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J Thorac Cardiovasc Surg 2006;132:530-536
© 2006 The American Association for Thoracic Surgery

General Thoracic Surgery

Electrophysiologic evaluation of phrenic nerve and diaphragm function after coronary bypass surgery: Prospective study of diabetes and other risk factors

Miguel A. Merino-Ramirez, MD, PhDa, Gustavo Juan, MD, PhDb, Mercedes Ramón, MD, PhDc, Julio Cortijo, PhDd, Elena Rubio, MD, PhDe, Anastasio Montero, MD, PhDf, Esteban J. Morcillo, MD, PhDe,*

a Department of Clinical Neurophysiology, Ribera Hospital, Alzira, Valencia, Spain
b Department of Medicine, Faculty of Medicine, University of Valencia, Valencia, Spain
e Department of Clinical Pharmacology, Faculty of Medicine, University of Valencia, Valencia, Spain
c Service of Pneumology, University General Hospital Consortium, Valencia, Spain
d Research Foundation, University General Hospital Consortium, Valencia, Spain
f Service of Cardiac Surgery, La Fe University Hospital, Valencia, Spain.

Received for publication March 7, 2006; revisions received April 19, 2006; accepted for publication May 12, 2006.

* Address for reprints: Esteban J. Morcillo, MD, PhD, Department of Clinical Pharmacology, Faculty of Medicine, Avda. Blasco Ibáñez, 15, E-46010 Valencia, Spain (Email: Gustavo.Juan{at}uv.es).


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
OBJECTIVE: Phrenic neuropathy after coronary artery bypass grafting has been related to various risk factors with conflicting results. The aim of this study was to assess the incidence, characteristics, and clinical consequences of phrenic neuropathy and the influence of diabetes and other risk factors.

METHODS: We conducted an observational, prospective study of parallel groups including 94 consecutive patients subjected to coronary artery bypass grafting, half of them with diabetes and associated polyneuropathy. Electrophysiologic study of phrenic nerve conduction as the reference method, chest radiography, diaphragm ultrasound, and functional respiratory tests were performed 24 to 48 hours before and 7 days after surgery. In those patients showing phrenic neuropathy, explorations were repeated, including needle diaphragmatic electromyography, at 1, 3, 6, 9, 12, 18, and 24 months or until recovery.

RESULTS: Fifteen of the 94 patients (16%) had phrenic neuropathy, 9 in the left side, 3 on the right, and 3 bilateral. Nine (60%) of the affected patients had diabetes, but diabetes did not represent a greater risk of neuropathy (relative risk 1.5, 95% confidence interval 0.6-3.9). Multivariate analysis showed no association of phrenic nerve injury with age, sex, ejection fraction, diabetes, use of internal thoracic artery, or number of grafts as risk factors. Phrenic neuropathy did not result in greater morbidity, and most patients recovered in less than 1 year.

CONCLUSIONS: None of the risk factors studied, including diabetes, influenced the appearance of phrenic neuropathy, thus indicating a role for nerve damage during surgery. Low morbidity and relatively rapid recovery were observed.

Abbreviations and Acronyms CABG = coronary artery bypass grafting; CI = confidence interval; EMG = electromyography; PEMAX = maximal static expiratory pressure; PIMAX = maximal static inspiratory pressure; PNCS = phrenic nerve conduction studies; PNI = phrenic nerve injury


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Phrenic nerve injury (PNI) is a widely recognized complication after cardiac surgery. Although chest radiographs and ultrasound examinations are the only criteria used in some studies to define PNI, these procedures lack sufficient sensitivity and specificity.1Go Electrophysiologic study of phrenic nerve conduction combined with diaphragm electromyography (EMG) are currently considered as the "gold standard" in assessing phrenic nerve function, providing information on the pathophysiology and prognosis of PNI.2Go In most cases, PNI is unilateral with scarce clinical impact; however, bilateral PNI may be associated with significant respiratory morbidity.3Go

