SPINE Volume 40, Number 1, pp E43-E48 ©2014, Lippincott Williams & Wilkins
DEFORMITY
Changes of the Abdomen in Patients With Ankylosing Spondylitis Kyphosis Chao Liu, MD, Kai Song, MD, Yonggang Zhang, MD, Jun Fu, MD, Guoquan Zheng, MD, Xiangyu Tang, MD, Lu Zhao, MD, Xuesong Zhang, MD, and Yan Wang, MD
Study Design. A retrospective clinical study. Objective. To investigate changes of the abdomen in patients with ankylosing spondylitis kyphosis. Summary of Background Data. Since 1945, many authors had reported the good clinical and radiographical outcomes and higher patient satisfaction rates of spinal osteotomy techniques. However, to our knowledge, whether the visceral and diaphragmatic compression that results from the inferior edge of the thoracic cage is relieved by the surgery has not yet been reported. Materials and Methods. From July 2010 to July 2013, 26 patients (24 males, and 2 females) with severe ankylosing spondylitis kyphosis, who underwent pedicle subtraction osteotomy in the Department of Orthopaedics at Chinese People’s Liberation Army General Hospital were studied. Preoperative and postoperative computed tomographic scan, 3-dimensional reconstruction, and preoperative pulmonary function test were performed. Via those tests, the minimum distance on the median sagittal plane of the abdomen (MD), the acreage of the abdominal median sagittal plane (AMSPA), the diaphragm angle on median sagittal plane can be gained. A paired sample t test was performed to determine the differences between the preoperative and postoperative AMSPA and MD and diaphragm angle on median sagittal plane, respectively. Postoperative MD/preoperative MD and postoperative AMSPA/ preoperative AMSPA and global kyphosis were also analyzed by performing independent sample t test for the 2 groups. Results. The diaphragm angle on median sagittal plane has changed significantly in all the patients. There was significant change of both MD and AMSPA in patients whose abdominal wall
From the Department of Orthopaedics, Chinese People’s Liberation Army General Hospital (301 Hospital), Beijing, PR China. Acknowledgment date: November 27, 2013. First revision date: April 6, 2014. Second revision date: July 20, 2014. Acceptance date: October 13, 2014. The manuscript submitted does not contain information about medical device(s)/drug(s). No funds were received in support of this work. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to Yonggang Zhang, MD, Department of Orthopaedics, Chinese People’s Liberation Army General Hospital (301 Hospital), 28 Fuxing Rd, 100853, Beijing, PR China; E-mail: [email protected] DOI: 10.1097/BRS.0000000000000662 Spine
was folded into abdomen, whereas neither MD nor AMSPA in patients without the factor. Conclusion. To a certain degree, the diaphragmatic compression and the visceral compression could be compensated for by turning to flattening or even developing into kyphosis of the lumbar lordosis before surgery, which could be corrected by a spinal osteotomy. Sagittal rotation of diaphragm in ankylosing spondylitis kyphosis could also be improved by a spinal osteotomy. Key words: abdomen, kyphosis, ankylosing spondylitis, diaphragm. Level of Evidence: 4 Spine 2015;40:E43–E48
A
nkylosing spondylitis (AS) is a common inflammatory rheumatic disease predominantly affecting the sacroiliac joints and spine that causes a characteristic spinal deformity such as flattening of the normal lumbar lordosis, which can lead to structural and functional impairments and a decrease in quality of life.1 In severe cases, the spinal kyphotic deformity results in muscle fatigue and inability to look straight ahead as well as intra-abdominal complications and impaired respiratory function because of visceral compression.2–5 In 1945, Smith-Petersen et al6 first reported the anterior opening wedge osteotomy technique. Many authors had reported good clinical and radiographical outcomes and higher patient satisfaction rates of different osteotomy techniques for the AS kyphotic deformity.6–18 At a follow-up visit, most of the patients restored sagittal balance and improved the living ability. Diaphragmatic respiration and visceral compression were also improved.12–18 However, to our knowledge, whether the visceral and diaphragmatic compression that results from the inferior edge of the thoracic cage is relieved by the surgery have not yet been reported. By studying the patients with AS kyphosis, it was found that rotation of diaphragm occurred on the sagittal plane. Hence, this study aimed to investigate some abdominal changes in patients with AS kyphosis.
MATERIALS AND METHODS From July 2010 to July 2013, 26 patients (24 males, and 2 females) in our department were eligibly involved in this study. The average age was 36.57 years (range, 26–52 yr). www.spinejournal.com
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DEFORMITY All patients with AS kyphosis underwent a spinal pedicle subtraction osteotomy with good radiographical and clinical outcomes. Preoperative 3-dimensional computed tomographic (3DCT) scans of the full spine were routinely performed on the patients with AS before surgery to observe their vertebral structure and vertebral pedicle, ensuring the accuracy of pedicle screw placement. However, for the patients who had neurological complications postoperatively or had the radiographs that showed a suspected screw malposition, it was necessary to perform postoperative 3D-CT scans of the spinal segment that had pedicle screws. The postoperative 3D-CT scans were carried out after operation. All pre- and postoperative 3D-CT examinations were performed using a sliding gantry 40-slice CT scanner (SAMATOM Sensation Open; Siemens Medical Solutions, Forchheim, Germany). A 1.5-mm scan slice was used to guarantee the accuracy and decrease the spatial resolution. The voltage of the x-ray tube was adjusted to be 80 kV to reduce the radiation. All patients underwent a preoperative pulmonary function test to assess their preoperative physical condition.
