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Hand Surgery, Vol. 20, No. 1 (2015) 47–52 © World Scientific Publishing Company DOI: 10.1142/S0218810415500069
IMPACT OF PHRENIC NERVE PARALYSIS ON THE SURGICAL OUTCOME OF INTERCOSTAL NERVE TRANSFER Yusuke Kita, Yasuhito Tajiri, Shinya Hoshikawa, Yukinori Hara and Junichi Iijima Department of Orthopedic Surgery Tokyo Metropolitan Hiroo Hospital, Tokyo, Japan Received 24 June 2014; Revised 1 October 2014; Accepted 2 October 2014; Published 20 January 2015 ABSTRACT Brachial plexus injuries (BPI) can be complicated by diaphragmatic paralysis (DP). This study determined the influence of DP on biceps brachii (BB) recovery after intercostal nerve transfer (ICNT) for BPI and investigated the respiratory complications of ICNT. The study included 100 patients, 84 showing no DP in preoperative and early postoperative chest radiographic images (non-DP group) and 16 with DP that persisted for over one year after surgery (DP group). The postoperative reinnervation time did not differ between groups. BB strength one year after surgery was lower in the DP group than non-DP group ( p ¼ 0:0007). No differences were observed 2–3 years after surgery. In the DP group, four patients had respiratory symptoms that affected daily activities and their outcomes deteriorated ( p ¼ 0:04). Phrenic nerve transfer should not be combined with ICNT in patients with poor respiratory function because of the high incidence of respiratory complications. Keywords: Brachial Plexus Injury; Diaphragmatic Paralysis; Intercostal Nerve Transfer; Phrenic Nerve Transfer.
INTRODUCTION
surgical outcome of these patients. The purpose of this study was to determine the influence of DP on biceps brachii (BB) recovery after undergoing ICNT and to investigate the respiratory complications of ICNT for the treatment of BPI.
Intercostal nerve transfer (ICNT) is performed on patients with brachial plexus injury (BPI) to restore lost elbow flexion function.1 Breathing movements require coordination between the diaphragm and the intercostal muscles. However, after an ICNT, the phrenic and intercostal nerves are functionally dissociated from each other; the former is responsible for breathing movements, and the latter is responsible for optional non-respiratory movements. This functional dissociation is believed to enable elbow flexion.2 In some cases, BPIs can be further complicated by diaphragmatic paralysis (DP) (Fig. 1). Therefore, when this surgical procedure is performed in patients with phrenic nerve paralysis, problems may occur during postoperative functional training, which may affect the
SUBJECTS AND METHODS Diagnosis of DP The diagnosis of DP was based on detailed observations published by Pornrattanamaneewong et al.3 Plain chest radiographs of the patients were analysed, and the right and left sides were compared by drawing a line parallel to the most cephalic side of the diaphragm on both sides of the inferior endplate of T10. Based on these analyses, patients who met one
Correspondence to: Dr. Yasuhito Tajiri, Department of Orthopedic Surgery Tokyo Metropolitan Hiroo Hospital, 2-34-10, Ebisu, Shibuya-ku, Tokyo 150-0013, Japan. Tel: (þ81) 3-3444-1181, Fax: (þ81) 3-3444-3196, E-mail: [email protected] 47
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Fig. 1
Left DP (41-year-old man; left-sided complete brachial plexus injury at the time of injury). Left: during inspiration; Right: during expiration.
of the following criteria were diagnosed with DP: (1) patients who did not show any change in the elevation of the diaphragm during expiration and inspiration; (2) patients (rightsided DP) whose right diaphragm was 1.1 or more vertebral bodies higher than the left diaphragm; or (3) patients (leftsided DP) who showed a difference of 0.2 or less vertebral bodies between the right and left diaphragm, or whose left diaphragm was more elevated.
Patient Population The study was conducted on 268 patients who were treated with ICNT for elbow flexion dysfunction due to BPI at the Department of Orthopedics of Tokyo University Hospital and at Tokyo Metropolitan Hiroo Hospital between 1984 and 2011. ICNT is indicated for patients with avulsion of C6 and C7, avulsion or rupture of C5, independent of the status of lower roots. Also when nerve graft is reserved and the length of the available graft is not sufficient to connect large gaps, ICNT is performed to restore elbow flexion.1 This study has been approved by the Ethics Committee of Tokyo Metropolitan Hiroo Hospital. The exclusion criteria were as follows: Age less than 16 years or more than 45 years at the time of the injury and a waiting period of 6 months or longer between the injury and surgery, in which case the postoperative outcomes are conventionally regarded as unfavourable. The study included 100 patients, 84 patients (non-DP group) whose BB muscle strength was measured one year or more after surgery and whose preoperative and early postoperative chest radiographic images showed no DP, and 16 patients whose DP persisted for
one year or longer after surgery (DP group; right side: 7 patients, left side: 9 patients). All patients in the DP group had both BPI and DP on the same side of the body. In ten cases, DP was observed at the time of injury, and in six cases, DP developed postoperatively after an ICNT that was combined with phrenic nerve transfer. The patients’ age ranged from 16 to 41 years (mean age, 23.5 years). About 97 of them were men, and three were women. Paralysis was on the right side in 43 cases and on the left in 57 cases. Regarding the types of paralysis, the C5–6 type accounted for 9 cases, the C5–7 type accounted for 12 cases, the C5–8 type accounted for 17 cases, and the total-roots type accounted for 59 cases. In addition, the subclavian type accounted for three cases. The waiting period between the injury and surgery was 2–6 months (average, 3.0 months). The follow-up period after surgery was 12–200 months (average, 51.4 months).
