The pathological and anatomical changes in the spine and its surrounding tissues caused by spinal disease were related to the arterial and venous blood supply around the vertebral bodies[2].
The arterial blood supply of vertebral bodies
The arteries supplying blood to the vertebra were segmental arteries, which came from the vertebral artery, posterior intercostal artery, lumbar artery, and lateral sacral artery from top to bottom. The arteries ran along the ventral surface of the spinal nerve into the intervertebral foramen, also known as the spinal artery. After entering the intervertebral foramen, the spinal artery was divided into three branches: 1) dorsal collateral artery, which mainly supplied blood to the pedicle, lamina, transverse process, spinous process, dura mater, and epidural space. The dorsal branches of the superior and inferior spinal artery anastomosed with each other and were accompanied by the posterior side of the internal vertebral venous plexus. 2) The middle branch artery, which supplied the dura mater, including the spinal nerve root, and penetrated into the dura with the nerve root to supply blood to the spinal cord. 3) The abdominal collateral artery, which supplied the vertebral bodies, the anterolateral part of the dura mater, and the tissue of the epidural space. The typical abdominal collateral artery was divided into ascending and descending terminal branches, which entered to the center of the rear of the two adjacent vertebral bodies oblique upward and downward, respectively, and penetrated into the vertebral body at the deep surface of the posterior longitudinal ligament. Therefore, each vertebral body received a blood supply from four arteries from the rear: two on each side, one upper, and one lower.
Venous return to the spine
The veins of vertebra constitute the vertebral venous plexus, which is the same length as the spine, and is divided into two parts: the internal vertebral venous plexus and the extravertebral venous plexus. The internal vertebral venous plexus is located in the spinal canal, is densely distributed between the dura mater and the periosteum, and is divided into two parts, each with two longitudinal venous trunks and many anastomotic branches. The intravertebral venous plexus collects venous blood from the vertebra and spinal cord and passes it into the intervertebral vein (segmental vein) at the intervertebral foramen. The external vertebral venous plexus is also divided into two parts: anterior and posterior. These parts collect venous blood from the vertebra and surrounding soft tissues. The internal vertebral venous plexus is connected with the extravertebral venous plexus at the gap between the intervertebral foramen and the ligamentum flavum on both sides, and is also connected with the intracranial basal venous plexus at the foramen magnum. Therefore, inflammation of the posterior abdominal wall and lumbar back can spread to the brain through the vertebral venous plexus at any time[3].
Blood supply to the cartilage endplate
The main role of the cartilage endplate is load-bearing. It also participates in nutrient exchange and infiltration of intervertebral discs. The nutrient exchange channel and osmotic function of the cartilage endplate are closely related to spondylitis. Although the blood vessels passing through the cartilage endplate are occluded in adulthood in humans, many pores in the endplate remain open, which can maintain the characteristics of the semi-permeable membrane of the cartilage endplate[4]. This particularity enables small molecular components, such as water, to diffuse with changes in osmotic pressure. Under a scanning electron microscope, the vascular buds, which did not penetrate the interface between the cartilage endplate and nucleus pulposus, were still densely distributed in the cartilage endplate. In the area near the nucleus pulposus, these small vascular buds were more densely distributed. These small blood vessels were intertwined in the form of branches and had expanded branches.Along with these microvascular buds, many tiny lymphatic vessels existed. There were also dense microvessels, blood sinuses, and lymphatic capillaries at the two ends of the vertebral body adjacent to the cartilage endplate, especially at the central part of the cartilage endplate. After bacteria enter the human body, because of the abundant blood supply of the vertebral endplate, this site is the first to be invaded by bacteria. Bacteria then further invade the intervertebral disc and vertebral body, causing discitis and vertebritis. The vascular supply of intervertebral discs changes significantly with age. Infants and children have a more abundant vascular supply compared with adults. The capillary networks at the edges of vertebra adjacent to intervertebral discs are denser in infants and children compared with adults. Several blood vessels penetrate deep into the infant’s intervertebral disc, which are not present in most adolescents and all adults[5].
Occurrence and development of spinal infection
Embolism is caused by bacteria staying in the terminal vertebral artery. At present, the most commonly accepted hypothesis for vertebral bone infection is that the infected bacterial embolus diffuses in the arterial system and stays in one place to form a bacterial mass, resulting in arterial infarction and subsequent infection. Because of the abundant capillary networks at the edges of vertebra adjacent to intervertebral discs and the number of arteries at this position, bacteria often stay here, and osteomyelitis is the most common occurrence at the edge of the vertebral body. In adults, the epiphyseal artery is the terminal artery, and septic embolism can lead to a large area of purulent infarction. Then, the infection may extend to the contralateral vertebral endplate through the periosteal aorta or through the intervertebral artery to the endplate artery of the adjacent vertebral body, leading to infection in the adjacent vertebral body, which does not necessarily affect the central part of the vertebral body.
Another route of bloodborne transmission is the venous route. The epidural venous plexus in the central canal is a series of valveless veins. Inflammatory bowel disease, urinary tract infection, and pelvic infection spread to the vertebral body through venous blood. In cases of penetrating trauma or direct exposure related to skin rupture and open wounds, bacteria may be directly inoculated in the spine. Spinal surgery, negligent exposure related to non-spinal surgery, and secondary hospital infection are also sources of spinal infection[6].
