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. 2016 Jul 7;8(2):179–185. doi: 10.1111/os.12232

Transnasal Endoscopic Biopsy Approach to Atlas Tumor with X‐ray Assisted and Related Radiographic Measure

Zhen‐feng Li 1, Xian‐hao Shao 1, Li‐qiang Zhang 1, Zhi‐ping Yang 1, Xin Li 1, Qiang Yang 1, Jian‐min Li 1,✉
PMCID: PMC6584101  PMID: 27384726

Abstract

Objective

To develop an endoscopic transnasal approach to atlas tumors and study its practicability.

Methods

This article comprises two components: an illustrative case report and observational data on 50 volunteers. As to the case report, a 34 year old man presented with occipital pain for more than 3 months and underwent systematic investigation in Qilu Hospital of Shandong University. CT and MRI scans showed bony destruction in the craniovertebral junction (CVJ) suggestive of tumor. Via an endoscopic transnasal approach to the suspected atlas tumor through the inferior nasal meatus, a Gallini biopsy needle was used to obtain tissue for examination. The procedure was performed endoscopically with double orientation X‐ray guidance and coaxial technology after establishing the shortest distance for the biopsy track and range of target tissue and was assisted by manual palpation. As to the observational data, 50 volunteers underwent atlas‐related morphometric image measurement using gemstone CT equipment. Biopsy track angles, range for biopsy of the atlas and biopsy track distances were measured by a blinded operator on CT images.

Results

Case report: pathological examination of the biopsy resulted in diagnosis of a chordoma. There were no complications such as bleeding, infection or spinal cord injury. One month later, the patient underwent tumor resection and reconstruction in other hospital and the diagnosis of chordoma was confirmed by pathological examination of the resected specimen. Observational data: measurements obtained from CT scans of the 50 volunteers were as follows. Biopsy track angles: mean leaning inside angle 3.53° ± 0.39° and mean posterior slope angle 13.05° ± 1.39°. Range for atlas biopsy: transverse diameter 11.84 ± 1.24 mm and longitudinal diameter 9.67 ± 0.90 mm. Biopsy track distances: from atlas to nostril, and to anterior and posterior edges of the inferior turbinate mucosa were 94.52 ± 5.03 mm, 78.21 ± 4.63 mm, and 33.51 ± 3.13 mm, respectively.

Conclusions

An endoscopic transnasal approach enables biopsy and diagnosis of tumors in the anterior arch of the atlas. Relevant measurements were obtained by assessing CT scans of 50 volunteers to assist operators to determine the effective and safe range for transnasal atlas biopsy.

Keywords: Atlas, Biopsy, Endoscopy, Image measurement, Transnasal approach

Introduction

The atlas is located at the craniovertebral junction (CVJ); adjacent organs include the spinal cord, C1 nerve, vertebral artery and pharynx1. Chordomas, osteoblastomas and Ewing sarcomas are the commonest tumors that occur in in the anterior tubercle and anterior arch of the atlas, which may also be affected by rheumatoid arthritis and other inflammatory conditions2, 3, 4. Atlas tumors reportedly have little morbidity5, 6. According to George et al., chordoma is the commonest type of tumor in this location7. Before operating on suspected chordomas, a biopsy is essential to make a definite diagnosis. The biopsy approach should be selected according to the planned procedure for subsequent reconstruction and screw fixation of the atlas8. Ewing sarcoma, which is also a common primary tumor of the C1 vertebra, most frequently occurs in children9. Other tumors such as synovial sarcoma, mesenchymal chondrosarcoma and primitive neuroectodermal tumor have reportedly occurred in the atlas10, 11, 12. Thus, it is essential to diagnose an atlas tumor by biopsy prior to planning its definitive management.