Outcome Assessment We defined postoperative reinnervation as the period elapsed until needle electromyography demonstrated reinnervation of the BB muscle. In the DP and non-DP groups, data were collected for the period until postoperative reinnervation. We also defined postoperative elbow flexion strength as a surgical outcome, and the manual evaluation of BB muscle strength (Medical Research Council) was studied retrospectively to assess postoperative elbow flexion strength at time points one, two, and three years after surgery. The impact of respiratory symptoms on the postoperative recovery of muscle strength and on elbow flexion strength were examined using the Hugh-Jones
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Table 1 Hugh-Jones Classification for Breathlessness Based on Daily Activities Affected.
Table 2 Groups.
Grade
Description
Variables
Non-DP Group
DP Group
The patient’s breathing is as good as that of others of the same sex, age, and build while at work, on walking, or on climbing hills or stairs. The patient is able to walk with healthy persons of the same sex, age, and build on the level but is unable to keep up on hills or stairs. The patient is unable to keep up with healthy persons on the level but is able to walk a mile or more at a slower speed. The patient is unable to walk more than about 100 yards on the level without a rest. The patient is breathless on talking or undressing or is unable to leave the house because of breathlessness.
Numbers Gender Male Female
84
16
82 2
15 1
Side Left Right
48 36
9 7
Age at the time of injury
23.2
23.8
Type of injury C5–6 C5–7 C5–8 Total Subclavian
6 8 14 53 3
3 4 3 6 0
Waiting period
3.07
2.87
II
III IV V
classification (Table 1) for patients in the DP group whose respiratory symptoms could be ascertained after surgery.4
Statistical Analysis Statistical analyses compared the data from the two groups using Student’s t-tests, Mann–Whitney U-tests, and the m n Yates Chi square test.
RESULTS Patient Demographics No statistically significant differences were observed in the patients’ gender, paralysis sides, age at injury, type of injury, waiting period, and the number of intercostal nerves used for transfer between the DP group and the non-DP group ( p > 0:05, Mann–Whitney U-test, or m n Yates Chi square test for differences in the type of injury) (Table 2).
Overall Outcomes The time before postoperative reinnervation was 4–8 months (average, 4.89 months) in the non-DP group and 4–7 months (average, 5.37 months) in the DP group, and this difference was not significant ( p ¼ 0:13, Student’s t-test) (Fig. 2). Strength in the BB muscle one year after surgery was significantly lower in the DP group than in the non-DP group ( p ¼ 0:0007, Mann–Whitney U-test) (Fig. 3). Two and three years after surgery, no differences were observed in the surgical outcomes between the two groups ( p ¼ 0:94 and p ¼ 0:73, respectively; Mann–Whitney U-test) (Fig. 3).
Demographic Data of Patients in the DP or Non-DP p 0.41*
0.95*
0.35* 0.46**
Number of intercostal nerves used for transfer 2 3
0.40* 0.95*
74 10
14 2
Notes: No statistically significant differences were observed in the patients’ gender, paralysis sides, age at time of injury, types of injury, waiting periods, and number of intercostal nerves used for transfer between the DP group and the non-DP group ( p > 0:05, *Mann–Whitney U-test, **m n Yates Chi square test).
p > 0.05 100% 90% percentage of patients
I
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80% 70% 60% 50% 40% 30% 20% 10% 0% DP group
8 months
7 months
6 months
non-DP group 5 months
4 months
Fig. 2 Time spent before reinnervation. No significant difference was found between the DP and the non-DP groups in the time elapsed before postoperative reinnervation ( p ¼ 0.13, Student’s t-test).
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p = 0.0007
Respiratory Complications in the DP and Non-DP Groups
p > 0.05
100% 90%
percentage of patients
80% 70% 60% M5 50%
M4 M3
40%
M2
30%
M1
20% 10% 0% Non-DP DP group group one year after surgery
Non-DP DP group group two years after surgery
Non-DP DP group group three years after surgery
Fig. 3 Outcomes after surgery. The surgical outcomes one year after surgery was significantly lower in the DP group than the non-DP group ( p ¼ 0:0007; Mann–Whitney U-test). Two and three years after surgery, no differences were observed in the surgical outcomes between the two groups ( p ¼ 0:94, 0.73, respectively; Mann–Whitney U-test).
