Laminoplasty Improves Respiratory Function in Elderly Patients With Cervical Spondylotic Myelopathy

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1 Neurol Med Chir (Tokyo) 41, , 2001 Laminoplasty Improves Respiratory Function in Elderly Patients With Cervical Spondylotic Myelopathy Kiyoyuki YANAKA*, **, ShozoNOGUCHI*, HiroyukiASAKAWA*, and Tadao NOSE** *Neurosurgery Division, Satte General Hospital, Satte, Saitama; **Department of Neurosurgery, Institute of Clinical Medicine, University of Tsukuba, Tsukuba, Ibaraki Abstract Respiratory insufficiency after acute cervical trauma is well documented, but the relationship between respiratory function and chronic lesions, such as cervical spondylosis, has received scant attention. This clinical study investigated the effect of cervical spondylosis on respiratory function in 12 patients over 65 years of age who underwent expansive laminoplasty. Functional and neurological status were assessed using the Japanese Orthopaedic Association (JOA) scale and Neurosurgical Cervical Spine Scale (NCSS). To assess the effect of laminoplasty on respiratory function in patients with cervical spondylotic myelopathy, lung volumes including vital capacity, tidal volume (TV), inspiratory reserve volume, expiratory reserve volume, inspiratory capacity, and forced expiratory volume were measured by spirometer before surgery and 6 months after surgery. The arterial blood gas values were also measured before and after surgery. All patients showed functional improvement after surgery, and neurological examination 6 months after surgery revealed a significant improvement in both JOA scale and NCSS scores (p º 0.001). There were no significant differences in most lung volumes, but TV (p = 0.039) at 6 months after surgery showed a significant increase compared to before surgery. PCO 2 also showed a significant reduction after surgery (p = 0.047). This limited study revealed that laminoplasty improved respiratory function in patients over 65 years of age with cervical spondylotic myelopathy. Lung volume measurement may be one method to estimate spinal cord function after a surgical procedure. Key words: cervical spondylosis, decompression, laminoplasty, myelopathy, respiration Introduction The ``respiratory center'' consists of several groups of neurons located bilaterally in the brain stem. 13) Respiratory dysfunction may occur as a result of lesions in the upper cervical spinal cord disturbing the descending pathways subserving automatic and volitional ventilatory control. 2) Acute traumatic lesions of the spinal cord, particularly at high cervical levels, are well known to affect respiratory control. 6) However, the effect of long-standing lesions such as cervical degenerative disease on respiratory function has received scant attention. This clinical study investigated the effect of chronic lesions of the cervical spine on respiratory function by examining the changes in respiratory function after laminoplasty. Received April 27, 2001; Accepted July 23, 2001 Materials and Methods Twelve patients, five men and seven women aged over 65 years (mean age 71.5 ± 6.3), with cervical spondylotic myelopathy underwent cervical laminoplasty at our hospital between April 1998 and September 1999 (Table 1). All patients had radiological and long-standing clinical signs of cervical spondylotic myelopathy. The neurological statuses at admission were preoperatively recorded according to the Neurosurgical Cervical Spine Scale (NCSS) 3) and Japanese Orthopaedic Association (JOA) scale. 9) Radiography, magnetic resonance imaging, and computed tomographic myelography were performed in all patients before surgery. None of the patients complained of respiratory insufficiency, but family members of two patients commented on irregular respiratory patterns during sleep, such as nocturnal panting. Prior to surgery, a physician examined the 488

2 Laminoplasty and Respiration 489 Table 1 Patient profiles Case No. Age/ Sex Extent of laminoplasty Preop. JOA scale Postop. Preop. NCSS Postop. 1 73/F C /F C /M C /F C /M C /F C /M C /F C /M C /M C /F C /F C Average JOA: Japan Orthopaedic aesociation, NCSS: Neurosurgical Cervical Spine Scale. Fig. 1 Diagram showing respiratory excursions during normal breathing and during maximal inspiration and maximal expiration. ERV: expiratory reserve volume, FRC: functional residual capacity, IC: inspiratory capacity, IRV: inspiratory reserve volume, RV: residual volume, TC: total lung capacity, TV: tidal volume, VC: vital capacity. respiratory functions by reviewing chest radiograph and lung capacity measurements. Quantitative evaluation of lung capacity subdivided the lung volume into a number of components, as follows (Fig. 1): tidal volume (TV), the volume exchanged in normal inspiration or expiration; inspiratory