149: Incision, Resection, and Replacement of the Diaphragm

The fan-shaped muscle of the diaphragm arises from the internal circumference of the thorax, with attachments to the sternum, the lower six or seven ribs, and the lumbar vertebral bodies. The muscle fibers also attach posteriorly to the aponeurotic arch of the ligamentum arcuatum externum, which overrides the psoas and quadratus lumborum muscles (Fig. 149-1). Laterally, the fibers of the diaphragm interdigitate with slips from the transversalis muscle of the abdomen to originate from the ribs.¹ The right crus is larger and longer than the left and arises from the bodies of the upper three or four lumbar vertebrae. The left crus arises from the upper two lumbar vertebral bodies.

There are three natural openings within the diaphragm (Fig. 149-2). The aortic opening is the most posterior of the three and is formed from fibers comprising the right and left diaphragmatic crura.¹ This tunnel is actually behind the diaphragm, not within it, and contains the aorta, azygos vein, and thoracic duct. The esophageal hiatus is slightly more ventral in relation to the aortic hiatus and consists of fibers passing between the aorta and the esophagus toward the right crus, as well as fibers converging on the pericardial tendon. The opening of the inferior vena cava lies within the confluence of the tendons of the right hemithorax and the tendon beneath the pericardium.

The muscular diaphragm acts as a boundary between the positive pressure abdominal cavity and the negative pressure thoracic cavity. Although diaphragmatic disease is infrequent, exposure to the diaphragm is commonplace, because it is visualized during every thoracic surgical procedure and most intraabdominal operations. Therefore the basic principles advocated by this chapter can be verified in the operating room. The diaphragm makes a good fence, but neighbors on both sides of that fence should know its anatomy, physiology, and surgical principles of resection and repair.

A number of incisions in the diaphragm are possible once the location of the nerve and vessel branches have been learned. These structures frequently lie within the muscle itself and are not seen on the cranial surface of the structure. Therefore, the concept of a neurovascular “manacle” around the junction of the central tendon to the muscle is a very helpful visual mnemonic.

The phrenic nerve originates from the C3, C4, and C5 nerve roots and then enters the chest anterior to the subclavian artery. On the left-hand side, the nerve lies medial to the internal mammary (thoracic) artery 64% of the time, and on the right-hand side, it lies medial to the internal mammary artery only 46% of the time (Fig. 149-3).² Thus the left nerve is more prone to injury during mobilization of the left internal mammary artery through a median sternotomy incision.

While the origin of the phrenic nerve and its proximal course through the mediastinum are well known, the distal extent of the nerve as it branches into the diaphragm proper is less well described. In 1956, Merendino et al.³ published the most descriptive study regarding this intradiaphragmatic portion of the phrenic nerve. Their anatomic findings and drawings are based on electrical stimulation studies and gross dissection in dogs as well as intraoperative dissection of approximately 40 human diaphragms.

The phrenic nerve usually divides at the level of the diaphragm or just above it. The right phrenic nerve enters the diaphragm just lateral to the inferior vena cava within the central tendon. The left phrenic nerve enters lateral to the left border of the heart just anterior to the central tendon within the muscle itself.

The intradiaphragmatic course of the phrenic nerve can be predicted, even when not directly seen, by knowing the distribution of the four main motor divisions (Fig. 149-4). The phrenic nerve first splits into an anterior and posterior trunk. The anterior trunk subsequently divides into a sternal and anterolateral branch near the anteromedial border of the central tendon. The posterior trunk likewise divides into a crural and posterolateral branch along the posteromedial border of the central tendon. The sternal and crural branches are short and continue to run in an anteromedial and posteromedial direction, respectively. The anterolateral and posterolateral branches are much longer and run close to the muscular fiber insertions into the central tendon. These two branches innervate the majority of the diaphragm. Their anatomic relation to one another is often described as a pair of handcuffs or manacles. Often these branches are within the muscle layers and are not readily visible.

The superior phrenic arteries are located on the thoracic surface of the diaphragm (Fig. 149-5). These represent small branches from the lower thoracic aorta and traverse the posterior diaphragm over the top portion of each crus close to the mediastinum.¹ They terminate in small anastomoses with the musculophrenic and pericardiophrenic arteries, which are both branches from the internal mammary artery. These latter two arteries also supply blood to the phrenic nerve and the pericardial fat pad.⁴

The inferior phrenic arteries lie on the undersurface of the crus and the dome of the diaphragm (Fig. 149-6). These are small, paired vessels with frequent anatomic variations. They can originate separately from the aorta above the celiac artery. Alternatively, a common trunk arising from either the aorta or the celiac artery gives rise to these two arteries. Occasionally, one vessel will originate from the aorta, whereas the other emerges from one of the renal arteries. The inferior phrenic arteries then course obliquely superior and lateral along the inferior surface of the diaphragm. The left phrenic artery passes posterior to the esophagus and then runs anteriorly along the lateral side of the esophageal hiatus. The right inferior phrenic artery passes behind the inferior vena cava.¹