Table 3
Case Number
Among the 16 patients in the DP group, the respiratory symptoms after surgery could be ascertained in 11 patients. One year after surgery, six patients showed a persistence of subjective symptoms, such as shortness of breath, and developed restrictive respiratory dysfunction; two of these patients had chronic respiratory failure (Table 3). Among these six patients, four had subjective symptoms that were likely to interfere with activities of daily living (ADL), and they were classified as grade II or higher in the Hugh-Jones classification. They showed a percent vital capacity (%VC) of 65% or less one year after surgery. This did not include the other two patients who showed subjective symptoms that were classified as grade I in the Hugh-Jones classification and had virtually no impact on ADL. The four patients with respiratory dysfunction showed significant deterioration in comparison with the remaining six patients who performed respiratory function tests. These six patients showed no respiratory symptoms that could interfere
Surgical Outcome (Manual Muscle Testing, MMT) and Postoperative Respiratory Status in the DP Group.
Gender
Side (Left/Right)
Type of Injury
1 2 3 4 5 6 7
Male Male Male Male Male Male Male
Right Right Left Left Left Left Left
C5–6 C5–7 Total C5–7 Total Total C5–6 þ post
8 9
Male Male
Right Right
C5–7 C5–8
10 11
Male Male
Right Right
Total C5–8
Respiratory Symptoms One Year After Surgery Normal Normal Normal Normal Normal Hugh-Jones I Hugh-Jones I Hugh-Jones II Hugh-Jones II ! chronic Respiratory failure (PaO2 47, PaCO2 51) Hugh-Jones III Hugh-Jones III ! chronic Respiratory failure (PaO2 56, PaCO2 51)
Notes: Hugh-Jones (HJ) classification I or lower versus HJ II or higher; Percent Vital Capacity (%VC; one year after surgery) p ¼ 0:04; Manual Muscle Testing (MMT; one year after surgery) p ¼ 0:03; MMT final outcome (MMT final; p ¼ 0:013 (Mann–Whitney U-test was used in all). Case number 9: 11 years after surgery, home oxygen therapy has been continued (%VC of 59%); Case number 10: 5 years after surgery, respiratory symptoms remain as HJ III (%VC of 60%); Case number 11: 4 years after surgery, home oxygen therapy has been continued (%VC of 44%).
%VC
MMT
MMT Final
Not performed 67% 63% 84% 83% 68% 75%
1 3 3 1 2 3 3
4 4 4 3 3 4 4
53% 65%
1 1
3 2
53% 45%
1 1
2 2
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with ADL and were classified as grade I or lower in the HughJones classification ( p ¼ 0:04, Mann–Whitney U-test). The time to reinnervate was 4–7 months in these patients, which was not particularly prolonged, and the muscle strength of the brachial biceps one year after surgery was M1 in all cases. Muscle strength deteriorated significantly in four patients who were classified as grade II or higher compared with the remaining seven patients who were classified as grade I or lower in the Hugh-Jones classification. Among these four patients, the final outcomes (3–11 years after surgery) were M2 for three patients and M3 for one patient, and these outcomes were significantly worse than the findings for the remaining seven patients ( p ¼ 0:013, Mann–Whitney U-test) (Table 3).