Computed Tomographic Measurements For this study, the minimum distance between the xiphoid process and the spine (Figures 1D and 2A, D) or that between the abdominal wall and the spine when the abdominal wall
Changes of the Abdomen in Patients With AS • Liu et al
was folded in abdomen (Figure 1A, line h–i) was obtained on the median sagittal plane of the abdomen (MD). The acreage of the abdominal median sagittal plane was also gained (AMSPA) (Figures 1C, F and 2C, F), which was used to quantify the change of abdominal volume, and the acreage subtended by the following 4 peripheries: (1) a beeline from the xiphoid process to the inferior edge of T12, (2) a beeline from the xiphoid process to the superior edge of the pubis, (3) a beeline between the superior edge of the pubis and the anterosuperior corner of the sacrum, and (4) the anterior edge of T12–S1. Those peripheries were considered because they were independent of the respiratory movement and the food intake. On median sagittal plane the diaphragm angle (DA) was measured (Figures 1B, E and 2B, E), and the DA was subtended by the following 2 lines: (1) the p line that is perpendicular to the a–b line between the xiphoid process and the anteroinferior edge of T12; (2) the e–f line between the midpoints of the following 2 lines : (1) the midpoint e of the a–b line between the xiphoid process and the anteroinferior edge of T12, and (2) the midpoint f of the c–d line between the superior edge of the pubis and the anterosuperior corner of the sacrum. The DA was used to quantify the diaphragmatic rotation. Furthermore, the angle was defined as positive if the plumb line of the beeline from the xiphoid process to inferior edge of T12 was in front of the beeline between the 2 midpoints; if not, the angle was negative. All the values were
Figure 1. A 52-year-old male patient with ankylosing spondylitis of the group with the abdominal wall folded into abdomen undergoing pedicle subtraction osteotomy at the level of L3. The preoperative and postoperative MDs were 6.15 cm (A) and 13.93 cm (D), respectively. The preoperative and postoperative DAs were −32° (B) and 0° (E), respectively. And the preoperative and postoperative AMSPAs were 201.01 cm2 (C) and 241.42 cm2 (F), respectively. MD indicates the minimum distance on the median sagittal plane of the abdomen; AMSPA, acreage of the abdominal median sagittal plane; DA, diaphragm angle on median sagittal plane.
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Changes of the Abdomen in Patients With AS • Liu et al
Figure 2. A 44-year-old female patient with ankylosing spondylitis of the group without the abdominal wall folded into abdomen undergoing pedicle subtraction osteotomy at the level of L1 and L3. The preoperative and postoperative MDs were 13.00 cm (A) and 11.89 cm (D), respectively. The preoperative and postoperative DAs were −19° (B) and 24° (E), respectively. And the preoperative and postoperative AMSPAs were 183.03 cm2 (C) and 193.10 cm2 (F), respectively. MD indicates the minimum distance on the median sagittal plane of the abdomen; AMSPA, acreage of the abdominal median sagittal plane; DA, diaphragm angle on median sagittal plane.
measured twice by 2 independent observers, and the average was calculated.
Radiological Parameters Before the operation, full-length spinal radiographs of the patients with AS standing in a neutral unsupported position, including the whole spine and pelvis, were derived. The global kyphosis (GK) was measured from the superior endplate of the maximal thoracic vertebra to the inferior endplate of the maximal lower end vertebra.
Statistical Analysis Data analyses were performed using SPSS version 16.0, for Windows. A paired sample t test was performed to determine the differences between the preoperative and postoperative MD, AMSPA, and DA. The patients were also divided into 2 groups according to whether the patient’s abdominal wall was folded into their abdomen (Figures 1A, 2A). A paired sample t test was also used to determine the differences between the 2 groups regarding the preoperative and postoperative MD and AMSPA. Furthermore, to eliminate any influence from the patient’s differing body sizes, the ratios of the postoperative MD to the preoperative MD and those of the postoperative AMSPA to preoperative AMSPA were also analyzed by independent sample t test of the 2 groups, respectively. In Spine
addition, GK was also analyzed by independent sample t test of the 2 groups. A P value less than 0.05 was considered to be significant in all analyses.
RESULTS Pre-and Postoperative MD, AMSPA, and DA for All Patients In our cohort, the preoperative and postoperative MD were 10.609 ± 3.674 cm and 12.79 ± 2.421 cm, respectively (df = 25, P = 0.001). AMSPA and DA were obtained in only 18 patients, because the pubis was not covered by CT scans in 8 patients. The preoperative and postoperative AMSPA were 172.106 ± 43.487 cm2 and 219.698 ± 30.449 cm2, respectively (df = 17, P = 0.001). The preoperative and postoperative DA were −25.333º ± 4.283º and 18.222º ± 2.409º, respectively (df = 17, P = 0.000) (Table 1).
Pre-and Postoperative MD and AMSPA in the 2 Groups In group 1 (Figure 1A, D), the abdominal wall was folded into the abdomen. The preoperative and postoperative MD were 6.985 ± 1.292 cm and 12.299 ± 2.188 cm, respectively (df = 9, P = 0.0001), and the preoperative and postoperative AMSPA were 140.528 ± 30.031 cm2 and 219.441 ± 27.687 cm2, respectively, (df = 7, P = 0.0001) (Table 2). In www.spinejournal.com
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Changes of the Abdomen in Patients With AS • Liu et al
TABLE 1. Pre- and Postoperative MD, AMSPA, and DA of All Patients Parameters MD
Preoperative
Postoperative
10.60 ± 3.674 cm
12.79 ± 2.421 cm
df
P
25
0.001
AMSPA
172.10 ± 43.487 cm
219.69 ± 30.449 cm
17
0.001
DA
−25.33° ± −18.169°
18.222° ± 10.219°
17
0.000
2
2
MD indicates the minimum distance on the median sagittal plane of the abdomen between the xiphoid process and the spine or between the abdominal wall and the spine when the abdominal wall was folded in abdomen preoperatively; AMSPA, acreage of the abdominal median sagittal plane; DA, the diaphragm angle on median sagittal plane.
group 2 (Figure 2A, D), the abdominal wall was not folded into the abdomen. The preoperative and postoperative MD were 12.205 ± 2.910 cm and 12.774 ± 2.437 cm, respectively (df = 15, P = 0.2670), and the preoperative and postoperative AMSPA were 197.369 ± 35.708 cm2 and 209.985 ± 38.754 cm2, respectively (df = 9, P = 0.4104) (Table 3).
