information regarding survival pressures, socioeconomic development, human ailments, and population conflicts(Zhang et al., 2021). Traumatic lesions are commonly identified when examining human skeleton remains(Grauer & Roberts, 1996), especially traumatic lesions of the cranial bones and long bones of the limb. These lesions can be used to explore disease etiology(Ciesielska & Stark, 2020; Gonzalez-Garrido et al., 2022), social culture(Kokotovic, 2021; Lambert & Welker, 2019; Magalhaes et al., 2023), and medical advancements(Grauer & Roberts, 1996)^,9 from a broad cultural and social perspective.

Although fractures are frequently encountered in human remains, there are few historical reports of the medical interventions that were used to treat fractures. Archaeologists face challenges when studying the medical treatment of fractures for several reasons. First, the splints used for fracture treatment were often constructed from wood, which is challenging to preserve. Second, the absence of soft tissue makes the details of diagnosis difficult to obtain. Finally, complete bone remodeling makes it difficult to identify fractures or ascertain the post-traumatic time interval. Although historical accounts of medical interventions for fractures in ancient times exist in the literature(Knusel et al., 1995; Licata et al., 2019; Redfern, 2010; Smith, 1908), these accounts fail to address the development of the anatomical understanding of the human body in relation to fractures and the rationale behind the medical interventions that were applied.

In the present study, we investigated the remains of an individual with segmental femoral fracture. The remains were unearthed from the Tuchengzi site in Horinger, Inner Mongolia, China. Macroscopic observation, computed tomography (CT), and finite element analysis were used to reconstruct fracture formation, determine the nature of medical intervention, understand the healing process, and perform post-healing behavioral analysis. The application of finite element analysis in orthopedic biomechanics spans over four decades. It has been used for fracture mechanics analysis and to evaluate the efficacy of internal fixation(Huiskes & Chao, 1983; Taylor & Prendergast, 2015). Here, we present the first documented case of segmental femoral fracture in the field of archaeology and provide initial evidence of the type of medical intervention used for fracture treatment in China during the Warring States period.

Archaeological background

The Tuchengzi site, situated in Horinger, Inner Mongolia, China, at the southern base of the Yin Mountains and on the northern shore of the Yellow River, served as a significant thoroughfare from the Central Plains to the northern desert in ancient times (Fig. 1). Between 1997 and 2002, the Institute of Archaeology of Inner Mongolia Autonomous Region conducted several surveys and excavation campaigns at the Tuchengzi site and its surrounding tombs. Based on archaeological data analyses, the Tuchengzi site is broadly classified into six distinct periods (Supplementary Table S1). Archaeological investigations and historical documents(Chen et al., 2006; Yucai, 2007) indicate that during the Warring States period in ancient China, the state of Zhao military forces at this location and soldiers in the garrison predominantly engaged in agricultural activities.

The human bone specimen examined in this study was identified as HT1M18 and originated from a burial dating back to the Warring States period (3rd century BC) at the Tuchengzi site, which was excavated between 1997 and 2002. The skeleton of HT1M18 is incompletely preserved, with only the bilateral femur, bilateral tibia, and right humerus remaining. Our examination centered on the left femur of HT1M18, wherein the proximal one third exhibited an exaggerated bone callus connecting two angular and overlapping fracture fragments, while the distal one third protruded abnormally (Fig. 2).

Macroscopic observation

Macroscopic observation of all remaining bones of HT1M18 was performed following the methodology established by Roberts and Connell(Brickley & McKinley, 2004). Morphometric measurements of the femur, tibia, and humerus were obtained in accordance with Shao’s approach(Shao, 1985) (Supplementary Tables S2). Markers of sex and age, such as the cranial and hip bones, were missing; therefore, the long-bone sex determination formula was utilized to determine the sex of the individual(Liu, 1989; Liu et al., 1989.05). The body mass of HT1M18 was estimated using the body mass formula proposed by Ruff, McHenry, and Grine et al.(Auerbach & Ruff, 2004), taking the mean value from the calculations of the three formulae.

Radiological analysis

CT of the left femur of HT1M18 was performed to generate a three-dimensional virtual reconstruction. Conventional medical radiological equipment (Neusoft NeuViz Glory CT, Neusoft Medical Systems, Shenyang City, Liaoning Province, China) was used with the following imaging parameters: tube current = 59 mAs, tube voltage = 140 kV.