DISCUSSION Although no significant difference was found between the DP and non-DP groups in the time that elapsed before electromyography demonstrated postoperative reinnervation, the outcome one year after surgery was significantly worse in the DP group compared with the non-DP group. This suggests that the complications of phrenic nerve paralysis had no impact on the early phases of nerve regeneration but affected subsequent functional training. A previous report on the relationship between respiratory function and DP after phrenic nerve transfer showed that respiratory function improved one year after surgery and almost reached pre-surgery levels.5 However, other reports have shown a decline in respiratory function that continued for approximately one year after surgery.6,7 During functional training in the early period after surgery, long-duration breath-holding exercises are performed with biofeedback. However, in the DP group, this exercise training could not be performed well because of the decreased VC that shortened the patients’ breathholding durations. As a result, their outcome was likely to deteriorate one year after surgery. Respiratory movements result from coordinated movements by the diaphragm and the intercostal muscles. However, when an ICNT is performed, the functions of the phrenic nerve and the intercostal nerves start to dissociate from each other one year after surgery, and the execution of respiratory movements relies mainly on the phrenic nerve.3 In other words, to perform an elbow flexion, the intercostal nerves continue their contractile activity, whereas breathing is performed through the action of the phrenic nerve alone. Therefore, if the phrenic
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nerve is paralyzed, breathing becomes difficult when the elbow is in the flexed position. During ADL, shortness of breath may occur, and holding the breath may be difficult for the patient. Thus, functional training that should include sustained breathholding exercises may become difficult to achieve. In terms of the muscle strength three years after surgery, there was no significant difference between patients with or without DP. In the DP group, 10 patients had confirmed DP that persisted 2 years or more after surgery. The other patients could have recovered from DP during the period after surgery. It is also possible that patients in the DP group with mild respiratory symptoms and normal %VC gradually acquired voluntary muscle movements with long-term training, and, even in the presence of DP, they learned to perform elbow flexion using the intercostal nerves. However, in this study, manual muscle testing (MMT), which is based on instantaneous muscle contractions, was used as a standard scale for the measurements. Thus, it is possible that there would be differences if the evaluations were conducted using endurance tests for which the effects of respiratory dissociation are expected to be remarkable. In the DP group, there were four patients with respiratory symptoms including shortness of breath, which interfered with ADL and they were classified as grade II or higher in the HughJones classification. The final outcomes were poor in those four patients compared with patients who were classified as grade I or lower in the Hugh-Jones classification and who did not experience any interference with ADL. Among the three patients in the DP group who had severe postoperative respiratory symptoms, two patients developed chronic respiratory failure and required home oxygen therapy, whereas one patient’s condition remained at stage III of the Hugh-Jones classification. For these patients, the postoperative outcome was MMT2, which was extremely poor. Therefore, a grade II or higher respiratory dysfunction and a %VC of 60% or lower may have an impact on training after one or more years. Even if an ICNT is performed, the chances of finally achieving elbow flexion are predicted to be low. In such patients, diaphragm plication may have to be performed to improve the respiratory symptoms.8,9 Accordingly, the outcomes for patients with DP in combination with a decline in respiratory function may be poor even if an ICNT is performed. The performance of an ICNT will not itself cause the postoperative respiratory status to deteriorate.10 However, if phrenic nerve transfer is performed in combination with an
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ICNT, mild restrictive respiratory dysfunction with a %VC of around 70% is seen.11 According to a study by Chuang et al., even if both the procedures are used, the only consequence is mild respiratory dysfunction that is not clinically problematic, suggesting that it is safe to use both procedures together.11 Our cases, however, included three patients who developed DP as a complication of the ICNT, resulting in a deterioration of respiratory function. According to Lisboa et al., the %VCs in DP patients without complications are in the 70–80% range, but, in those with respiratory and circulatory complications, it deteriorates to 50–60%.12 Two of the three patients developed atelectasis as an additional respiratory complication of DP, and their respiratory function deteriorated markedly, ultimately leading to poor outcomes. Outcomes may thus be poor if ICNT and phrenic nerve transfer are performed in combination and respiratory dysfunction develops. Caution should therefore be applied to the combined use of ICNT and phrenic nerve transfer. The limitations of the present study were that it was a retrospective study and the evaluated patients were mainly those with severe respiratory symptoms among patients complicated with respiratory symptoms. Because of the small number of sample cases with mild or lesser respiratory symptoms that had undergone respiratory function tests in the DP group, the comparison of respiratory symptoms was performed between the severe group and some of the mild group. In addition, a small number of cases from the DP group have been shown.
Concluding Remarks The following observations were made regarding ICNT performed on patients with complications of DP: . .
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There was no difference in the reinnervation time. The outcomes were poorer one year after surgery, but there was no difference two or more years after surgery.
.
In some cases, respiratory symptoms affecting ADL persisted. In such patients, the final outcome was also worse.