PNI after coronary surgery has been related to phrenic nerve cold injury,4Go diabetes mellitus,5Go surgical manipulations,1,6Go and ischemia of the nerve resulting from harvesting of the internal thoracic artery.7Go In particular, diabetes is an important risk factor for coronary disease, and up to 30% of these patients undergo coronary artery bypass grafting (CABG).8Go A greater incidence of PNI has been reported in patients with diabetes.5Go However, no prospective, controlled, clinical study has been carried out to date, including electrophysiologic evaluation, to assess diabetes as a risk factor for PNI during CABG.

Therefore, the main objective of the present work was to conduct an electrophysiologic evaluation of PNI during CABG and to assess the relative importance of long-duration diabetes with polyneuropathy as well as other risk factors. In addition, recovery after PNI and clinical evolution were studied.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
Patients
From February 2, 2000, to February 28, 2002, 109 patients subjected to CABG were consecutively enrolled in this study, 53 with diabetes and 56 without diabetes. All patients gave written informed consent, and the study protocol was approved by the University of Valencia Hospital Ethics Committee. A recent electrophysiologic study excluding diabetics found an incidence of PNI after cardiac surgery of about 10%.9Go An increased relative risk of 2.8-fold for the development of PNI after CABG has been reported in patients with versus those without diabetes.5Go In the present study, sample size was approached considering an incidence of PNI after CABG of 15% for controls and 40% for diabetics (2.66-fold increase), with an {alpha} error of .05, a potency of 80%, and a 10% failure rate in patient follow-up. Inclusion criteria were diabetes mellitus of more than 10 years' duration with associated polyneuropathy evidenced with standard electrophysiologic evaluation.10Go As a control group, patients without diabetes but concurrently subjected to CABG were included. Patients with precedent cardiac or thoracic surgery, chronic respiratory disease, neuromuscular disease, severe or unstable psychologic alterations, or toxic habits including alcohol abuse were excluded.

Study Design
An observational, prospective study of parallel groups of patients subjected to CABG in a reference university hospital was conducted. Clinical data, respiratory function tests, chest radiographs, diaphragmatic ultrasound examination, and phrenic nerve conduction studies (PNCS) were carried out 1 to 2 days before and 6 to 7 days after surgery. In patients with PNI, clinical and electrophysiologic evaluations were repeated, including needle diaphragmatic EMG at 1, 3, 6, 9, 12, 18, and 24 months after surgery or until neurophysiologic variables returned to normal values.

Surgical Technique
CABG was performed with a standard technique. Cardiopulmonary bypass was begun with moderate antegrade-retrograde cold intermittent blood cardioplegia (nasopharyngeal temperature 28°C-32°C). Topical hypothermia was elicited by intermittently applied cold saline (4°C). A group of 24 patients were subjected to surgery in normothermic conditions, with the heart beating (no cardiopulmonary bypass).

Electrophysiologic Evaluation of Phrenic Nerve and Diaphragm
Amplitude, latency, negative peak duration and area, and right-to-left differences for these variables were measured according to established protocols11Go in 920 healthy volunteers to establish the normal reference values and their reproducibility for our laboratory.12Go Latencies greater than 8.4 ms, amplitude values less than 300 µV, right-left differences greater than 12.6% and greater than 40% for latency and amplitude, respectively, as well as variation greater than 11% for latency and greater than 34% for amplitude between the first and the second consecutive studies, were considered beyond normal limits.12Go

The PNCS in patients subjected to CABG were performed by the same technician in all evaluations (electromyograph Medelec Synergy T-EP-system; Viasys Healthcare, Conshohocken, Pa,). Those patients with abnormalities in nerve conduction were re-evaluated after 1 month and also underwent a diaphragmatic EMG to assess whether neuropathy was primarily axonal or demyelinating. Diaphragm EMG was performed by monopolar needle electrodes.13Go