Ratios of the Postoperative MD to Preoperative MD and Those of the Postoperative AMSPA to Preoperative AMSPA, and GK of the 2 Groups The ratio of the postoperative MD to the preoperative MD in group 1 and group 2 was 190.330 ± 46.217% and 108.313 ± 20.164%, respectively (df = 24, P = 0.0000). That of the postoperative AMSPA to preoperative AMSPA in group 1 and group 2 was 159.819 ± 27.237% and 113.211 ± 18.029%, respectively (df = 16, P = 0.0005). The GK in group 1 and group 2 was 75.360º ± 15.559º and 51.856º ± 21.424º, respectively (df = 24, P = 0.0062) (Table 4).
DISCUSSION Advanced patients with AS with a spinal kyphotic deformity experience muscle fatigue, activity-related pain due to continuous strain of the spinal muscles while standing, inability to look straight ahead, intra-abdominal complications and impaired respiratory function because of visceral compression that could be corrected by a spinal osteotomy. However, it has not been demonstrated whether the diaphragmatic and visceral compression resulted from the inferior edge of the thoracic cage would be relieved. We hypothesized that the diaphragm and viscera were not compressed by the inferior edge of the thoracic cage because of turning to flattening or even developing into kyphosis of the lumbar lordosis before surgery. Hence, this research would reveal some abdominal changes in AS kyphosis.
Abdominal changes occurring in all patients with AS kyphosis mainly included changes of abdominal shape and abdominal volume as well as location of the viscera. Changes in shape were easily observed. It was necessary to document the visceral compression resulted from the inferior edge of the thoracic cage because of abdominal shape and volume changes by some quantized indexes. By studying the patients with AS kyphotic deformity, it was found that the diaphragm rotation occurred on the sagittal plane, with necessity of being proved by some quantized indexes. MD, AMSPA, and DA were used to quantify viscera compression, abdominal volume changes, and diaphragmatic rotation, respectively. AMSPA was subtended by 4 peripheries: (1) a beeline from the xiphoid process to the inferior edge of T12, (2) a beeline from the xiphoid process to the superior edge of the pubis, (3) a beeline between the superior edge of the pubis and the anterosuperior corner of the sacrum, and (4) the anterior edge of T12–S1. We used these peripheries because they were independent of respiratory movement and the amounts of food intake. Although designing the DA, a beeline from the xiphoid process to the anteroinferior edge of T12 was adopted as the diaphragmatic plane on the sagittal plane. It was difficult to quantify the level of diaphragmatic rotation on the sagittal plane because the diaphragm was irregular on the frontal plane. According to the diaphragmatic anatomy, the beeline from the xiphoid process to the anteroinferior edge of T12 changed in line with the diaphragm on the sagittal plane. Thus, the beeline was adopted as the diaphragmatic plane on the sagittal plane. In this study, a statistical analysis (Table 1) showed that abdominal volume and compression significantly changed and that corrective surgery of spinal osteotomy could improve the abdominal conditions of patients with AS. Tables 2 to 4 revealed that there was significant change of
TABLE 2. Pre- and Postoperative MD, AMSPA in Group 1 Parameters MD
Preoperative
Postoperative
6.985 ± 1.292 cm
AMSPA
12.299 ± 2.188 cm
140.528 ± 30.031 cm
2
219.441 ± 27.687 cm
2
df
P
9
0.0001
7
0.0001
MD indicates the minimum distance on the median sagittal plane of the abdomen between the abdominal wall and the spine because of the abdominal wall was folded in abdomen; AMSPA, acreage of the abdominal median sagittal plane.
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TABLE 3. Pre- and Postoperative MD, AMSPA in Group 2 Parameters MD
Preoperative
Postoperative
12.205 ± 2.910 cm
AMSPA
12.774 ± 2.437 cm 209.985 ± 38.754 cm
197.36 ± 35.708 cm
2
2
df
P
15
0.2670
9
0.4104
MD indicates the minimum distance on the median sagittal plane of the abdomen between the xiphoid process and the spine; AMSPA, acreage of the abdominal median sagittal plane.