References 1. Nagano A, Ochiai N, Okinaga S, Restoration of elbow flexion in root lesions of brachial plexus injuries, J Hand Surg Am 17:815–821, 1992. 2. Homma I, Sibuya M, Hara T, Tsuyama N, Physiological characteristics of biceps muscle reinnervated by intercostal nerves, J Jpn Soc Surg Hand 4:868–871, 1988. 3. Pornrattanamaneewong C, Limthongthang R, Vathana T, Kaewpornsawan K, Songcharoen P, Wongtrakul S, Diaphragmatic height index: new diagnostic test for phrenic nerve dysfunction, J Neurosurg 117:890–896, 2012. 4. Hugh-Jones P, Lambert AV, A simple standard exercise test and its use for measuring exertion dyspnea, Brit Med J 1:65–71, 1951. 5. Xu WD, Gu YD, Lu JB, Yu C, Zhang CG, Xu JG, Pulmonary function after complete unilateral phrenic nerve transection, J Neurosurg 103:464– 467, 2005. 6. Chalidapong P, Sananpanich K, Kraisarin J, Bumroongkit C, Pulmonary and biceps function after intercostal and phrenic nerve transfer for brachial plexus injuries, J Hand Surg Br 29:8–11, 2004. 7. Luedemann W, Hamm M, Bl€omer U, Samii M, Tatagiba M, Brachial plexus neurotization with donor phrenic nerves and its effect on pulmonary function, J Neurosurg 96:523–526, 2002. 8. Freeman RK, Wozniak TC, Fitzgerald EB, Functional and physiologic results of video-assisted thoracoscopic diaphragm plication in adult patients with unilateral diaphragm paralysis, Ann Thorac Surg 81:1853–1857, 2006. 9. Celik S, Celik M, Aydemir B, Tunckaya C, Okay T, Dogusoy I, Long-term results of diaphragmatic plication in adults with unilateral diaphragm paralysis, J Cardiothorac Surg 5:111, 2010. 10. Giddins GE, Kakkar N, Alltree J, Birch R, The effect of unilateral intercostal nerve transfer upon lung function, J Hand Surg Br 20:675– 676, 1995. 11. Chuang ML, Chuang DC, Lin IF, Vintch JR, Ker JJ, Tsao TC, Ventilation and exercise performance after phrenic nerve and multiple intercostal nerve transfers for avulsed brachial plexus injury, Chest 128:3434–3439, 2005. 12. Lisboa C, Pare PD, Pertuze J, Contreras G, Moreno R, Guillemi S, Cruz E, Inspiratory muscle function in unilateral diaphragmatic paralysis, Am Rev Respir Dis 134:488–492, 1986.
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Hand Surgery, Vol. 20, No. 1 (2015) 47–52 © World Scientific Publishing Company DOI: 10.1142/S0218810415500069
IMPACT OF PHRENIC NERVE PARALYSIS ON THE SURGICAL OUTCOME OF INTERCOSTAL NERVE TRANSFER Yusuke Kita, Yasuhito Tajiri, Shinya Hoshikawa, Yukinori Hara and Junichi Iijima Department of Orthopedic Surgery Tokyo Metropolitan Hiroo Hospital, Tokyo, Japan Received 24 June 2014; Revised 1 October 2014; Accepted 2 October 2014; Published 20 January 2015 ABSTRACT Brachial plexus injuries (BPI) can be complicated by diaphragmatic paralysis (DP). This study determined the influence of DP on biceps brachii (BB) recovery after intercostal nerve transfer (ICNT) for BPI and investigated the respiratory complications of ICNT. The study included 100 patients, 84 showing no DP in preoperative and early postoperative chest radiographic images (non-DP group) and 16 with DP that persisted for over one year after surgery (DP group). The postoperative reinnervation time did not differ between groups. BB strength one year after surgery was lower in the DP group than non-DP group ( p ¼ 0:0007). No differences were observed 2–3 years after surgery. In the DP group, four patients had respiratory symptoms that affected daily activities and their outcomes deteriorated ( p ¼ 0:04). Phrenic nerve transfer should not be combined with ICNT in patients with poor respiratory function because of the high incidence of respiratory complications. Keywords: Brachial Plexus Injury; Diaphragmatic Paralysis; Intercostal Nerve Transfer; Phrenic Nerve Transfer.
INTRODUCTION
surgical outcome of these patients. The purpose of this study was to determine the influence of DP on biceps brachii (BB) recovery after undergoing ICNT and to investigate the respiratory complications of ICNT for the treatment of BPI.
Intercostal nerve transfer (ICNT) is performed on patients with brachial plexus injury (BPI) to restore lost elbow flexion function.1 Breathing movements require coordination between the diaphragm and the intercostal muscles. However, after an ICNT, the phrenic and intercostal nerves are functionally dissociated from each other; the former is responsible for breathing movements, and the latter is responsible for optional non-respiratory movements. This functional dissociation is believed to enable elbow flexion.2 In some cases, BPIs can be further complicated by diaphragmatic paralysis (DP) (Fig. 1). Therefore, when this surgical procedure is performed in patients with phrenic nerve paralysis, problems may occur during postoperative functional training, which may affect the
SUBJECTS AND METHODS Diagnosis of DP The diagnosis of DP was based on detailed observations published by Pornrattanamaneewong et al.3 Plain chest radiographs of the patients were analysed, and the right and left sides were compared by drawing a line parallel to the most cephalic side of the diaphragm on both sides of the inferior endplate of T10. Based on these analyses, patients who met one
Correspondence to: Dr. Yasuhito Tajiri, Department of Orthopedic Surgery Tokyo Metropolitan Hiroo Hospital, 2-34-10, Ebisu, Shibuya-ku, Tokyo 150-0013, Japan. Tel: (þ81) 3-3444-1181, Fax: (þ81) 3-3444-3196, E-mail: [email protected] 47
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Fig. 1
Left DP (41-year-old man; left-sided complete brachial plexus injury at the time of injury). Left: during inspiration; Right: during expiration.
of the following criteria were diagnosed with DP: (1) patients who did not show any change in the elevation of the diaphragm during expiration and inspiration; (2) patients (rightsided DP) whose right diaphragm was 1.1 or more vertebral bodies higher than the left diaphragm; or (3) patients (leftsided DP) who showed a difference of 0.2 or less vertebral bodies between the right and left diaphragm, or whose left diaphragm was more elevated.