Other Measurements
Patients with diabetes of more than 10 years' duration were subjected to a standard electrophysiologic study before surgery to evaluate associated polyneuropathy (distal bilateral lesions without any other apparent cause).10Go Pulmonary function testing (Compact Transfer; Erich Jaeger, Inc, Würzburg, Germany) according to the American Thoracic Sociey,14Go maximal static inspiratory (PIMAX) and expiratory (PEMAX) pressures (Sibelmed 163, Barcelona, Spain), chest radiographs (left and right hemidiaphragm elevations defined according to established criteria),15Go and diaphragmatic ecography in M mode (mobility < 2 cm was considered)16Go were recorded. Duration of stay in intensive care unit, duration of mechanical ventilation, and total duration of hospital stay were also recorded.

Statistical Analysis
Data are presented as proportions for qualitative variables and as means for quantitative variables. Ninety-five percent confidence intervals (CI) or standard deviations are given as indicated. The {chi}2 test was used to compare proportions, and analysis of variance followed by post hoc t test or the corresponding nonparametric tests were used to compare means of different experimental groups. The influence of risk factors on PNI was estimated by comparison of relative risk or odds ratios with univariate and multivariate analysis as appropriate by logistic regression analysis. Statistical analysis was carried out by the SPSS version10 software package (SPSS, Inc, Chicago, Ill).


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Patient Characteristics
Fifteen of the 109 patients initially recruited were excluded from the analysis because of refusals (1 patient to surgery and 2 patients to the electrophysiologic evaluation during the first week after the operation), death (1 patient died in the immediate postoperative period of acute cardiac tamponade), and failures in data monitoring during the follow-up (11 patients). These excluded patients did not differ from the remaining 94 patients in terms of their risk factors for PNI or their clinical outcomes, especially with respect to PNI (not shown). Of the 94 patients who finally entered the study, 47 (50%) had diabetes. Demographic characteristics, cardiorespiratory status, and surgical data of patients are shown in Table E1. Patients with diabetes were slightly older (64.7 vs 60.6 years old; P = .02) and had a smaller forced expiratory volume in 1 second (91.7% vs 96.3%; P = .03). The other demographic characteristics, preoperative cardiorespiratory parameters and type of surgery, were not different between the groups. PNCS before surgery showed no differences between patients with and without diabetes (Table E2).


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  		TABLE E1. Demographic, preoperative cardiorespiratory function, and surgical variables regarding the 94 patients in the study
 

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  		TABLE E2. Comparison of preoperative phrenic nerve parameters between diabetic and nondiabetic patients
 
Evaluation of Risk Factors for Phrenic Nerve Dysfunction
The univariate analysis comparing incidence and relative risk of postoperative PNI between diabetic and nondiabetic patients showed no statistically significant difference (Table 1). The logistic regression analysis failed to find any particular risk factor associated with PNI (Table 2). However, the univariate analysis showed differences in relative risk for some factors. Thus, right internal thoracic artery harvesting was used in 8 patients, of whom 1 (12.5%) had left PNI and 3 (37.5%) had right PNI. Therefore, although in multivariate analysis the use of the right internal thoracic artery was not associated with PNI, in the univariate analysis there was a significantly increased risk of phrenic dysfunction in the right side (relative risk 10.8, 95% CI 2.6-44.8; P < .01). Left internal thoracic artery harvesting resulted in no significant differences between left and right PNI (relative risk 2.0, 95% CI 0.8-5.1; P = .21). Use of on-pump CABG resulted in PNI in 12 patients (17.1%), while 3 PNI cases were observed with off-pump surgery (12.5%): relative risk 1.4 (95% CI 0.4-4.5; P = 0.75). Use of on-pump CABG resulted in 10 left versus 4 right PNIs, whereas off-pump surgery produced 2 left and 2 right PNI cases. The relative risk for left PNI associated with on-pump surgery was 1.7 (95% CI 0.4-7.3; P = .72) and that for right PNI was 0.7 (95% CI 0.1-3.5; P = .64). On the other hand, the univariate analysis showed also that the use of fewer than 3 grafts was significantly associated with a decreased risk of PNI (relative risk 0.9, 95% CI 0.85-0.98; P < .05). Patients were operated on by 6 surgeons, but the incidence of PNI among patients operated on by these different surgeons did not significantly differ (P = .42).