Finite element analysis of the femur

As depicted in Fig. 3, the CT images of the left femur of HT1M18 were imported in Digital Imaging and Communication in Medicine (DICOM) format into Mimics Research 21.0 (Materialise Inc., Leuven, Belgium), Geomagic Studio 2013 (Geomagic, US), and SolidWorks 2017 (Dassault Systemes, US) for three-dimensional virtual model processing. Subsequently, the finite element analysis results were computed using Ansys Workbench (Ansys, US).

Within Ansys Workbench, a static structural analysis model was constructed. In this investigation, all materials were simplified as isotropic homogeneous linear substances. Materials for the femur’s cortical and cancellous bone were assigned in accordance with Table 1(Sowmianarayanan et al., 2008). The finite element analysis of the femur was meshed with tetrahedral cells, resulting in 353,750 nodes and 219,247 meshes for the femur model. The mesh size was set to 3 mm.

Table 1

Material properties assigned to femur
	Elasticity modulus(MPa)	Poisson's ratio
Femoral cortical bone	17000	0.3
Femoral cancellous bone	1500	0.3

To simulate the post-fracture healing of the specimen, we examined two states: 1) standing with both legs and 2) walking. Previous reports have indicated that the stress on the hip joint during standing and walking is approximately 100–140% and 211–285% of the body weight, respectively(Bergmann et al., 2001). Moreover, the femur experiences varying degrees of torsional force during human locomotion(Duda et al., 1997; Schneider et al., 2001). Therefore, the loads were set as follows: 1) standing: femur head load of 100% of the body weight directed vertically downward, hip joint inversion of 15°, and distal fixation; 2) walking: femur head load of 250% of the body weight directed vertically downward, hip joint inversion of 10°, flexion of 20°, external rotation of 15°, torque force of 7 N-m, and distal fixation. The stress distribution of the femur in these two states of motion was then computed.

Macroscopic observation

Based on the presence of epiphyseal closure, we determined that the individual was likely an adult. Markers of sex and age, such as the cranial and hip bones, were missing; therefore, we used the method proposed by Liu et al.(Liu, 1989; Liu et al., 1989.05) in which two formulae that yield high success rates for femur-based sex determination were selected to determine the sex of the individual, as follows:

Z = maximum femur length + 0.5312 mid-femur circumference + 6.9691 superior femur width + 5.7888 femur epicondyle breadth − 3.4722 lateral femoral condyle length

Z = maximum femur length + 10.9605 sagittal subtrochanteric femur diameter + 6.9846 superior femur width + 7.2925 femoral head maximum diameter

Using these formulae, HT1M18 was identified as male, with the left femur displaying evident signs of a fracture in the proximal one third of the diaphysis. Displacement of the proximal fracture fragment occurred (Fig. 4). Intortion meant that the femoral neck anteversion angle disappeared and was replaced by a retroversion angle of 10.74°. The adduction angle was 5.47°, and the flexion angle was 21.34°. A conspicuous periosteal reaction was observed at the fracture site, resulting in the formation of an exaggerated bone callus. The bone callus exhibited favorable remodeling, bridging the fracture fragments and closing their medullary cavities. Simultaneously, an abnormal lordosis angle of 144.60° formed in the distal one third of the diaphysis. No macroscopic signs of fracture or periosteal reaction were detected, and the cause of the abnormal lordosis could not be determined.

Radiological study

CT revealed a concurrent double femoral fracture in the proximal one third and distal one third of the diaphysis. The proximal fracture exhibited an oblique pattern with a notable periosteal reaction at the fracture site, giving rise to a substantial bone callus that bridged the fractured ends and sealed off the bone marrow cavity. Callus remodeling occurred, and internally, pressure-induced trabecular bundles were observed (Figs. 5a and 5b), indicating that the individual engaged in extensive weight-bearing activities after fracture healing. The presence of sufficient mechanical stimulation prompted bone remodeling and trabecular bundle formation(Huiskes et al., 2000). Conversely, the distal fracture displayed a transverse insertion pattern, which was accompanied by bone remodeling and bone callus development within the medullary cavity (Fig. 5c).

Finite element analysis

The finite element analysis revealed that in the standing position, the femur exhibited a localized area of stress distributed along the medial side at the proximal end of the bone callus (Fig. 6). This area encompassed an approximate surface area of 80 mm², with the stress magnitude ranging from 46 to 51 MPa, while the stress distribution across the other regions remained uniform. In the walking position, different degrees of stress were observed along the medial side at the proximal end of the bone callus and along the lateral side at the distal end. Along the medial side at the proximal end, the stress was concentrated over an area of approximately 150 mm², with the stress magnitude ranging from 120 to 182 MPa. Along the lateral side at the distal end, the stress was concentrated over a region of 110 mm², and the magnitude of stress varied between 130 and 300 MPa.