Patient Population The study was conducted on 268 patients who were treated with ICNT for elbow flexion dysfunction due to BPI at the Department of Orthopedics of Tokyo University Hospital and at Tokyo Metropolitan Hiroo Hospital between 1984 and 2011. ICNT is indicated for patients with avulsion of C6 and C7, avulsion or rupture of C5, independent of the status of lower roots. Also when nerve graft is reserved and the length of the available graft is not sufficient to connect large gaps, ICNT is performed to restore elbow flexion.1 This study has been approved by the Ethics Committee of Tokyo Metropolitan Hiroo Hospital. The exclusion criteria were as follows: Age less than 16 years or more than 45 years at the time of the injury and a waiting period of 6 months or longer between the injury and surgery, in which case the postoperative outcomes are conventionally regarded as unfavourable. The study included 100 patients, 84 patients (non-DP group) whose BB muscle strength was measured one year or more after surgery and whose preoperative and early postoperative chest radiographic images showed no DP, and 16 patients whose DP persisted for
one year or longer after surgery (DP group; right side: 7 patients, left side: 9 patients). All patients in the DP group had both BPI and DP on the same side of the body. In ten cases, DP was observed at the time of injury, and in six cases, DP developed postoperatively after an ICNT that was combined with phrenic nerve transfer. The patients’ age ranged from 16 to 41 years (mean age, 23.5 years). About 97 of them were men, and three were women. Paralysis was on the right side in 43 cases and on the left in 57 cases. Regarding the types of paralysis, the C5–6 type accounted for 9 cases, the C5–7 type accounted for 12 cases, the C5–8 type accounted for 17 cases, and the total-roots type accounted for 59 cases. In addition, the subclavian type accounted for three cases. The waiting period between the injury and surgery was 2–6 months (average, 3.0 months). The follow-up period after surgery was 12–200 months (average, 51.4 months).
Outcome Assessment We defined postoperative reinnervation as the period elapsed until needle electromyography demonstrated reinnervation of the BB muscle. In the DP and non-DP groups, data were collected for the period until postoperative reinnervation. We also defined postoperative elbow flexion strength as a surgical outcome, and the manual evaluation of BB muscle strength (Medical Research Council) was studied retrospectively to assess postoperative elbow flexion strength at time points one, two, and three years after surgery. The impact of respiratory symptoms on the postoperative recovery of muscle strength and on elbow flexion strength were examined using the Hugh-Jones
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Table 1 Hugh-Jones Classification for Breathlessness Based on Daily Activities Affected.
Table 2 Groups.
Grade
Description
Variables
Non-DP Group
DP Group
The patient’s breathing is as good as that of others of the same sex, age, and build while at work, on walking, or on climbing hills or stairs. The patient is able to walk with healthy persons of the same sex, age, and build on the level but is unable to keep up on hills or stairs. The patient is unable to keep up with healthy persons on the level but is able to walk a mile or more at a slower speed. The patient is unable to walk more than about 100 yards on the level without a rest. The patient is breathless on talking or undressing or is unable to leave the house because of breathlessness.
Numbers Gender Male Female
84
16
82 2
15 1
Side Left Right
48 36
9 7
Age at the time of injury
23.2
23.8
Type of injury C5–6 C5–7 C5–8 Total Subclavian
6 8 14 53 3
3 4 3 6 0
Waiting period
3.07
2.87
II
III IV V
classification (Table 1) for patients in the DP group whose respiratory symptoms could be ascertained after surgery.4
Statistical Analysis Statistical analyses compared the data from the two groups using Student’s t-tests, Mann–Whitney U-tests, and the m n Yates Chi square test.
RESULTS Patient Demographics No statistically significant differences were observed in the patients’ gender, paralysis sides, age at injury, type of injury, waiting period, and the number of intercostal nerves used for transfer between the DP group and the non-DP group ( p > 0:05, Mann–Whitney U-test, or m n Yates Chi square test for differences in the type of injury) (Table 2).
Overall Outcomes The time before postoperative reinnervation was 4–8 months (average, 4.89 months) in the non-DP group and 4–7 months (average, 5.37 months) in the DP group, and this difference was not significant ( p ¼ 0:13, Student’s t-test) (Fig. 2). Strength in the BB muscle one year after surgery was significantly lower in the DP group than in the non-DP group ( p ¼ 0:0007, Mann–Whitney U-test) (Fig. 3). Two and three years after surgery, no differences were observed in the surgical outcomes between the two groups ( p ¼ 0:94 and p ¼ 0:73, respectively; Mann–Whitney U-test) (Fig. 3).