A definite diagnosis and subsequent selection of appropriate surgical options are important in determining patients’ prognoses13, 14. However, a definite diagnosis cannot be made based only on the medical history and imaging findings; pathological examination of a biopsy specimen is the gold standard for diagnosis. Histopathologic examination and immunohistochemistry allows diagnosis of the specific type of tumor: sarcomatoid chordoma, undifferentiated chordoma and so on. Open biopsies are rarely performed for diseases of the anterior tubercle of the atlas. Needle biopsies can be obtained from the anterior parts of the atlas via transoral, lateral percutaneous and posterior approaches; however, all of these approaches have significant limitations15, 16, 17, 18, 19, 20, 21. Transnasal endoscopic (TNE) and transoral endoscopic (TOE) approaches are the most popular methods because they utilize convenient pathways to the CVJ area. According to Seker et al., TOE is more appropriate for lesions from the atlantoaxial joint to the C3 level, whereas TNE utilizes a more direct pathway to the clivus and atlas22. Visocchi et al. believe that the TOE approach is more flexible, whereas the TNE approach better protects the soft palate and causes minimal injury23. Liu et al. state that, while TOE was previously regarded as the “gold standard” and has undergone various modifications24; the advent of TNE has provided another safe and effective approach that also delivers a wide panoramic view via the endoscope25. Both TOE and TNE have extensive application in other diseases of the CVJ such as osteoradionecrosis, rheumatologic disorders, infections, traumatic injury and so on26, 27. A lateral transcondylar approach is another important way of approaching the CVJ; however, it involves extensive resection of posterior and lateral bony structures. Although this approach avoids the extracranial and intracranial vertebral artery, it is inevitable that the complex adjacent vessels and nerves are encountered and are at risk of injury during the procedure28, 29, 30. In contrast, an endoscopic transnasal approach to the atlas is via a natural cavity approach, which reduces the risk of trauma, allows more accurate biopsy location, and is very convenient for the surgeon31, 32. However, although some endoscopic endonasal surgery has been performed on the clivus and upper cervical vertebrae33, 34, thus far use of this approach to obtain image‐guided biopsies has not been systematically reported.

In the late 1980s, endoscopy for the management of sinonasal inflammatory conditions was introduced and in the 1990s the use of endoscopy was extended to neurosurgical procedures in the CVJ region35. Development of transnasal endoscopic procedures has been a long journey. The original aim of using TNE to perform surgery on the base of the skull was to modify the traditional transsphenoidal approach36. Thereafter TNE was confirmed to be a safer and more effective means of performing surgery on the base of the skull37. After 20 years of development, TNE has been successfully used to diagnose and treat pituitary adenomas, clivus chordomas and other common diseases of the base of the skull. There are more reports about the role of TNE in clivus and foramen magnum operations than in procedures in the CVJ region. However, this technique has also been used for atlantoaxial subluxation and odontoidectomy38. Endoscopic approaches offer several advantages, including lower infection rate, decreased pain, shorter hospital stay and faster recovery. However, TNE can have adverse effects, including nasal crusting or discomfort, cerebrospinal fluid (CSF) leakage and meningitis, which can occur after surgery on the central nervous system39. Endoscopic techniques have been developed rapidly in recent decades, an expanded endonasal approach remedying some of the disadvantages of traditional TNE40. The developments of simulators has enabled realistic stereoscopic visualization and improved biofeedback. Nowadays, transnasal endoscopic technology is also utilized for paranasal lesions, orbital tumors and even oesophagogastroduodenoscopy41, 42, 43.

The purpose of this study was to introduce a new surgical strategy, namely transnasal biopsy in a patient with an atlas tumor via X‐ray‐assisted nasal endoscopy. Additionally, we obtained images from 50 volunteers and used them to measure and calculate the normal biopsy angle, depth, track distance and biopsy range. We then compared our data with those reported by others to determine whether it was effective.

Materials and Methods

Case Report

A 34‐year man presented to our institution with pain in the occiput and posterior cervical discomfort with no obvious cause, accompanied by cervical stiffness and limitation of activity. The pain was paroxysmal and was more intense at night. He had no limb pain or numbness.