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  		TABLE 1. Comparison of incidence (percent) and relative risk of postoperative phrenic nerve injury between diabetic and nondiabetic patients
 

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  		TABLE 2. Results of logistic regression analysis for phrenic nerve dysfunction
 
Incidence and Recovery of Phrenic Nerve Dysfunction
There was a tendency to decreased diaphragmatic potential amplitude and to increased latency values in the postoperative study. Individual phrenic nerve conduction latency and amplitude data from those patients with neuropathy is shown in Figure 1. Fifteen patients (15.95%) had PNI, 9 on the left side, 3 on the right side, and 3 bilateral (ie, 18 nerves were affected). The relative risk of a lesion in the left side relative to the right side was 2.0 (95% CI 0.8-4.8; P = .18). Demyelinating neuropathy was observed in 12 nerves with block conduction criteria in 6 of them. In the other 6 nerves there was axonal injury. The recovery took place earlier for demyelination (1-3 months) than for axonal injury (6-18 months), and 1 nerve failed to recover during the observation period (Figure 2). A severe case of axonal neuropathy is shown in Figure E1, with data for phrenic nerve conduction and hemidiaphragm needle EMG shown at 1, 3, 9, and 18 months after surgery.


Figure 1
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  		Figure 1. Evaluation of phrenic nerve conduction before and after surgery in 14 patients with phrenic neuropathy who either did or did not have diabetes (1 additional patient showed no response and was not included in the figure). Augmented latency and decreased amplitude was observed in these patients after surgery, but individual predominance of changes in latency or amplitude is discussed in text. No significant differences were found between diabetics and nondiabetics for relative changes in latency and amplitude. Percentage differences of first-to-second study and right-to-left side were within standard limits (not shown). In the graph, each line represents a diabetic (broken line) or nondiabetic (continuous line) patient. Points are mean ± SEM. A significant difference was found between the preoperative and postoperative evaluations (*P < .05).

 

Figure 2
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  		Figure 2. Time course of postoperative recovery of phrenic nerve injury. Eighteen nerves were affected in 15 patients. The most rapid recovery corresponded to demyelination without blocked conduction (6 nerves), which recuperated in 1 month ({square}). Cases of demyelination associated with blockade of conduction (6 nerves) recovered within 3 months ({circ}). The lowest rate of recovery was associated with axonal injury (6 nerves) ({triangleup}). In this last group, 1 of the 6 nerves did not recover after 24 months (not shown).

 

Figure 1
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  		Figure E1. Summary of the results of phrenic nerve conduction (left panels) and hemidiaphragmatic needle electromyography (right panels) of a diabetic patient with absent response at 1 week after surgery but then showing a progresive improvement in the following months, as indicated. One month later, no responses were seen in the right side (panel A), but needle electromyography showed profuse positive sharp waves and fibrillations (panel B). Three months later, polyphasic responses were recorded with needle electrode from the right hemidiaphragm in response to phrenic nerve stimulation, with an onset latency of 22.5 ms (panel C), and small polyphasic reinervation motor unit action potentials were observed (panel D). Nine months later, reduced and delayed responses were recorded with a surface electrode from the right hemidiaphragm to phrenic nerve stimulation, with an onset latency of 10.2 ms and amplitude of 380 µV (panel E) and needle electromyography with a larger number of motor unit actions potentials (panel F). Eighteen months later, normal response (latency 6.85 ms; amplitude 835 µV) was recorded with a surface electrode from the right hemidiaphragm to phrenic nerve stimulation (panel G). Calibration: sensitivity is 0.1 (A, B,), 0.2 (D-G), and 0.5 (C) mV per division, and sweep speed is 10 ms per division in all panels except F, which is 100 ms per division.