Demographic Data of Patients in the DP or Non-DP p 0.41*
0.95*
0.35* 0.46**
Number of intercostal nerves used for transfer 2 3
0.40* 0.95*
74 10
14 2
Notes: No statistically significant differences were observed in the patients’ gender, paralysis sides, age at time of injury, types of injury, waiting periods, and number of intercostal nerves used for transfer between the DP group and the non-DP group ( p > 0:05, *Mann–Whitney U-test, **m n Yates Chi square test).
p > 0.05 100% 90% percentage of patients
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80% 70% 60% 50% 40% 30% 20% 10% 0% DP group
8 months
7 months
6 months
non-DP group 5 months
4 months
Fig. 2 Time spent before reinnervation. No significant difference was found between the DP and the non-DP groups in the time elapsed before postoperative reinnervation ( p ¼ 0.13, Student’s t-test).
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p = 0.0007
Respiratory Complications in the DP and Non-DP Groups
p > 0.05
100% 90%
percentage of patients
80% 70% 60% M5 50%
M4 M3
40%
M2
30%
M1
20% 10% 0% Non-DP DP group group one year after surgery
Non-DP DP group group two years after surgery
Non-DP DP group group three years after surgery
Fig. 3 Outcomes after surgery. The surgical outcomes one year after surgery was significantly lower in the DP group than the non-DP group ( p ¼ 0:0007; Mann–Whitney U-test). Two and three years after surgery, no differences were observed in the surgical outcomes between the two groups ( p ¼ 0:94, 0.73, respectively; Mann–Whitney U-test).
Table 3
Case Number
Among the 16 patients in the DP group, the respiratory symptoms after surgery could be ascertained in 11 patients. One year after surgery, six patients showed a persistence of subjective symptoms, such as shortness of breath, and developed restrictive respiratory dysfunction; two of these patients had chronic respiratory failure (Table 3). Among these six patients, four had subjective symptoms that were likely to interfere with activities of daily living (ADL), and they were classified as grade II or higher in the Hugh-Jones classification. They showed a percent vital capacity (%VC) of 65% or less one year after surgery. This did not include the other two patients who showed subjective symptoms that were classified as grade I in the Hugh-Jones classification and had virtually no impact on ADL. The four patients with respiratory dysfunction showed significant deterioration in comparison with the remaining six patients who performed respiratory function tests. These six patients showed no respiratory symptoms that could interfere
Surgical Outcome (Manual Muscle Testing, MMT) and Postoperative Respiratory Status in the DP Group.
Gender
Side (Left/Right)
Type of Injury
1 2 3 4 5 6 7
Male Male Male Male Male Male Male
Right Right Left Left Left Left Left
C5–6 C5–7 Total C5–7 Total Total C5–6 þ post
8 9
Male Male
Right Right
C5–7 C5–8
10 11
Male Male
Right Right
Total C5–8
Respiratory Symptoms One Year After Surgery Normal Normal Normal Normal Normal Hugh-Jones I Hugh-Jones I Hugh-Jones II Hugh-Jones II ! chronic Respiratory failure (PaO2 47, PaCO2 51) Hugh-Jones III Hugh-Jones III ! chronic Respiratory failure (PaO2 56, PaCO2 51)
Notes: Hugh-Jones (HJ) classification I or lower versus HJ II or higher; Percent Vital Capacity (%VC; one year after surgery) p ¼ 0:04; Manual Muscle Testing (MMT; one year after surgery) p ¼ 0:03; MMT final outcome (MMT final; p ¼ 0:013 (Mann–Whitney U-test was used in all). Case number 9: 11 years after surgery, home oxygen therapy has been continued (%VC of 59%); Case number 10: 5 years after surgery, respiratory symptoms remain as HJ III (%VC of 60%); Case number 11: 4 years after surgery, home oxygen therapy has been continued (%VC of 44%).
%VC
MMT
MMT Final
Not performed 67% 63% 84% 83% 68% 75%
1 3 3 1 2 3 3
4 4 4 3 3 4 4
53% 65%
1 1
3 2
53% 45%
1 1
2 2
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with ADL and were classified as grade I or lower in the HughJones classification ( p ¼ 0:04, Mann–Whitney U-test). The time to reinnervate was 4–7 months in these patients, which was not particularly prolonged, and the muscle strength of the brachial biceps one year after surgery was M1 in all cases. Muscle strength deteriorated significantly in four patients who were classified as grade II or higher compared with the remaining seven patients who were classified as grade I or lower in the Hugh-Jones classification. Among these four patients, the final outcomes (3–11 years after surgery) were M2 for three patients and M3 for one patient, and these outcomes were significantly worse than the findings for the remaining seven patients ( p ¼ 0:013, Mann–Whitney U-test) (Table 3).