Physical Examination

On examination, the physiological curvature of the spine was normal. The mobility of the cervical spine was limited with cervical flexion 20°, posterior extension 15°, left lateral flexion 30°, right lateral flexion 45°, left rotation 45° and right rotation 45°. There was no tenderness or percussion pain in the spinous processes. Neck compression and cervical nerve stretch tests were negative. Movement in all limbs was normal. Muscle strength and tone and sensation in the extremities were normal. Reflexes were as follows: bilateral biceps (++), bilateral elbow (++), bilateral knee jerk (+++), bilateral ankle jerk (++), bilateral Hoffmann sign (−) and bilateral Babinski's sign (−).

CT and MRI

A CT scan showed expansive destruction of the odontoid process of the axis and worm‐eaten‐like destruction of the anterior arch of the atlas, which was more pronounced on the right. MRI showed long T1 and T2 changes in the area of the lesions. Fat‐saturated T2‐weighted (T2WI) images showed a cauliflower‐like high signal, local compression of the dural sac and a narrowed subarachnoid space. Enhanced MRI showed the lesion signals were enhanced and mixed. Emission computed tomography showed slightly uneven increased upper cervical radioactivity. A provisional diagnosis of chondrosarcoma or chordoma was made (Figs 1, 2).

Figure 1.

Figure 1

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CT image showing bone destruction in the anterior arch of the atlas and clivus.

Figure 2.

Figure 2

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MRI T2WI image showing soft tissue mass and destruction of the anterior arch of the atlas.

Transnasal Approach Biopsy

After induction of general anesthesia, the patient was placed in a supine position and the operation area sterilized and draped as usual. The mucosa of the right nasal cavity was infiltrated with adrenaline and tetracaine. A 3 mm‐diameter 0° endoscopic probe showed a bulge in the retropharynx at the level of the anterior arch of the atlas and 0.5 cm right of the median line of the nasopharynx. An Italian Gallini bone biopsy needle was inserted 0.5 cm to pierce the mucosa, longus collis muscle and tumor capsule and the yellowish‐white tumor tissue thus revealed grabbed with a grabbing instrument. The needle was then inserted 1.5 cm beyond the submucosa to pierce the anterior arch of the atlas. Tumor tissue was grabbed after confirmation of the location by C‐arm (Arcadis Varic; Siemens, Sacramento, CA, USA). The needle was then removed and a 0.4 cm × 1 cm gelatin sponge used to fill the biopsy track and a cotton dressing to cover the surface. There was no bleeding. Postoperatively, the patient had good for movement of the extremities, voluntary breathing and stable vital signs (Figs 3, 4).

Figure 3.

Figure 3

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X‐ray film showing the relationship between the biopsy needle and the atlas during the procedure.

Figure 4.

Figure 4

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Endoscopic image showing the location and depth of the biopsy needle in the anterior arch of the atlas.

Imaging Data

Equipment

Images were obtained using GE gemstone CT equipment produced by General Electric (GE Healthcare Bio‐Science, Piscataway, NJ, USA).

Volunteers

Fifty volunteers ranging in age from 20 to 60 years underwent 1 mm thin CT scanning and sagittal images were reconstructed for analysis. This study was approved by the Ethics Committee of our institution.

Variables Measured

The following variables were assessed on the volunteers’ CT images (Figs 5, 6).

Figure 5.

Figure 5

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Sagittal CT image showing the method for measuring (A) the posterior slope angle (PSA), the distances from the atlas to the anterior or posterior edge of the inferior turbinate mucosa and nostril and (B) longitudinal diameter of the atlas.

Figure 6.

Figure 6

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CT image showing the method for measuring (A) the leaning inside angle (LIA) and (B) transverse diameter of the anterior arch of the atlas behind the nasopharynx.

Biopsy Track Angles

(i) Leaning inside angle (LIA): The sectional image that most clearly showed the nostrils and nasal mucosa was identified and the angle between a line linking the anterior edge of the inferior nasal turbinate and the bony structure of the clivus and the median line measured and defined as the LIA.(ii) Posterior slope angle (PSA): The sectional sagittal reconstruction image that most clearly showed the nasal concha bony structure was identified and the angle between a line connecting the midpoint of the inferior nasal meatus and the anterior tubercle of the atlas and horizontal line measured and defined as the PSA.