both MD and AMSPA in group 1, whereas neither MD nor AMSPA in group 2, with significant difference of GK between group 1 and group 2. Table 4 also demonstrated that the improvement in MD and AMSPA in group 1 was significant compared with that of group 2. An elevated intraabdominal pressure would affect respiratory mechanics, which may impede ventilation and require a greater pressure variation under normal conditions.19 Already in 1948, Duomarco and Rimini proposed that the abdomen could be considered as a fluid-filled container.19–21 In some pathological conditions, such as increase of abdominal contents or decrease of abdominal volume and increase of abdominal pressure, diaphragmatic expansion would be restricted and pulmonary function would be subsequently reduced, if the abdominal wall distention did not compensate for the increased abdominal pressure or if the abdominal wall could not distend because of the pathological conditions. For patients with AS, an AS kyphotic deformity was another example. Thus, patients with AS who had a spinal kyphotic deformity and fold of the anterior abdominal wall into the abdomen were more likely to experience visceral compression, which resulted in intra-abdominal complications and impaired respiratory function. Although the patients who did not have the factors mentioned in the previous text had mild or no visceral compression, because the turning to plane or even developing into kyphosis of lumbar lordosis could compensate for the compression to a certain degree. Moreover, the patients who had increased GK were more likely to experience visceral compression. The follow-up results were inconsistent with the findings mentioned in the previous text. Actually, most patients with these factors could ingest more food, and their body weight was heavier postoperatively. There was no obvious change in either food
intake or weight after surgery in most patients without the factors mentioned in the previous text. With advanced AS, chest expansion was limited, and ventilation became more dependent on the diaphragm. Respiration was compensated by the diaphragm, especially during hyperventilation,22–24 but there was no spinal kyphotic deformity in all patients with AS involved in those studies. The results of the preoperative and postoperative DA (Table 1) showed that diaphragmatic rotation did occur on the sagittal plane and the direction of diaphragmatic movement was dependent on the diaphragmatic sagittal rotation. Thus, the diaphragm pushed the viscera in the patients with AS kyphotic deformity more downward and backward during respiration compared with those without kyphotic deformity. To our knowledge, the posterior abdominal wall was not distended in contrast to the anterior abdominal wall. The posterior abdominal wall distention was not able to compensate for the increased abdominal pressure, especially during hyperventilation. Thus, the expansion of the diaphragm would be reduced, and then the pulmonary function was reduced in patients with AS kyphotic deformity. The change of the diaphragmatic movement may be an affecting factor of pulmonary dysfunction in AS kyphosis, which could be improved via restoration of DA by the spinal osteotomy. Further investigation was still required to confirm this hypothesis.
CONCLUSION To a certain degree, the diaphragmatic compression and the visceral compression could be compensated for by turning to flattening or even developing into kyphosis of the lumbar lordosis before surgery, which could be corrected by a spinal osteotomy. What’s more, sagittal rotation of diaphragm in AS kyphosis could also be improved by a spinal osteotomy.
TABLE 4. Postoperative MD/Preoperative MD and Postoperative AMSPA/Preoperative AMSPA and
the GK of the 2 Groups
Group 1
Group 2
df
P
MD%
190.330 ± 46.217%
108.313 ± 20.164%
24
0.0000
AMSPA%
159.819 ± 27.237%
113.211±18.029%
16
0.0005
75.360° ± 15.559°
51.856° ± 21.424°
24
0.0062
Parameters
GK
MD indicates the minimum distance on the median sagittal plane of the abdomen; MD%, ratio of postoperative MD/preoperative MD; AMSPA, acreage of the abdominal median sagittal plane; GK, global kyphosis; AMSPA%, ratio of postoperative AMSPA/postoperative AMSPA.
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DEFORMITY ➢ Key Points To a certain degree, the diaphragmatic compression and the visceral compression could be compensated for by turning to flattening or even developing into kyphosis of the lumbar lordosis before surgery. The diaphragmatic compression and the visceral compression could be corrected by the spinal osteotomy. The diaphragm did have sagittal rotation in AS kyphosis, and sagittal rotation could also be improved by a spinal osteotomy.
Acknowledgments Chao Liu is the first author and Kai Song is the cofirst author of the article.
References
1. Braun J, Sieper J. Ankylosing spondylitis. Lancet 2007;369:1379– 90. 2. Kim KT, Suk KS, Cho YJ, et al. Clinical outcome results of pedicle subtraction osteotomy in ankylosing spondylitis with kyphotic deformity. Spine 2002;27:612–8. 3. Suk KS, Kim KT, Lee SH, et al. Significance of chin-brow vertical angle in correction of kyphotic deformity of ankylosing spondylitis patients. Spine 2003;28:2001–5. 4. Ragnarsdottir M, Geirsson AJ, Gudbjornsson B. Rib cage motion in ankylosing spondylitis patients: a pilot study. Spine J 2008;8:505–9. 5. Chang KW. Quality control of reconstructed sagittal balance for sagittal imbalance. Spine 2011;36:E186–97. 6. Smith-Petersen MN, Larson CB, Aufranc OE. Osteotomy of the spine for correction of flexion deformity in rheumatoid arthritis. J Bone Joint Surg 1945;27:1–11. 7. Wilson MJ, Turkell JH. Multiple spinal wedge osteotomy. Its use in a case of Marie Strumpell spondylitis. Am J Surg 1949;77: 777–82. 8. Scudese VA, Calabro JJ. Vertebral wedge osteotomy correction of rheumatoid (ankylosing) spondylitis. JAMA 1963;186:627–31.