 
Postoperative Outcome
Clinical consequences of PNI are summarized in Tables 3A and 3B. Go There were no consequences in cardiac intensive care unit and hospital stays and in duration of mechanical ventilation. The patient with severe axonal injury received mechanical ventilation for 5 days. The 3 patients with bilateral PNI were successfully weaned in the first 24 hours after surgery. Only patients with phrenic neuropathy had clinical signs of diaphragmatic paralysis such as paradoxical breathing plus orthopnea (5 patients) and diaphragmatic elevation (4 patients). The ultrasound evaluation showed abnormalities in only 7 patients (46%) with neuropathy but also in 29 (36%) without neuropathy. Pleural effusion was present in 59 (62.8%) patients and 8 (8.5%) had atelectasis, affecting in the same proportion to patients with and without PNI. Spirometric and PIMAX and PEMAX values fell below 80% of their predicted values in 90 patients (15 with PNI and 75 without PNI) more than 1 week after surgery. After 1 month, only patients with hemidiaphragm elevation (4 patients) maintained respiratory function values below 80% of normal, with recovery paralleling that indicated by chest radiographs.


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  		TABLE 3A. Clinical data comparing patients with and without phrenic neuropathy: Duration of mechanical ventilation, ICU, and hospital stay
 

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  		TABLE 3B. Clinical data comparing patients with and without phrenic neuropathy: Clinical, radiologic, and ultrasound consequences of phrenic neuropathy
 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
The incidence of PNI in 94 patients subjected to CABG was 15 patients (15.9%), with predominance of the left side (9 patients) compared with the right side (3 patients), and bilateral dysfunction in 3 patients. The main objective of our study was to assess the influence of diabetes in the development of PNI after CABG. To our knowledge, no prospective study has been designed with this defined purpose. In our study, both groups (patients with diabetes and those without diabetes) had similar characteristics and were subjected to similar surgical procedures; therefore, the two populations were comparable. The small difference in age (4 years) is unlikely to have any influence because only marked differences are relevant.11Go Forced expiratory volumes in 1 second were slightly lower in diabetics,17Go but this small difference is likely irrelevant inasmuch as it was unrelated to phrenic nerve dysfunction as demonstrated by phrenic nerve conduction and diaphragm studies showing no significant difference between the two groups of patients. The finding in this study of normal PNCS in diabetics with associated polyneuropathy is consistent with clinical predominance of symmetrical distal polyneuropathy, whereas proximal diabetic neuropathy is uncommon.18Go

In multivariate analysis, no significant association was found between PNI after CABG and any of the risk factors studied, including diabetes mellitus. Although diabetics were reported at higher risk for elevated hemidiaphragm after CABG,5Go other studies using electrophysiology to define PNI found no increased risk for these patients.2,16Go However, a limitation of our study is that, despite a trend toward differences between groups, sample size is not sufficient to exclude a level of increased risk in diabetics lower than that previously reported as significant.5Go

Other risk factors also appeared as not significantly associated with PNI. Thus, hypothermia was not a risk factor, because PNI was also observed on the right side (6 cases not subjected to local hypothermia), as well as in patients without cardiopulmonary bypass (3 cases, 1 of them bilateral). However, unlike in other studies,9Go iced slush was not used; therefore, the degree of hypothermia in our study was not intense enough to affect phrenic nerve function. An association between use of the internal thoracic artery and PNI has been reported,16Go but others failed to corroborate this finding.2,9Go In keeping with this, the left internal thoracic artery was used in 84% of our patients without PNI. However, the predominance of left PNI and the increased risk of right PNI linked to the use of a high number of grafts (and therefore also of the right internal thoracic artery, as indicated by the univariate analysis) suggest that, independently of other factors, direct or indirect insult to the nerve during surgical manipulation (dissection of internal thoracic artery and electrocautery) could be a causative factor in our study. This is in keeping with other observations.1,6,7Go