reservevolume(irv),thevolumethatcanstillbeinhaledattheendofanormalinspiration;expiratory reserve volume (ERV), the volume that can still be exhaled at the end of a normal expiration; residual volume (RV), the volume remaining in the lungs after maximal expiration; vital capacity (VC), the greatest volume that can be exhaled after maximal inspiration, the sum of TV, IRV, and ERV; inspiratory capacity (IC), the greatest volume that can be inhaled after normal expiration, the sum of TV and IRV; functional residual capacity (FRC), the volume remaining in the lung after normal expiration, the sum of ERV and RV; and total capacity, the volume in the lung after maximal inspiration, the sum of RV and VC. 13) A special instrument is required to measure FRC and RV, but other compartments are easily measured by the spirometer. A decrease in vital capacity can be taken as a sign of restrictive impairment. Obstructive impairment can easily be identified by measuring the volume expelled from the lungs by forced expiration in 1 second, forced expiratory volume (FEV 1 ). 13) Therefore, lung volumes including VC, TV, IRV, ERV, IC, and FEV were measured using a spirometer (AS-300; Minato Ika Co., Osaka), and the values of %VC (= measured value/expected value 100) and FEV 1 %(= FEV/FEV 1 100) calculated. Respiratory status can be classified into four groups, obstructive, restrictive, combined, or normal, by comparing the values of %VC and FEV 1 %. 13) The respiratory function test and neurological examination were performed 6 months after surgery again after obtaining informed consent from each patient. Blood gas analysis was also performed before and after surgery. All patients underwent expanding laminoplasty using the spinous process splitting technique as previously described. 7,14) In brief, the spinous processes were cut off for the roofing of the spinal canal. Midline drilling of the lamina was continued until the yellow ligament was exposed, and then bilateral gutters were formed. The resected spinous process was put between the two sprayed laminae and fixed by sutures. Facet resection and foraminotomy were not performed. The extent of cervical laminoplasty was determined according to preoperative radiological data. Allvalueswereexpressedasmean± SD. Statistical analysis of the values of VC, TV, IRV, IC, FEV 1 %, and %VC was performed using the paired t-test. A Wilcoxon signed rank test was carried out to comparetheneurologicaloutcomeestimatedbythejoa scale and NCSS. Differences were considered significant if p º Results Expanding laminoplasty was performed in five levels (C3 7) in seven patients and four levels (C4 7) in five patients. The mean values of the JOA scale were 6.83 ± 2.76 and ± 2.39, and the NCSS were 8.25 ± 1.14 and ± 0.75, before surgery

3 490 K. Yanaka et al. and at 6 months after surgery, respectively. Neurological examination at 6 months after surgery revealed significant improvements in both JOA scale andncssscores(pº 0.001). There were no major surgical complications. All chest radiographs showed no abnormalities and there were no abnormalities in the nasopharynx. Blood gas analysis also found no abnormalities, such as hypoxia or hypercapnia before surgery. The mean values of lung volumes before and at 6 months after surgery were: VC 2.25 ± 0.53 and 2.27 ± 0.55 l, TV 0.33 ± 0.06 and 0.40 ± 0.07 l, IRV 2.28 ± 0.99 and 1.88 ± 0.87 l, ERV 0.41 ± 0.16 and 0.36 ± 0.15 l, and IC 2.55 ± 1.14 and 2.29 ± 0.97 l, respectively (Fig. 2). There were no significant differences in VC, IRV, ERV, and IC between before and 6 months after surgery. However, TV showed a significant increase after surgery (p = 0.039). The mean calculated values of %VC and FEV 1 %before and 6 months after surgery were: %VC 91.2 ± 11.4% and 88.7 ± 12.2%, and FEV 1 % 87.4 ± 10.4% and 88.3 ± 7.8%, respectively. There were no significant differences in %VC and FEV 1 % between before and 6 months after surgery. The nocturnal irregular respiration pattern of two patients disappeared after surgery. Bloodgasanalysiswasperformedonallpatients before surgery, and seven patients underwent blood gas analysis at 6 months after surgery. The other six patients did not consent to repeated blood gas analysis. The mean values of PO 2 and PCO 2 before and 6 months after surgery were: PO ± 9.3 and 83.9 ± 8.8 mmhg, and PCO ± 2.9 and 42.1 ± 2.8 mmhg, respectively (Fig. 3). The PO 2 value tended to increase (p = 0.593), and there was a significant decrease in the PCO 2 value (p = 0.047). Discussion Fig. 2 Graph showing changes in the respiratory function before (open columns) and after (closed columns) surgery. There are no significant differences in vital capacity (VC), inspiratory reserve volume (IRV), expiratory reserve volume (ERV), and inspiratory capacity (IC) between before and after surgery. However, only