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Changes of the Abdomen in Patients With AS • Liu et al
9. Ziwjan JL. Die behandlung der Flexionsdeformitäten der Wirbelsäule bei der Bechterewschen Erkrankung. Beitr Orthop Traumatol 1982;29:195–9. 10. Thomasen E. Vertebral osteotomy for correction of kyphosis in ankylosing spondylitis. Clin Orthop 1985;194:142–52. 11. Van Royen BJ, De Gast A. Lumbar osteotomy for correction of thoracolumbar kyphotic deformity in ankylosing spondylitis. A structured review of three methods of treatment. Ann Rheum Dis 1999;58:399–406. 12. Chen IH, Chien JT, Yu TC. Transpedicular wedge osteotomy for correction of thoracolumbar kyphosis in ankylosing spondylitis: experience with 78 patients. Spine 2001;26:E354–60. 13. Chang KW, Chen YY, Lin CC, et al. Closing wedge osteotomy versus opening wedge osteotomy in ankylosing spondylitis with thoracolumbar kyphotic deformity. Spine 2005;30:1584–93. 14. Bridwell KH. Decision making regarding Smith-Petersen vs. pedicle subtraction osteotomy vs. vertebral column resection for spinal deformity. Spine 2006;31:S171–8. 15. Wang Y, Zhang Y, Mao K, et al. Transpedicular bivertebrae wedge osteotomy and discetomy in lumbar spine for severe ankylosing spondylitis. J Spinal Disord Tech 2010;23:186–91. 16. Kiaer T, Gehchen M. Transpedicular closed wedge osteotomy in ankylosing spondylitis: results of surgical treatment and prospective outcome analysis [J]. Eur Spine J 2010;19:57–64. 17. Wang Y, Zhang YG, Zheng GQ, et al. Vertebral column decancellation for the management of rigid scoliosis: the effectiveness and safety analysis. Zhonghua Wai Ke Za Zhi 2010;48:1701–4. 18. Song RX, Zhang YG, Wang Y. Clinical efficacies of skipping two-level transpedicular wedge osteotomy for correction of severe kyphosis in ankylosing spondylitis. Zhonghua Yi Xue Za Zhi 2012;92:1476–80. 19. Hedenstierna G, Larsson A. Influence of abdominal pressure on respiratory and abdominal organ function. Curr Opin Crit Care 2012;18:80–5. 20. Duomarco JL, Rimini R. La Presion Intraabdominal en el Hombre. Buenos Aires, Argentina: El Ateneo; 1947:1–159. 21. Hedenstierna G, Strandberg A, Brismar B, et al. Functional residual capacity, thoracoabdominal dimensions and central blood-volume during general anesthesia with muscle paralysis and mechanical ventilation. Anesthesiology 1985;62:247–54. 22. Grimby G, Fugl-Meyer AR, Bloomstand A. Partitioning of the contribution of rib cage and abdomen to ventilation in ankylosing spondylitis. Thorax 1974;29:179–84. 23. Hauge BN. Diaphragmatic movement and spirometric volume in patients with ankylosing spondylitis. Scand J Respir Dis 1973;54:38–44. 24. Ünlü E, Pamuk ÖN, Erer B, et al. Diaphragmatic movements in ankylosing spondylitis patients and their association with clinical factors: an ultrasonographic study. Rheumatol Int 2012;32:435–7.
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DEFORMITY
Changes of the Abdomen in Patients With Ankylosing Spondylitis Kyphosis Chao Liu, MD, Kai Song, MD, Yonggang Zhang, MD, Jun Fu, MD, Guoquan Zheng, MD, Xiangyu Tang, MD, Lu Zhao, MD, Xuesong Zhang, MD, and Yan Wang, MD
Study Design. A retrospective clinical study. Objective. To investigate changes of the abdomen in patients with ankylosing spondylitis kyphosis. Summary of Background Data. Since 1945, many authors had reported the good clinical and radiographical outcomes and higher patient satisfaction rates of spinal osteotomy techniques. However, to our knowledge, whether the visceral and diaphragmatic compression that results from the inferior edge of the thoracic cage is relieved by the surgery has not yet been reported. Materials and Methods. From July 2010 to July 2013, 26 patients (24 males, and 2 females) with severe ankylosing spondylitis kyphosis, who underwent pedicle subtraction osteotomy in the Department of Orthopaedics at Chinese People’s Liberation Army General Hospital were studied. Preoperative and postoperative computed tomographic scan, 3-dimensional reconstruction, and preoperative pulmonary function test were performed. Via those tests, the minimum distance on the median sagittal plane of the abdomen (MD), the acreage of the abdominal median sagittal plane (AMSPA), the diaphragm angle on median sagittal plane can be gained. A paired sample t test was performed to determine the differences between the preoperative and postoperative AMSPA and MD and diaphragm angle on median sagittal plane, respectively. Postoperative MD/preoperative MD and postoperative AMSPA/ preoperative AMSPA and global kyphosis were also analyzed by performing independent sample t test for the 2 groups. Results. The diaphragm angle on median sagittal plane has changed significantly in all the patients. There was significant change of both MD and AMSPA in patients whose abdominal wall
From the Department of Orthopaedics, Chinese People’s Liberation Army General Hospital (301 Hospital), Beijing, PR China. Acknowledgment date: November 27, 2013. First revision date: April 6, 2014. Second revision date: July 20, 2014. Acceptance date: October 13, 2014. The manuscript submitted does not contain information about medical device(s)/drug(s). No funds were received in support of this work. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to Yonggang Zhang, MD, Department of Orthopaedics, Chinese People’s Liberation Army General Hospital (301 Hospital), 28 Fuxing Rd, 100853, Beijing, PR China; E-mail: [email protected] DOI: 10.1097/BRS.0000000000000662 Spine
was folded into abdomen, whereas neither MD nor AMSPA in patients without the factor. Conclusion. To a certain degree, the diaphragmatic compression and the visceral compression could be compensated for by turning to flattening or even developing into kyphosis of the lumbar lordosis before surgery, which could be corrected by a spinal osteotomy. Sagittal rotation of diaphragm in ankylosing spondylitis kyphosis could also be improved by a spinal osteotomy. Key words: abdomen, kyphosis, ankylosing spondylitis, diaphragm. Level of Evidence: 4 Spine 2015;40:E43–E48
A
nkylosing spondylitis (AS) is a common inflammatory rheumatic disease predominantly affecting the sacroiliac joints and spine that causes a characteristic spinal deformity such as flattening of the normal lumbar lordosis, which can lead to structural and functional impairments and a decrease in quality of life.1 In severe cases, the spinal kyphotic deformity results in muscle fatigue and inability to look straight ahead as well as intra-abdominal complications and impaired respiratory function because of visceral compression.2–5 In 1945, Smith-Petersen et al6 first reported the anterior opening wedge osteotomy technique. Many authors had reported good clinical and radiographical outcomes and higher patient satisfaction rates of different osteotomy techniques for the AS kyphotic deformity.6–18 At a follow-up visit, most of the patients restored sagittal balance and improved the living ability. Diaphragmatic respiration and visceral compression were also improved.12–18 However, to our knowledge, whether the visceral and diaphragmatic compression that results from the inferior edge of the thoracic cage is relieved by the surgery have not yet been reported. By studying the patients with AS kyphosis, it was found that rotation of diaphragm occurred on the sagittal plane. Hence, this study aimed to investigate some abdominal changes in patients with AS kyphosis.