In both children and adults, epiphyseal infection can affect the corresponding intervertebral disc. Because the adult intervertebral disc is almost without a vascular supply, there is no immediate bloodborne immune defense mechanism. Infection occurs easily and develops rapidly. Bloodborne pathogens mainly involve intervertebral discs. In children with vertebral infection, because of the continuous blood supply of intervertebral discs, the chance of disc infection is reduced. Sometimes it may only present as discoid inflammation. Children may experience abdominal pain, which is often their initial symptom, when the anterior longitudinal ligament is pulled during lumbar extension. Prevertebral and paravertebral abscesses are caused by continuous spread of infection from the spine to adjacent soft tissues[7].
In addition, involvement of paravertebral veins provides a route for abscess formation; thus, infection can enter adjacent soft tissues, and abscesses can from phlebitis or thrombophlebitis. In extensive paravertebral inflammation, secondary involvement of adjacent vascular structures, such as the aorta, may lead to vasculitis and mycotic aneurysm. In the middle and late stages of disease, if the abscess around the vertebral body is not completely absorbed, granulation tissue can be produced around the injured vertebrae, which is evenly distributed around the vertebral body. Sometimes we can see formation of the epidural mass behind the vertebral body, which is an equal strength mass formed by the vertebral cortex, posterior longitudinal ligament, dura, and cerebrospinal fluid. With T2WI, subdural effusion may be equal to the high signal intensity of cerebrospinal fluid, so it may be missed at diagnosis. At this time, the image can be added to differentiate between epidural abscess and subdural effusion. In the absence of detectable bone or disc disease, hematogenous dissemination of purulent organisms rarely causes an epidural abscess alone.
Pathophysiology of spinal disease
Spinal tuberculosis
Spinal tuberculosis is a chronic and destructive disease, which tends to be in a relatively late stage when symptoms appear[8]. The morphological and pathophysiological changes of spinal tuberculosis are the most serious changes observed in infectious spondylitis. Tuberculosis is most common in thoracic vertebra, followed by lumbar and cervical vertebra. Infection begins in the vertebral body, and the most common site is the anterior and upper part of the vertebral body. Tuberculosis can selectively affect part or all of the vertebral body (pedicle, lamina, posterior spinous process) without involving adjacent intervertebral discs[9]. Mycobacteria lack proteolytic enzymes to digest the nucleus pulposus, which can avoid destruction of intervertebral discs in the early stages of disease. In the late stages of disease, with the destruction of the rich blood supply area by Mycobacterium tuberculosis and its impact on marginal blood vessels supplying nutrition to the intervertebral disc, the intervertebral disc will lose its nutritional supply and undergo pathological changes. In other words, intervertebral disc damage will occur only when spinal tuberculosis infection is relatively advanced.
Cancellous bone is abundant in the vertebral body. When spinal tuberculosis occurs, damage occurs to the vertebral body. The vertebral endplate is easy to damage, and when bone destruction is serious, compression fracture will occur. Infection involves the tissue around the vertebral body and formation of paravertebral abscess. When liquefaction of the cheese-like material in spinal tuberculosis occurs, a localized abscess will form on the periosteum on one side of the vertebral body, and periosteal hyperplasia and granuloma formation will occur under inflammatory stimulation. If inflammation cannot be controlled in time, pus may continue to peel off the vertebral periosteum, the abscess will continue to increase in size, and the periosteum will burst. The huge abscess will flow to different places through the space. A cervical tuberculous abscess can form a retroesophageal abscess, and a lumbar tuberculous abscess can flow to the anteromedial thigh. Spinal tuberculosis is associated with bone abscess, but paraspinal soft tissue abscess is often beyond the scope of the affected vertebral body and intervertebral disc[10].
Suppurative spondylitis
Staphylococcus aureus, Escherichia coli, Salmonella, Pseudomonas aeruginosa, and Klebsiella pneumoniae are common pathogens of spinal infection. Aureus is the most common pathogenic bacterium that causes suppurative spondylitis, which mostly occurs in adults. It is mainly associated with bloodstream infection, and a few cases are caused by trauma, intervertebral disc surgery, lumbar puncture, and acupuncture. The onset of disease is acute, and symptoms are obvious, often involving chills and high fever and lower back pain with thorn process percussion pain[11].
Suppurative spondylitis progresses rapidly, and MRI signal changes can be found after 1 week. Early lesions easily diffuse the entire vertebral body, which can lead to osteolytic bone destruction in different areas of the vertebral body. In the early stages, the pathogen can easily affect the intervertebral disc, mainly because during inflammation, a large number of neutrophils secrete proteolytic enzymes, which directly dissolve and destroy the intervertebral disc. Aureus spondylitis often appears in the early stages of paravertebral soft tissue signal abnormalities, is prone to paravertebral abscess and can present with a number of small abscess foci. The main reason is that the abscess under the action of proteolytic enzymes is more likely to spread to paravertebral tissue, but the range is generally not more than the height of the diseased vertebral body[12].