tidal volume (TV) shows a significant increase (25%) after surgery (*p = 0.039). This clinical study clearly demonstrated the influence of decompressive laminoplasty on respiratory function in elderly patients with cervical spondylotic myelopathy. Significant increases in TV and decreases in PCO 2 value were observed after decompressive laminoplasty. Respiratory insufficiency may occur due to variouscausessuchasspinalcordtraumaandinfarction, 3,4,6,12) which are all acute lesions in the cervical spinal cord. This study clearly demonstrated the change of respiratory function in patients with chronic cervical degenerative disease after laminoplasty. Respiratory insufficiency can occur as a result of lesions in the cervical spinal cord disturbing the descending pathways. 2) Therefore, it is not surprising that decompression for long-standing Fig. 3 Graph showing changes in the arterial blood gas before (open columns) andafter(closed columns) surgery. There is an increasing tendency in the PO 2 value (p = 0.593), and there is a significant decrease in the PCO 2 value (*p = 0.047). spinal cord compression results in an alteration of respiratory function. Several measurements of lung volume, such as IC, VC, and TV, were investigated, but only TV showed a significant increase after surgery. The most anterior part of the lateral columns of the cervical spinal cord is critical for the maintenance of automatic

4 Laminoplasty and Respiration 491 respiratory activity in humans, 2) and damage during cervical cordotomy to the reticulospinal tracts can cause respiratory dysfunction. 1,8) Studies of patients undergoing high cervical cordotomies showed that the section of the cord in the region of the descending reticulospinal pathways selectively impaired spontaneous respiratory muscle activity. 10) High bilateral ventrolateral cordotomy also causes decreased tidal volume. 1,5) Respiratory insufficiency after cordotomy is caused by the interruption of descending respiratory pathways rather than damage to lower motor neurons. 1) Therefore, with depression of the reticulospinal tracts, decreased amplitude of inspiratory discharge would result in decreased TV. In addition, the initial impairment of respiratory function after cervical spinal cord damage is a fall in TV. 11) Thus, the effect of the chronic lesion of the cervical spine on respiratory function may be small and only TV shows a significant change. It is also possible that decompression improves respiratory muscle function, thus resulting in the improvement of respiratory function. The value of PCO 2 was also found to show a significant decrease. However, the mean value of PCO 2 reduced from 45.1 to 42.1 mmhg, and neither value was within the normal limits. Therefore, the clinical impact of PCO 2 reduction is unknown. Inadequate respiration has not been monitored in patients with cervical spondylotic myelopathy, because the patients may not have overt clinical evidence of pulmonary disease. In this study, family members of two patients noticed irregular respiration patterns during sleep, but the patients considered their respiration to be normal. Their irregular respiratory patterns disappeared after laminoplasty. Therefore, although the alteration of respiratory function after laminoplasty was minimal, respiratory insufficiency may be occult and difficult to recognize in patients with chronic cervical degenerative disease. We need to keep in mind the signs of respiratory insufficiency, despite the absence of clinical symptoms of pulmonary distress. Neurosurgeons have several grading and scoring systems for neurological function in degenerative cervical spine disease such as the NCSS 3) and JOA scale. 9) These scales consist of several evaluation factors of the motor, sensory, urinary system or performance status. The lateral corticospinal tract, lateral spinothalamic tract, and fasciculus gracilis and cuneatus are important in such functions. These descending spinal tracts run in the posterior two thirds of the spinal cord in the axial plane. Therefore, these grading scales can estimate the function of only the posterior two thirds of the spinal cord. The respiratory pathway descends ipsilaterally in the most anterior part of the spinal cord. 10) Therefore, lung volume measurement may be one method to estimate the function of the spinal cord. Although improvement of respiratory function after laminoplasty was small, this limited study demonstrates the effect of chronic lesions of the cervical spine on respiratory function. This study also suggests that lung volume measurement could be used to evaluate spinal cord function because lung volume measurement by spirometer is easy and universally accepted. This study is preliminary and other factors should be assessed by well-designed clinical trials in a large