MATERIALS AND METHODS From July 2010 to July 2013, 26 patients (24 males, and 2 females) in our department were eligibly involved in this study. The average age was 36.57 years (range, 26–52 yr). www.spinejournal.com
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DEFORMITY All patients with AS kyphosis underwent a spinal pedicle subtraction osteotomy with good radiographical and clinical outcomes. Preoperative 3-dimensional computed tomographic (3DCT) scans of the full spine were routinely performed on the patients with AS before surgery to observe their vertebral structure and vertebral pedicle, ensuring the accuracy of pedicle screw placement. However, for the patients who had neurological complications postoperatively or had the radiographs that showed a suspected screw malposition, it was necessary to perform postoperative 3D-CT scans of the spinal segment that had pedicle screws. The postoperative 3D-CT scans were carried out after operation. All pre- and postoperative 3D-CT examinations were performed using a sliding gantry 40-slice CT scanner (SAMATOM Sensation Open; Siemens Medical Solutions, Forchheim, Germany). A 1.5-mm scan slice was used to guarantee the accuracy and decrease the spatial resolution. The voltage of the x-ray tube was adjusted to be 80 kV to reduce the radiation. All patients underwent a preoperative pulmonary function test to assess their preoperative physical condition.
Computed Tomographic Measurements For this study, the minimum distance between the xiphoid process and the spine (Figures 1D and 2A, D) or that between the abdominal wall and the spine when the abdominal wall
Changes of the Abdomen in Patients With AS • Liu et al
was folded in abdomen (Figure 1A, line h–i) was obtained on the median sagittal plane of the abdomen (MD). The acreage of the abdominal median sagittal plane was also gained (AMSPA) (Figures 1C, F and 2C, F), which was used to quantify the change of abdominal volume, and the acreage subtended by the following 4 peripheries: (1) a beeline from the xiphoid process to the inferior edge of T12, (2) a beeline from the xiphoid process to the superior edge of the pubis, (3) a beeline between the superior edge of the pubis and the anterosuperior corner of the sacrum, and (4) the anterior edge of T12–S1. Those peripheries were considered because they were independent of the respiratory movement and the food intake. On median sagittal plane the diaphragm angle (DA) was measured (Figures 1B, E and 2B, E), and the DA was subtended by the following 2 lines: (1) the p line that is perpendicular to the a–b line between the xiphoid process and the anteroinferior edge of T12; (2) the e–f line between the midpoints of the following 2 lines : (1) the midpoint e of the a–b line between the xiphoid process and the anteroinferior edge of T12, and (2) the midpoint f of the c–d line between the superior edge of the pubis and the anterosuperior corner of the sacrum. The DA was used to quantify the diaphragmatic rotation. Furthermore, the angle was defined as positive if the plumb line of the beeline from the xiphoid process to inferior edge of T12 was in front of the beeline between the 2 midpoints; if not, the angle was negative. All the values were
Figure 1. A 52-year-old male patient with ankylosing spondylitis of the group with the abdominal wall folded into abdomen undergoing pedicle subtraction osteotomy at the level of L3. The preoperative and postoperative MDs were 6.15 cm (A) and 13.93 cm (D), respectively. The preoperative and postoperative DAs were −32° (B) and 0° (E), respectively. And the preoperative and postoperative AMSPAs were 201.01 cm2 (C) and 241.42 cm2 (F), respectively. MD indicates the minimum distance on the median sagittal plane of the abdomen; AMSPA, acreage of the abdominal median sagittal plane; DA, diaphragm angle on median sagittal plane.
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Figure 2. A 44-year-old female patient with ankylosing spondylitis of the group without the abdominal wall folded into abdomen undergoing pedicle subtraction osteotomy at the level of L1 and L3. The preoperative and postoperative MDs were 13.00 cm (A) and 11.89 cm (D), respectively. The preoperative and postoperative DAs were −19° (B) and 24° (E), respectively. And the preoperative and postoperative AMSPAs were 183.03 cm2 (C) and 193.10 cm2 (F), respectively. MD indicates the minimum distance on the median sagittal plane of the abdomen; AMSPA, acreage of the abdominal median sagittal plane; DA, diaphragm angle on median sagittal plane.
measured twice by 2 independent observers, and the average was calculated.
Radiological Parameters Before the operation, full-length spinal radiographs of the patients with AS standing in a neutral unsupported position, including the whole spine and pelvis, were derived. The global kyphosis (GK) was measured from the superior endplate of the maximal thoracic vertebra to the inferior endplate of the maximal lower end vertebra.