Expansion of adjacent vertebral body lesions is caused by direct invasion of intervertebral discs. Plain MRI findings of hematogenous suppurative spondylitis are characteristic and can reflect pathophysiological changes. If collapse and deformity are not observed in the spine, early suppurative spondylitis is usually limited to the spinal marrow and does not extend to the paravertebral region. In the early stages of spondylitis, bone marrow edema in the vertebral body is first found on MRI, which shows a low signal on T1WI and a high signal on T2WI. After using an enhancer, the signal difference increases. In the early stages of infection, lesions begin to occur below the endplate. As the disease progresses, it gradually involves the intervertebral disc between the endplate and the involved vertebrae. Early discitis may be difficult to detect, and normal discs show a high signal intensity on T2WI. The decrease in T2WI signal of intervertebral discs can be regarded as a reliable early sign of an improvement in discitis.
Bone marrow edema adjacent to the endplate may be a part of normal intervertebral disc degeneration. In a severely degenerated spine, intervertebral disc degeneration produces edema or fluid in the intervertebral space. At this time, T2WI shows a high-intensity signal, accompanied by signal changes in the endplate. However, careful examination of the cortex of the endplate without erosion should indicate presence of degenerative changes in the spine rather than intervertebral disc infection. Fat-suppression techniques combined with intravenous contrast agents have recently been recommended because they can improve the significance of enhanced structures by eliminating signals from adjacent adipose tissue[13].
Brucella spondylitis
Brucellosis is an infectious and allergic disease caused by the Brucella genus. Cattle, sheep, and other livestock are the main sources of infection. Bacteria enter the human body through the skin, respiratory tract, digestive tract, conjunctiva, and other routes. The incidence rate in pastoral areas is high, but with the development of population mobility and non-pastoral farming, and an increase in the number of mutton-eating people, the trend of spread to pastoral areas is increasing.
The upper endplate of the vertebral body has a rich blood supply, which is the first site of Brucella invasion. When the cells further invade the intervertebral disc and vertebral body, discitis and vertebritis occur. With discitis, the intervertebral space becomes narrow and bone near the upper and lower edges of the vertebral body is damaged. Bone destruction in Brucella spondylitis is limited and mild. At the same time, there is new bone formation. The speed of bone formation and repair is faster than bone destruction. Bone hyperplasia of the vertebral periosteum is characterized by lip-like protrusions of the vertebral body edge, and osteophytes are formed nearby. A bone bridge is gradually formed in adjacent vertebra, and the edge of the vertebral body presents a “lace-shaped” change. In general, the state is relatively complete or only slightly wedge-shaped. Brucella can also invade the soft tissue around the vertebral body, forming paravertebral abscess and intraspinal abscess, which compresses the spinal cord, nerves, and cauda equina, resulting in corresponding neurological damage. Multiple granulomas and multiple small purulent foci can coexist[14].
MRI is a reliable follow-up tool in the treatment of suppurative spondylitis. As spinal infection improves, the abnormal high signal intensity on T2-weighted sagittal images of infected vertebral bodies gradually decreases, and the signal intensity on T1-weighted images gradually increases, which suggests that cellular bone marrow is replaced by fat, indicating healing[15].
Pathological fracture of the vertebral body may occur when tumor growth invades vertebral bone. Pathological fracture is characterized by compression and deformation of the involved vertebral body to varying degrees, which can bulge to the four sides and cause obvious kyphosis. Discoid fracture may involve chronic uniform compression of trabecula or cortical structures when all vertebral bodies are eroded by the tumor. The inverted wedge fracture is due to the abundant blood supply of the posterior upper quarter of the vertebral body, which is also the site of early metastasis. In the process of metastatic invasion, the load-bearing time of the lesion is long, so compression occurs relatively early and is more marked. At the same time, it can be accompanied by enlargement and deformation of involved vertebral appendages[16].
Second, compression of the spinal canal, spinal cord, and nerve root can be observed. The results show that the epidural mass protruded into the spinal canal, and epidural fat was compressed, deformed, and even disappeared. The subarachnoid space was compressed and occluded; the spinal cord was mostly compressed, with varying degrees of compression and displacement. Compression of lateral recess could lead to stenosis.
In addition, a paravertebral soft tissue mass can be observed. The mass is often connected with the vertebral body, with the lesion at its center, and the upper and lower range is limited. The larger soft tissue mass is located on the side of the junction between the vertebral body and the appendix, and its signal is similar to that of vertebral body disease. The intervertebral disc was rarely involved in the metastatic tumor, so there was no obvious change in the intervertebral space. This may be related to the avascular structure of the hyaline cartilage endplate, fibrocartilage ring, and nucleus pulposus. Metabolism of the intervertebral disc is realized by diffusion of the endplate. The cartilage endplate and fibrocartilage ring act as a barrier to tumor expansion[17].
Bacteria and tumor cells have distinct characteristics and different manifestations of spinal invasion. Combined with clinical manifestations, we should carefully identify differences in spinal diseases using MRI to facilitate early drug intervention and unnecessary invasive operations. This study found that MRI can provide early diagnostic evidence for spinal lesions.