Range for Atlas Biopsy

(i) Transverse diameter of anterior arch of the atlas: The transverse diameter of the anterior tubercle and arch adjacent to the retropharynx were measured in the image in which this angle was at its maximum. (ii) Longitudinal diameter of the atlas: The longitudinal diameter from the superior to the inferior edge of the atlas was measured on a sagittal reconstruction image.

Biopsy Track Distances

(i) The distances between the atlas and the anterior and posterior edges of the inferior turbinate mucosa were measured on the sagittal image that showed the mucosa most clearly. (ii) The distance between the atlas and nostril was measured from the center of the nostril to the atlas on a sagittal image.

Results

Clinical Outcomes for Illustrative Case

Gross assessment of the patient's tumor revealed yellowish white crisp tissue. Histopathological findings were characteristic of chordoma and immunohistochemistry showed epithelial membrane antigen (+), creatine kinase (+), S100 (+), and Ki67 positivity rate of 5%, all of which are consistent with the diagnosis of chordoma. There was no evidence postoperatively of injury to adjacent areas; vital signs were stable, and sensation and motor function in all four limbs was normal. There were no postoperative complications such as pharyngeal discomfort, bleeding, infection, or failure to heal. The patient subsequently underwent tumor resection and reconstruction surgery in another hospital and postoperative pathological examination confirmed the diagnosis of chordoma (Figs 7, 8).

Figure 7.

Figure 7

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Gross appearance of tumor: a yellowish, gelatinous mass.

Figure 8.

Figure 8

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Photomicrograph (×40) showing some vacuolated cells with a signet‐ring like appearance. EMA (+), CK (+), S100 (+).

Imaging Data

Seven imaging indexes were measured on the 50 volunteers, providing 50 sets of valid data. The minimum and maximum LIAs were 2.8° and 4.4°, respectively; the mean LIA being 3.53° ± 0.39°. The corresponding PSAs were 9.8°, 15.8° respectively, and 13.05° ± 1.39°.

The minimum and maximum transverse diameters of the biopsy range were 9.10 mm and 14.40 mm, respectively; the mean transverse diameter being 11.84 ± 1.24 mm. The corresponding longitudinal diameters were 8.00 mm and 12.40 mm, respectively, and 9.67 ± 0.90 mm.

The minimum and maximum distances from the atlas to the nostril were 84 mm and 106.1 mm, respectively; the average distance being 94.52 ± 5.03 mm. The corresponding distances from the atlas to the anterior edge of the inferior turbinate mucosa were 67.7 mm, 86.4 mm, respectively, and 78.21 ± 4.63 mm. The corresponding distances from the atlas to the posterior edge of the inferior turbinate mucosa were 27.9 mm and 40.3 mm, respectively, and 33.51 ± 3.13 mm.

Comparisons with Previously Reported Values

Attempts were made to compare our measurement with those reported by others; however, because of different measure methods, the results varied considerably. The transverse diameter represents the safe and effective range within which to biopsy the atlas. This value should exceed the length of the ipsilateral anterior arch to ensure successful biopsy but be shorter than the distance between the external borders of the lateral masses to ensure safety. Cao et al. reported an average length for the anterior arch of the atlas of 10.0 mm and a distance between the external borders of the lateral masses of 25.8 mm on the left side and 27.2 mm on the right side44. Some studies have reported moderate variations in measurement that are attributable to individual differences45, 46. Our data are consistent with these findings. As for the total distance involved in this approach, we regard the entry point as the nostril whereas Lin et al. take the inferior edge of the nasal bone as the entry point47. Both Lin et al. and the present team chose the anterior point of the atlas as the destination. Their measurement was 93.65 ± 5.81 mm. The different entry points would impact the distance involved in the transnasal approach and the LIA; however, such discrepancies are acceptable because the nostril and inferior edge of the nasal bone are anatomically close to each other. We checked the consistency of our mean value by Student's t‐test and analyzed the homogeneity of variance by the χ2 test. We set α = 0.05 as the level indicating consistency and our results were t = 0.238 and χ2 = 37.45, both of which are significant according to their α values. Thus, our findings are consistent with previously published morphologic data.