Statistical Analysis Data analyses were performed using SPSS version 16.0, for Windows. A paired sample t test was performed to determine the differences between the preoperative and postoperative MD, AMSPA, and DA. The patients were also divided into 2 groups according to whether the patient’s abdominal wall was folded into their abdomen (Figures 1A, 2A). A paired sample t test was also used to determine the differences between the 2 groups regarding the preoperative and postoperative MD and AMSPA. Furthermore, to eliminate any influence from the patient’s differing body sizes, the ratios of the postoperative MD to the preoperative MD and those of the postoperative AMSPA to preoperative AMSPA were also analyzed by independent sample t test of the 2 groups, respectively. In Spine
addition, GK was also analyzed by independent sample t test of the 2 groups. A P value less than 0.05 was considered to be significant in all analyses.
RESULTS Pre-and Postoperative MD, AMSPA, and DA for All Patients In our cohort, the preoperative and postoperative MD were 10.609 ± 3.674 cm and 12.79 ± 2.421 cm, respectively (df = 25, P = 0.001). AMSPA and DA were obtained in only 18 patients, because the pubis was not covered by CT scans in 8 patients. The preoperative and postoperative AMSPA were 172.106 ± 43.487 cm2 and 219.698 ± 30.449 cm2, respectively (df = 17, P = 0.001). The preoperative and postoperative DA were −25.333º ± 4.283º and 18.222º ± 2.409º, respectively (df = 17, P = 0.000) (Table 1).
Pre-and Postoperative MD and AMSPA in the 2 Groups In group 1 (Figure 1A, D), the abdominal wall was folded into the abdomen. The preoperative and postoperative MD were 6.985 ± 1.292 cm and 12.299 ± 2.188 cm, respectively (df = 9, P = 0.0001), and the preoperative and postoperative AMSPA were 140.528 ± 30.031 cm2 and 219.441 ± 27.687 cm2, respectively, (df = 7, P = 0.0001) (Table 2). In www.spinejournal.com
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TABLE 1. Pre- and Postoperative MD, AMSPA, and DA of All Patients Parameters MD
Preoperative
Postoperative
10.60 ± 3.674 cm
12.79 ± 2.421 cm
df
P
25
0.001
AMSPA
172.10 ± 43.487 cm
219.69 ± 30.449 cm
17
0.001
DA
−25.33° ± −18.169°
18.222° ± 10.219°
17
0.000
2
2
MD indicates the minimum distance on the median sagittal plane of the abdomen between the xiphoid process and the spine or between the abdominal wall and the spine when the abdominal wall was folded in abdomen preoperatively; AMSPA, acreage of the abdominal median sagittal plane; DA, the diaphragm angle on median sagittal plane.
group 2 (Figure 2A, D), the abdominal wall was not folded into the abdomen. The preoperative and postoperative MD were 12.205 ± 2.910 cm and 12.774 ± 2.437 cm, respectively (df = 15, P = 0.2670), and the preoperative and postoperative AMSPA were 197.369 ± 35.708 cm2 and 209.985 ± 38.754 cm2, respectively (df = 9, P = 0.4104) (Table 3).
Ratios of the Postoperative MD to Preoperative MD and Those of the Postoperative AMSPA to Preoperative AMSPA, and GK of the 2 Groups The ratio of the postoperative MD to the preoperative MD in group 1 and group 2 was 190.330 ± 46.217% and 108.313 ± 20.164%, respectively (df = 24, P = 0.0000). That of the postoperative AMSPA to preoperative AMSPA in group 1 and group 2 was 159.819 ± 27.237% and 113.211 ± 18.029%, respectively (df = 16, P = 0.0005). The GK in group 1 and group 2 was 75.360º ± 15.559º and 51.856º ± 21.424º, respectively (df = 24, P = 0.0062) (Table 4).
DISCUSSION Advanced patients with AS with a spinal kyphotic deformity experience muscle fatigue, activity-related pain due to continuous strain of the spinal muscles while standing, inability to look straight ahead, intra-abdominal complications and impaired respiratory function because of visceral compression that could be corrected by a spinal osteotomy. However, it has not been demonstrated whether the diaphragmatic and visceral compression resulted from the inferior edge of the thoracic cage would be relieved. We hypothesized that the diaphragm and viscera were not compressed by the inferior edge of the thoracic cage because of turning to flattening or even developing into kyphosis of the lumbar lordosis before surgery. Hence, this research would reveal some abdominal changes in AS kyphosis.
Abdominal changes occurring in all patients with AS kyphosis mainly included changes of abdominal shape and abdominal volume as well as location of the viscera. Changes in shape were easily observed. It was necessary to document the visceral compression resulted from the inferior edge of the thoracic cage because of abdominal shape and volume changes by some quantized indexes. By studying the patients with AS kyphotic deformity, it was found that the diaphragm rotation occurred on the sagittal plane, with necessity of being proved by some quantized indexes. MD, AMSPA, and DA were used to quantify viscera compression, abdominal volume changes, and diaphragmatic rotation, respectively. AMSPA was subtended by 4 peripheries: (1) a beeline from the xiphoid process to the inferior edge of T12, (2) a beeline from the xiphoid process to the superior edge of the pubis, (3) a beeline between the superior edge of the pubis and the anterosuperior corner of the sacrum, and (4) the anterior edge of T12–S1. We used these peripheries because they were independent of respiratory movement and the amounts of food intake. Although designing the DA, a beeline from the xiphoid process to the anteroinferior edge of T12 was adopted as the diaphragmatic plane on the sagittal plane. It was difficult to quantify the level of diaphragmatic rotation on the sagittal plane because the diaphragm was irregular on the frontal plane. According to the diaphragmatic anatomy, the beeline from the xiphoid process to the anteroinferior edge of T12 changed in line with the diaphragm on the sagittal plane. Thus, the beeline was adopted as the diaphragmatic plane on the sagittal plane. In this study, a statistical analysis (Table 1) showed that abdominal volume and compression significantly changed and that corrective surgery of spinal osteotomy could improve the abdominal conditions of patients with AS. Tables 2 to 4 revealed that there was significant change of
TABLE 2. Pre- and Postoperative MD, AMSPA in Group 1 Parameters MD
Preoperative
Postoperative
6.985 ± 1.292 cm
AMSPA
12.299 ± 2.188 cm
140.528 ± 30.031 cm
2
219.441 ± 27.687 cm
2
df
P
9
0.0001
7
0.0001
MD indicates the minimum distance on the median sagittal plane of the abdomen between the abdominal wall and the spine because of the abdominal wall was folded in abdomen; AMSPA, acreage of the abdominal median sagittal plane.