Combining macroscopic observation and CT, fracture of the left femur of HT1M18 was identified as segmental femoral fracture. The fracture was located in the proximal one third and distal one third of the diaphysis. We determined that the segmental fracture resulted from a single traumatic event based on the extent of bone callus formation and remodeling.

Segmental femoral fracture is regarded as a specific type of fracture with a low incidence. Such fractures are commonly observed in younger people, and they are often associated with high-impact trauma, such as traffic accidents, heavy object impacts, or falls from great heights(Enninghorst et al., 2013; Liu et al., 2019; Salminen et al., 2000). However, in the present study, CT revealed that both parts of the fracture exhibited oblique and transverse patterns, while there was no indication of spiral or comminuted fracture. Consequently, we determined that the fracture was not a result of indirect force or crushing injury; rather, it was a result of direct trauma. Stress fractures and atypical fractures were ruled out based on their morphology and location(Shane et al., 2010; Uthgenannt et al., 2007). Additionally, the absence of infection and open fractures can be inferred from bone callus formation and remodeling(Licata et al., 2019). Numerous war-related mass graves, decapitated remains, and weapon remnants, such as arrowheads, bronze swords, and spearheads, have been discovered in several burials at the Tuchengzi site, which, in conjunction with historical documents, is identified as a war stronghold characterized by frequent violent conflicts(Chen et al., 2006; Yucai, 2007). Hence, we posit that the segmental fracture in the present case resulted from either a fall from a horse or a fall from a considerable height during battle. The high prevalence of violent trauma in this region contributed to a high incidence of fracture, subsequently driving the rapid accumulation of knowledge and expertise in fracture treatment among medical practitioners, as well as advancements in medical care.

Femoral fractures, particularly segmental femoral fractures, are frequently accompanied by complications, such as hemorrhage(Ostrum et al., 1993; Wertheimer et al., 2018), fat embolism(Allardyce et al., 1974; Blokhuis et al., 2017), knee stiffness(Morrison & Adams, 1949), and deep vein thrombosis of the lower extremity(Yang et al., 2022). The emergence of any complication poses a significant threat to individual’s life. Therefore, the trauma experienced by HT1M18 would likely have presented a formidable challenge to the medical standards of that era. CT demonstrated pronounced bone callus formation and remodeling in the fracture. Given that remodeling after fracture takes several years in humans, it was inferred that the individual survived for at least 1 year after the fracture occurred(de Boer et al., 2015). Therefore, the fracture itself was not the direct cause of the individual’s demise. Consequently, we concluded that the medical care during that time was sufficiently advanced to provide fracture fixation and high-quality treatment, thereby ensuring the individual’s survival despite severe trauma.

From the perspective of fracture displacement, segmental femoral fracture typically involves three fracture segments, each of which tends to undergo displacement due to muscular traction in the absence of human intervention (Fig. 7). In the present case, the proximal fracture segment exhibited deformities in flexion, external rotation, and abduction owing to the pull exerted by muscles, such as the iliopsoas, gluteus medius, and gluteus minimus muscles, along with other muscles around the hip(French & Tornetta, 1998; Garnavos et al., 1999). The mid-segment of the fracture demonstrated adduction and angulation outward due to the tension exerted by the hip adductor muscle groups. The distal fracture segment demonstrated posterior displacement due to the traction exerted by muscle groups surrounding the knee joint, such as the gastrocnemius muscle, as well as the gravitational force exerted on the limb(Zheng et al., 2014). However, abduction and external rotation displacement of the proximal fracture fragment and posterior displacement of the distal fracture fragment were rectified. The distal end actually displayed signs of overcorrection, indicating that the individual was treated with fracture reduction and splinting, with the use of compression pads beneath the splint to maintain reduction. The proximal compression pad was positioned on the anterolateral aspect of the proximal thigh to counteract muscle tension and correct the abduction and external rotation of the fractured mass. The distal compression pad was placed on the posterior aspect of the distal thigh to counteract muscle traction and rectify posterior displacement of the fracture mass.