number of patients. However, the present result reminds us of the importance of routine clinical examinations based on anatomy and basic physiology. Acknowledgment The authors wish to thank Hideaki Shoda, M.D. of the Department of Internal Medicine at Satte General Hospital for the assessment of respiratory function of patients, and Stephen Spellman, B.A. of the Department of Neurosurgery at University of Minnesota (Minneapolis, Minn., U.S.A.) for his assistance in proofreading the article in English. References 1) Belmusto L, Brown E, Owens G: Clinical observations on respiratory and vasomotor disturbances are related to cervical cordotomies. J Neurosurg 20: , ) HowardRS,ThorpeJ,BarkerR,ReveszT,HirschN, Miller D, Williams AJ: Respiratory insufficiency due to high anterior cervical cord infarction. J Neurol Neurosurg Psychiatry 64: , ) Kadoya S: Grading and scoring system for neurological function in degenerative cervical spine disease. Neurosurgical Cervical Spine Scale. Neurol Med Chir (Tokyo) 32: 40 41, ) Kadoya S, Massopust LC Jr, Wolin LR, Taslits N, White RJ: Effect of experimental cervical spinal cord injury on respiratory function. J Neurosurg 41: , ) Krieger AJ, Rosomoff H: Sleep-induced apnea. Part 1: A respiratory and automatic dysfunction syndrome following bilateral percutaneous cervical cordotomy. JNeurosurg39: , ) Loveridge B, Sanii R, Dubo HI: Breathing pattern adjustments during the first year following cervical spinal cord injury. Paraplegia 30: , ) Morimoto T, Yamada T, Okumura Y, Kakizaki T, Kawaguchi S, Hiramatsu K, Sakaki T: Expanding laminoplasty for cervical myelopathy spinous process roofing technique. Acta Neurochir (Wien) 138: , 1996

5 492 K. Yanaka et al. 8) Mullan S, Hosobuchi Y: Respiratory hazards of high cervical percutaneous cordotomy. J Neurosurg 29: , ) Naderi S, Ozgen S, Pamir MN, Ozek MM, Erzen C: Cervical spondylotic myelopathy: Surgical results and factors affecting prognosis. Neurosurgery 43: 43 50, ) Nathan PW: The descending respiratory pathway in man. J Neurol Neurosurg Psychiatry 26: , ) Rosomoff HL, Krieger AJ, Kuperman AS: Effects of percutaneous cervical cordotomy on pulmonary function. J Neurosurg 31: , ) Short DJ, Stradling JR, Williams SJ: Prevalence of sleep apnea in patients over 40 years of age with spinal cord lesions. J Neurol Neurosurg Psychiatry 55: , ) Thews G: Pulmonary respiration, in Schmidt RF, Thews G (eds): Human Physiology, ed 2. Berlin, Springer-Verlag, 1989, pp ) Yanaka K, Noguchi S, Asakawa H, Sakaguchi R, Yamamuro K, Syoda H, Yoshikawa H, Hyodo A, Nose T: [Expanding laminoplasty for cervical spondylotic myelopathy]. Saitamaken Igakukai Zasshi 34: , 2000 (Jpn) Address reprint requests to: K. Yanaka, M.D., Department of Neurosurgery, Institute of Clinical Medicine, University of Tsukuba, Tennodai, Tsukuba, Ibaraki , Japan. Commentary on this paper appears on the next page.

6 Laminoplasty and Respiration 493 Commentary This article might be better titled ``Respiratory Function in Myelopathic Patients.'' Basically it shows that when a patient is quite symptomatic with spinal cord compression their respiratory title volume is diminished, and their basic respiration rhythms are not effective. Respiratory function has to utilize not only the phrenic nerve (C3 4 areas), but also the intercostal nerves (T2 10), to have smooth and effective breathing. If the latter is significantly interfered with by the myelopathy, the title volume is diminished and the breathing is not as smooth. If the patient has some recovery from this, then the title volume will improve. It is probably true that patients without any myelopathy have even better title volumes and more even respirations. The other lesson to learn from this article is that these patients, especially after surgery, are going to be more prone to pulmonary problems. Therefore, actively working with them would be of value. Thomas B. DUCKER, M.D., F.A.C.S. Department of Neurosurgery Johns Hopkins University Annapolis, Maryland, U.S.A. This paper pointed out the very interesting and also veryimportantaspectofrespiratoryfunctioninthe surgical management of cervical spondylotic myelopathy, and proved a significant improvement in tidal volume following expansive laminoplasty for posterior decompression. As the authors also described, the most anterior part of the lateral columns of the spinal cord is critical for the maintenance of automatic respiratory activity in humans, so it may be really informative and of great value to investigate the respiratory function in anterior decompressive procedures for cervical spondylosis and OPLL causing myelopathy. I am looking forward to seeing further clinical investigations in this field by the authors. Hiroshi NAKAGAWA, M.D. Department of Neurological Surgery Aichi Medical University School of Medicine Aichi, Japan