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TABLE 3. Pre- and Postoperative MD, AMSPA in Group 2 Parameters MD
Preoperative
Postoperative
12.205 ± 2.910 cm
AMSPA
12.774 ± 2.437 cm 209.985 ± 38.754 cm
197.36 ± 35.708 cm
2
2
df
P
15
0.2670
9
0.4104
MD indicates the minimum distance on the median sagittal plane of the abdomen between the xiphoid process and the spine; AMSPA, acreage of the abdominal median sagittal plane.
both MD and AMSPA in group 1, whereas neither MD nor AMSPA in group 2, with significant difference of GK between group 1 and group 2. Table 4 also demonstrated that the improvement in MD and AMSPA in group 1 was significant compared with that of group 2. An elevated intraabdominal pressure would affect respiratory mechanics, which may impede ventilation and require a greater pressure variation under normal conditions.19 Already in 1948, Duomarco and Rimini proposed that the abdomen could be considered as a fluid-filled container.19–21 In some pathological conditions, such as increase of abdominal contents or decrease of abdominal volume and increase of abdominal pressure, diaphragmatic expansion would be restricted and pulmonary function would be subsequently reduced, if the abdominal wall distention did not compensate for the increased abdominal pressure or if the abdominal wall could not distend because of the pathological conditions. For patients with AS, an AS kyphotic deformity was another example. Thus, patients with AS who had a spinal kyphotic deformity and fold of the anterior abdominal wall into the abdomen were more likely to experience visceral compression, which resulted in intra-abdominal complications and impaired respiratory function. Although the patients who did not have the factors mentioned in the previous text had mild or no visceral compression, because the turning to plane or even developing into kyphosis of lumbar lordosis could compensate for the compression to a certain degree. Moreover, the patients who had increased GK were more likely to experience visceral compression. The follow-up results were inconsistent with the findings mentioned in the previous text. Actually, most patients with these factors could ingest more food, and their body weight was heavier postoperatively. There was no obvious change in either food
intake or weight after surgery in most patients without the factors mentioned in the previous text. With advanced AS, chest expansion was limited, and ventilation became more dependent on the diaphragm. Respiration was compensated by the diaphragm, especially during hyperventilation,22–24 but there was no spinal kyphotic deformity in all patients with AS involved in those studies. The results of the preoperative and postoperative DA (Table 1) showed that diaphragmatic rotation did occur on the sagittal plane and the direction of diaphragmatic movement was dependent on the diaphragmatic sagittal rotation. Thus, the diaphragm pushed the viscera in the patients with AS kyphotic deformity more downward and backward during respiration compared with those without kyphotic deformity. To our knowledge, the posterior abdominal wall was not distended in contrast to the anterior abdominal wall. The posterior abdominal wall distention was not able to compensate for the increased abdominal pressure, especially during hyperventilation. Thus, the expansion of the diaphragm would be reduced, and then the pulmonary function was reduced in patients with AS kyphotic deformity. The change of the diaphragmatic movement may be an affecting factor of pulmonary dysfunction in AS kyphosis, which could be improved via restoration of DA by the spinal osteotomy. Further investigation was still required to confirm this hypothesis.
CONCLUSION To a certain degree, the diaphragmatic compression and the visceral compression could be compensated for by turning to flattening or even developing into kyphosis of the lumbar lordosis before surgery, which could be corrected by a spinal osteotomy. What’s more, sagittal rotation of diaphragm in AS kyphosis could also be improved by a spinal osteotomy.
TABLE 4. Postoperative MD/Preoperative MD and Postoperative AMSPA/Preoperative AMSPA and
the GK of the 2 Groups
Group 1
Group 2
df
P
MD%
190.330 ± 46.217%
108.313 ± 20.164%
24
0.0000
AMSPA%
159.819 ± 27.237%
113.211±18.029%
16
0.0005
75.360° ± 15.559°
51.856° ± 21.424°
24
0.0062
Parameters
GK
MD indicates the minimum distance on the median sagittal plane of the abdomen; MD%, ratio of postoperative MD/preoperative MD; AMSPA, acreage of the abdominal median sagittal plane; GK, global kyphosis; AMSPA%, ratio of postoperative AMSPA/postoperative AMSPA.
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DEFORMITY ➢ Key Points To a certain degree, the diaphragmatic compression and the visceral compression could be compensated for by turning to flattening or even developing into kyphosis of the lumbar lordosis before surgery. The diaphragmatic compression and the visceral compression could be corrected by the spinal osteotomy. The diaphragm did have sagittal rotation in AS kyphosis, and sagittal rotation could also be improved by a spinal osteotomy.
Acknowledgments Chao Liu is the first author and Kai Song is the cofirst author of the article.
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