Close to the posterior aspect of the central tendon, both the left and right inferior phrenic arteries divide into a medial and lateral branch. The medial branch extends anteriorly, close to the mediastinum. Branches of this vessel traverse the muscular portion of the diaphragm to anastomose with the musculophrenic and pericardiophrenic arteries. The lateral branch of the inferior phrenic artery courses laterally and forms anastomoses with the lower intercostal arteries. The left inferior phrenic artery provides a minor contribution to the blood supply of the lower esophagus. Both the right and left inferior phrenic arteries have branches to the ipsilateral suprarenal gland. These branches are called the right and left superior suprarenal arteries.¹

In general, the venous anatomy in this region parallels that of the arteries. The superior phrenic veins are small and drain anteriorly to the internal mammary vein. The much larger inferior phrenic veins parallel the course of the inferior phrenic arteries. The right vein empties directly into the inferior vena cava. The left vein usually has two branches, one of which drains into the left renal or suprarenal vein and the other of which passes anterior to the esophageal hiatus and empties into the inferior vena cava.¹

Diaphragmatic incisions should be placed to avoid major branches of the arteries and nerves. Since the neurovascular bundles are swinging around the edge of the central tendon, incisions should avoid those areas except at the posterolateral edge of the tendon (the open area of the handcuff, Fig. 149-7). Incisions that cross major neurovascular bundles can be expected to result in bleeding, structural weakness, and partial diaphragmatic paresis.

Diaphragmatic incisions can be divided into three groups: circumferential, central tendon, and radial.

Circumferential

Circumferential incisions in the periphery result in little loss of function. These circumferential incisions, however, should lie at least 5-cm lateral to the edge of the central tendon to avoid the posterolateral and anterolateral branches of the phrenic nerve. These incisions can be difficult to correctly realign after a long operation. Placing surgical clips on each side of the muscular incision can greatly facilitate the correct spatial orientation on closing (see Fig. 149-7). Alternatively, a stapler can be used to divide the muscle, and these staple lines can greatly facilitate reapproximation of the muscle.

Closing suture should be a strong grade to withstand the force of a cough. This can include a monofilament such as 0-Prolene or a braided suture such as 0-Ethibond. Pledgets can help the closure if the muscle is fraying during closure. The incisions can be difficult to close in the face of truncal obesity if the abdominal contents are under pressure. Displacement of the central tendon caudally (toward the feet) in a vigorous manner can produce a nicely approximated edge of muscle that facilitates closure.

Central Tendon

Incisions in the central tendon, as far centrally as within 2 cm of the entrance of the phrenic nerve, do not interrupt any major branch of the nerve itself. This type of incision can provide excellent visualization of the abdomen from the thorax, and vice versa. These incisions are easy to open and close (Fig. 149-8). In general, we recommend that the incision be oriented toward the posterolateral portion of the central tendon if the incision needs to be opened further, as this represents the open area of the manacle, and thus, has the least chance of injuring a neurovascular branch.

Radial

A transverse radial incision made from the posterolateral portion of the tendon and moving centrally is relatively safe because it courses between the distal aspects of the anterolateral and posterolateral branches of the phrenic nerve (i.e., through the opening of the “handcuffs”) (Fig. 149-9). The lateral part of this incision roughly correlates to the line of the tip of the scapula along the chest wall.

Radial incisions from the costal margin extending all the way to the esophageal hiatus have previously been advocated for thoracoabdominal incisions and resection of the GE junction. This incision, however, may result in segmental diaphragmatic paralysis if the incision transects the crural or posterolateral branches of the phrenic nerve (see Fig. 149-9).

Pleural and Peritoneal Attachments

The pleurae are tightly adherent to the top surface of the diaphragmatic central tendon and most of the musculature. It is impossible to separate the pleura from the central tendon of each hemidiaphragm. As each pleura curves off the chest wall and folds back on the surface of the diaphragm, there is a circumferential diaphragmatic recess of approximately 1 cm that does not contain pleura (Fig. 149-10).⁵

The peritoneum is less adherent to the undersurface of the diaphragm and can be bluntly mobilized off the diaphragm during extraperitoneal approaches to the abdominal aorta. The plane of dissection lies between the inferior phrenic artery and vein on the muscle side and the peritoneal membrane. The peritoneum separates from the central tendon of the right diaphragm to form the falciform ligament and produces an area directly under the central tendon that does not have peritoneal covering. This is known as the bare area (Fig. 149-11).