Discussion

After 20 years of development, the transnasal endoscopic technique has become extremely well established and safe. When combined with imaging guidance and visual location during the procedure, this endoscopic approach provides realistic stereoscopic vision and a wide surgical field. Our patient had no complications, including no bacterial infection. However, we took care to avoid contact with the spinal canal to avert the potential risks of CSF leakage and meningitis. This technique exposes the atlas clearly and enables a needle biopsy approach to the atlas through the inferior nasal meatus. Our procedure also confirmed that the anterior structure of the atlas can be clearly exposed with the help of a transnasal endoscope. With X‐ray guidance, the depth of the puncture needle can be precisely evaluated, thus avoiding the inconvenient aspects of CT17. The whole process is minimally invasive while highly precise, safe and dependable.

There is a low incidence of tumors of the atlas; however its adjacent organs are complex and important. Common tumors in this region include chordomas, osteoblastomas, Ewing sarcomas and other primary and metastatic tumors. The treatment provided determines the patients’ prognosis and pathological examination remains the gold standard for diagnosis. Biopsy approaches include the transoropharyngeal, lateral percutaneous and posterior approaches. With lateral percutaneous biopsy, the adjacent organs are complex and easily injured15, 17. With posterior cervical puncture, the patients have to undergo laminectomy with its associated considerable trauma and high risk of infection13. Disadvantages of the transoropharyngeal approach include the low anatomical position of the atlas, difficulty in location of the target tissue, the transverse diameter limitations on surgery, a too deep longitudinal distance, and risk of complications such as infection by oral bacteria22, 48. The transnasal approach biopsy takes advantages of a natural cavity, avoids important adjacent organs, and involves little trauma. The procedure is relatively simple because it is easy to locate the position of the anterior tubercle of the atlas through the inferior nasal meatus32. A limitation of this approach is that only small biopsies can be obtained through the narrow nasal meatus. In our patient, needle biopsy was performed successfully and provided a satisfactory sample and outcome. The pathological findings were consistent with the preoperative evaluation, and there were no complications. Thus, we confirmed the safety and effectiveness of the transnasal approach.

In our volunteer study, we measured and determined the angles and depth of the nasal meatus path, identified the organs adjacent to different depths of the path, and determined safe transverse and longitudinal diameters for the biopsy area. Our data are consistent with previously published imaging16 and anatomic information46 about the transverse and vertical diameters of the atlas. The angles, range and distances we ascertained can be used to avoid damage to important adjacent organs during the biopsy procedure49. These data also help in locating the appropriate puncture area and maximizing the chance of obtaining a suitable biopsy. However, these variables can vary with differences in patients’ conditions, the nature of the tumor, involvement of nasopharyngeal tissue by tumor and status of the mucosa of the inferior nasal meatus. Biopsy track angles, range of target tissue on coronal section, appropriate biopsy track and effective and safe distances are important indexes and should be measured carefully in each patient preoperatively and compared with the data provided by our research.

Because the atlas is located deep in the CVJ and has important surrounding structures, biopsies must be obtained carefully. Operators need preoperative accurate measurements from imaging data to identify a definite and effective path and angle for the approach. Endoscopy, double X‐ray‐guidance, classic coaxial technology, manual palpation, and pathological examination of the specimen are essential. Either a cutting or grabbing sample or combination of these should be obtained, avoiding sampling by cut‐through, suction or scratching techniques.

A X‐ray‐assisted transnasal endoscopic approach is safe and effective for biopsying tumors in the anterior tubercle and arch of the atlas and has few complications. We have provided data about measurements on CT images from the inferior nasal meatus to provides a theoretical basis for anterior biopsy of the atlas.

Disclosure: No funds were received in support of this work.

Zhen‐fen Li and Xian‐hao Shao contributed equally to this work and are joint first co‐authors.

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