Segmental femoral fracture often results in significant lower-extremity shortening(Johnson et al., 1984; Winquist & Hansen, 1980), necessitating the use of lower-limb traction prior to fracture reduction, particularly for distal fracture segments. Thus, the individual in the present case appeared to have undergone brief lower-extremity traction before resetting, although the traction was likely not sustained, leading to femur deformity and shortening after fracture healing. Despite anatomically aligned fracture healing not being achieved, reduction of the distal fracture segment met the criteria for functional realignment. This understanding of fracture reduction using compression pads to counteract muscle tension led us to conclude that medical practitioners during the Warring States period possessed a knowledge of the thigh anatomy, enabling them to guide appropriate fracture reduction and fixation.

From the perspective of fracture healing, the individual exhibited significant bone callus formation in the proximal one third of the femoral fracture, indicating the application of semi-rigid fixation, which triggered endochondral bone formation. Conversely, no obvious bone callus was observed in the distal one third of the diaphysis, implying the implementation of rigid fixation leading to direct bone formation(Claes et al., 2012). CT revealed the presence of pressure-induced trabeculae within the bone callus. These observations indicate that the fracture underwent the three phases of fracture healing, namely inflammation, repair, and remodeling(Claes et al., 2012; Einhorn & Gerstenfeld, 2015; McKibbin, 1978). Previous studies have demonstrated that both early fracture instability and insufficient mechanical stimulation during the later stages can impact bone healing(Claes et al., 2012; Duan & Lu, 2021). Therefore, based on the results of fracture healing, it can be inferred that medical practitioners during that era possessed rudimentary knowledge of the fracture healing process, enabling them to guide the appropriate treatment of this individual, avoiding premature weight-bearing that could impede fracture healing and complications arising from prolonged fixation.

The finite element analysis results revealed variations in the magnitude, extent, and stress distribution at the fracture site during different motion states. In the standing position, the stress was primarily concentrated medially at the proximal end of the bone callus, aligning with the direction of femur force transmission. The maximum recorded stress was 51 MPa, which is significantly lower than the yield strength of the femur (120–140 MPa)(Mohammadkhah & Day, 2018). This suggests that the bone callus could withstand the load experienced during standing, and the individual would have been capable of standing after fracture healing. In the walking position, the stress was concentrated along the medial side at the proximal end of the bone callus and on the lateral side at the distal end, which is consistent with the direction of femur force transmission. However, some areas experienced stress that surpassed the yield strength of the femur(Mohammadkhah & Day, 2018), reaching up to 300 MPa. Physiologically, when bone stress exceeds yield strength, localized yield collapse occurs in small areas, leading to microfracture and bone resorption at the site at which stress is concentrated. However, yield collapse across a broader area may result in fracture, indicating that the bone callus was unable to withstand the load of normal walking. Consequently, HT1M18 would have required compensatory movement or assistance from tools to facilitate walking following fracture healing.

This study reports the examination results of a human specimen that was unearthed from the Tuchengzi site, Horinger, Inner Mongolia, China, and was believed to be from the Warring States period (3rd century BC). The individual experienced segmental femoral fracture. The occurrence of segmental femoral fracture could be directly attributed to an injury associated with an occupational activity. The medicine standards prevalent in China during the Warring States period appear to have been sufficiently advanced to successfully treat such complex fractures. We suggest that medical practitioners must have possessed a comprehensive understanding of thigh anatomy, enabling them to effectively guide fracture reduction and fixation. The application of appropriate medical intervention facilitated fracture healing and restoration of load-bearing capacity in the present case. Although the individual was capable of performing weight-bearing activities, femur malunion necessitated compensatory movement or the use of assistive devices during walking. This case is the first report of segmental femoral fracture within the field of archaeology, and it also serves as the earliest evidence of medical intervention for fractures in China. The findings substantially contribute to our understanding of ancient Chinese medical practices, and further research endeavors are warranted to comprehensively explore the extent of medical care in ancient China.

Funding

Partial financial support was received from Laboratory of Bioarchaeology, Jilin University.

Author contributions statement

Haiyang Xing and Ruiqi Zou performed the experiment and wrote the manuscript. Min Yi and Zhuoting Xie collected the data. Sen You and Jianhua Liu analyzed the data. Xiongfeng Tang, Quanchao Zhang and Yanguo Qin revised the paper and finished the submission. All authors reviewed the manuscript.

Data Availability

All data generated or analysed during this study are available in the main text and supplementary information.

Competing interests

The authors declare that they have no competing interests.

Ethics approval/declaration

Not applicable

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No competing interests reported.

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Segmental Femoral Fracture Malunion: Evidence and Prognostic Analysis of Medical Intervention in the 3rd Century BC

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