DISCUSSION Although no significant difference was found between the DP and non-DP groups in the time that elapsed before electromyography demonstrated postoperative reinnervation, the outcome one year after surgery was significantly worse in the DP group compared with the non-DP group. This suggests that the complications of phrenic nerve paralysis had no impact on the early phases of nerve regeneration but affected subsequent functional training. A previous report on the relationship between respiratory function and DP after phrenic nerve transfer showed that respiratory function improved one year after surgery and almost reached pre-surgery levels.5 However, other reports have shown a decline in respiratory function that continued for approximately one year after surgery.6,7 During functional training in the early period after surgery, long-duration breath-holding exercises are performed with biofeedback. However, in the DP group, this exercise training could not be performed well because of the decreased VC that shortened the patients’ breathholding durations. As a result, their outcome was likely to deteriorate one year after surgery. Respiratory movements result from coordinated movements by the diaphragm and the intercostal muscles. However, when an ICNT is performed, the functions of the phrenic nerve and the intercostal nerves start to dissociate from each other one year after surgery, and the execution of respiratory movements relies mainly on the phrenic nerve.3 In other words, to perform an elbow flexion, the intercostal nerves continue their contractile activity, whereas breathing is performed through the action of the phrenic nerve alone. Therefore, if the phrenic
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nerve is paralyzed, breathing becomes difficult when the elbow is in the flexed position. During ADL, shortness of breath may occur, and holding the breath may be difficult for the patient. Thus, functional training that should include sustained breathholding exercises may become difficult to achieve. In terms of the muscle strength three years after surgery, there was no significant difference between patients with or without DP. In the DP group, 10 patients had confirmed DP that persisted 2 years or more after surgery. The other patients could have recovered from DP during the period after surgery. It is also possible that patients in the DP group with mild respiratory symptoms and normal %VC gradually acquired voluntary muscle movements with long-term training, and, even in the presence of DP, they learned to perform elbow flexion using the intercostal nerves. However, in this study, manual muscle testing (MMT), which is based on instantaneous muscle contractions, was used as a standard scale for the measurements. Thus, it is possible that there would be differences if the evaluations were conducted using endurance tests for which the effects of respiratory dissociation are expected to be remarkable. In the DP group, there were four patients with respiratory symptoms including shortness of breath, which interfered with ADL and they were classified as grade II or higher in the HughJones classification. The final outcomes were poor in those four patients compared with patients who were classified as grade I or lower in the Hugh-Jones classification and who did not experience any interference with ADL. Among the three patients in the DP group who had severe postoperative respiratory symptoms, two patients developed chronic respiratory failure and required home oxygen therapy, whereas one patient’s condition remained at stage III of the Hugh-Jones classification. For these patients, the postoperative outcome was MMT2, which was extremely poor. Therefore, a grade II or higher respiratory dysfunction and a %VC of 60% or lower may have an impact on training after one or more years. Even if an ICNT is performed, the chances of finally achieving elbow flexion are predicted to be low. In such patients, diaphragm plication may have to be performed to improve the respiratory symptoms.8,9 Accordingly, the outcomes for patients with DP in combination with a decline in respiratory function may be poor even if an ICNT is performed. The performance of an ICNT will not itself cause the postoperative respiratory status to deteriorate.10 However, if phrenic nerve transfer is performed in combination with an
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ICNT, mild restrictive respiratory dysfunction with a %VC of around 70% is seen.11 According to a study by Chuang et al., even if both the procedures are used, the only consequence is mild respiratory dysfunction that is not clinically problematic, suggesting that it is safe to use both procedures together.11 Our cases, however, included three patients who developed DP as a complication of the ICNT, resulting in a deterioration of respiratory function. According to Lisboa et al., the %VCs in DP patients without complications are in the 70–80% range, but, in those with respiratory and circulatory complications, it deteriorates to 50–60%.12 Two of the three patients developed atelectasis as an additional respiratory complication of DP, and their respiratory function deteriorated markedly, ultimately leading to poor outcomes. Outcomes may thus be poor if ICNT and phrenic nerve transfer are performed in combination and respiratory dysfunction develops. Caution should therefore be applied to the combined use of ICNT and phrenic nerve transfer. The limitations of the present study were that it was a retrospective study and the evaluated patients were mainly those with severe respiratory symptoms among patients complicated with respiratory symptoms. Because of the small number of sample cases with mild or lesser respiratory symptoms that had undergone respiratory function tests in the DP group, the comparison of respiratory symptoms was performed between the severe group and some of the mild group. In addition, a small number of cases from the DP group have been shown.
Concluding Remarks The following observations were made regarding ICNT performed on patients with complications of DP: . .
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There was no difference in the reinnervation time. The outcomes were poorer one year after surgery, but there was no difference two or more years after surgery.
.
In some cases, respiratory symptoms affecting ADL persisted. In such patients, the final outcome was also worse.
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