In accordance with other reports,2,16Go an important finding of this study is the lack of predictive and diagnostic accuracy of clinical signs, chest x-ray films, pulmonary function tests, and ultrasound studies of diaphragm function, probably due to confounding clinical and radiologic alterations and difficulties in performing forced respiratory maneuvers in the immediate postoperative period. Therefore, we used PNCS as the "gold standard" to assess phrenic nerve dysfunction. Combined with diaphragm EMG, these studies provide clinically useful information on the pathophysiology and prognosis of the lesion.19,20Go With this technique, a lower incidence of phrenic neuropathy after CABG is found with values between 10%9Go and 36%.21Go The incidence of 16% found in this study is within this range of values.

In this study, latency and amplitude were used because these two variables provide complementary information for defining nerve lesion. Area measurements were not used since this variable has been less studied and its pathophysiologic value is similar to that of amplitude.22Go In our patients, 6 of the affected nerves showed prolonged latencies without decreased amplitudes and with no appreciated alterations in EMG. Along with rapid recovery after 1 month, these results suggest demyelination without axonal damage. Another 6 nerves showed marked decreases in amplitude without acute signs of axonal degeneration in EMG after 1 month but with a reduced number of activated motor units, which indicates partially blocked conduction owing to focal demyelination at the injured site of the nerve. In 5 of the 6 nerves with EMG data of axonal degeneration (fibrillation and positive waves) and predominant alteration of amplitude, a slowly progressive recuperation of nerve excitability with gradual increase in amplitude was shown, suggesting axonotmesis and requiring a longer recovery time (≥6 months). However, 1 additional patient showed marked signs of axonal damage with no response after stimulation during 2 years of follow-up, which suggests a severely damaged nerve (neurotmesis). Early cases of PNI with rapid recovery were undetected in the first postoperative electrophysiologic evaluation, but these mild transient nerve alterations are unlikely to have clinical relevance. The recovery times found in this study for the different types of lesions as indicated above are within values reported in the literature.6,21,23Go

Taken together, our data show that, at early stages, absent or reduced nerve responses do not necessarily indicate a bad outcome; a combination of needle EMG and serial conduction studies are necessary to determine a diagnosis and reliable prognosis. Most of the cases of phrenic nerve dysfunction were unilateral and not associated with greater morbidity, longer duration of respiratory support, or longer intensive care unit and hospital stays. This is in agreement with the irrelevant clinical consequences of unilateral PNI except when associated with other cardiorespiratory abnormalities.23Go These results applied only to adults, because in children, diaphragmatic paralysis complicating cardiothoracic surgery continues to have a significant morbidity.24Go Taking into account our results, diaphragm EMG could be useful in children to predict time of recovery and necessity of diaphragmatic plication.

In conclusion, neither diabetes nor any of the other risk factors analyzed significantly influenced the appearance of phrenic nerve injury, thus suggesting that surgical manipulation was the main causative agent in our patients. Phrenic nerve conduction and diaphragm needle EMG are useful and reliable techniques to evaluate phrenic nerve damage, providing valuable information on its pathophysiology, evolution, and prognosis. Nevertheless, the presence of phrenic neuropathy in our patients was without relevant clinical impact in terms of evolution and recovery except in 1 case.


   Footnotes
 
This study was supported in part by grants from SAF2005-00669 (J.C.) and SAF2003-07206-C02-01 (E.J.M.) from CICYT (Ministry of Science and Technology, Spanish Government) and Research Groups-03/166, Network-CTIAE/C/03/116 and Project-GV04B72 from Regional Government (Generalitat Valenciana).


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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