Partial diaphragmatic resections are necessary to remove tumors that have invaded a portion of the diaphragm. The redundancy of the muscle frequently permits primary repair for small to modest resections. Larger defects are easily repaired with the use of a mesh or impermeable graft sutured to the remnant of muscle. We use mesh for patients with lung tissue remaining in the ipsilateral hemithorax, but impermeable grafts for patients who have had a pneumonectomy. The impermeable patches prevent fluid shifts between the thorax and abdomen.

Complete diaphragmatic resection may be required for large tumors invading the diaphragm, such as lung cancer of the lower lobe or sarcomas of the chest. We have gained extensive experience with complete diaphragmatic resection in the course of developing the extrapleural pneumonectomy for mesothelioma.⁵

An extrapleural pneumonectomy is the complete removal of the pleural envelope and all its contents, including the ipsilateral lung, lateral pericardium, and underlying diaphragm. Because the pleura cannot be separated from the central tendon of the diaphragm, the diaphragm must be resected if the pleural envelope is to be kept intact during removal.

Diaphragmatic resection begins with the traction of the pleura away from the chest wall deep into the diaphragmatic sulcus. This exposes the bare area of the lateral diaphragm where the pleura folds off the ribcage and back onto the upper surface of the diaphragm (see Fig. 149-11). The division of these lateral radial bands of the fan-shaped portion of the diaphragm is started at the most anterior portion of the chest close to the pericardium. The fingers of the surgeon bluntly dissect the peritoneum from beneath the muscle, then pull the fibers taut to facilitate visualization. The muscle is generally divided with cautery. It is not unusual for the posterolateral portion of the diaphragm to be beyond the direct vision of the surgeon. Fibers in this area can be bluntly avulsed with minimal risk of bleeding. Once the ligamentum arcuatum externum (external arcuate ligament) is reached in the paravertebral sulcus, the perinephric fat of Gerota fascia, and not the peritoneum, is directly beneath the fan-shaped muscle. This part of the dissection quickly progresses to the lateral margin of the crus. The diaphragm can then be separated from the peritoneum up toward the lateral border of the pericardium. Defects in the peritoneum are closed as they are recognized.

The phrenic nerve is divided. The trileaflet of the diaphragmatic tendon is divided along the line demarcating the central tendon of the ipsilateral muscle from the tendon lying beneath the pericardium. This cut is made medial to the insertion of the phrenic nerve into the anterior muscle. This medial cut is extended along the fused portion of diaphragmatic tendon and pericardium to the inferior vena cava on the right, or the esophageal hiatus on the left.

The only attachment of the diaphragm remaining is the crus. Blunt dissection of the pleura of the deep diaphragmatic sulcus needs to be completed before division of the crus to prevent buttonholing the inferior extent of the posterolateral pleura.

The superior phrenic arteries are surgically inconsequential and rarely identified. The inferior phrenic vessels, however, lie on the deep surface of the crus and are easily seen and ligated. These vessels may bifurcate low over the crus, and a second branch may therefore be found after ligation of a branch thought to be the main trunk. The left inferior phrenic vein usually has two branches, one of which drains into the left renal or suprarenal vein and another that passes anterior to the esophageal hiatus and empties into the inferior vena cava. The right inferior phrenic vein empties directly into the inferior vena cava and therefore requires careful dissection and ligation. Vigorous lateral traction can avulse this vessel from the inferior vena cava, close to the insertion of the hepatic veins. Once these vessels have been divided, the crus is easily divided. This completes the diaphragmatic resection.

The postpneumonectomy space fills with fluid. To prevent fluid shifts between the thorax and abdomen, we use a 2-mm impermeable Gore-Tex prosthetic patch to reconstruct the resected diaphragm. This patch prevents herniation of abdominal contents into the chest, holds the abdominal viscera out of the thoracic radiation field, and also bolsters the contralateral diaphragm by fixing the medial edge of the fan into place. This then facilitates the function of the opposite diaphragm by allowing its central tendon to become the anchor point for the lateral fan fascicles. Without patching the ipsilateral diaphragmatic defect, the contralateral muscle function is compromised.

After the patch has been cut to the shape of the removed diaphragm, the medial edge is sewn to the pericardial tendon with a soft nonabsorbable stitch. We prefer 0-Ethibond for this suture. This suture line runs from the free edge of the divided anterior fan muscles, along the pericardial edge, to either the inferior vena cava or esophageal hiatus. A reliable lateral anchorage system has been devised, requiring a sterilized leatherworking awl. Loops of suture material that have been passed through the lateral edge of the patch are then brought through the chest wall with the awl. The sutures are then passed through a small postage stamp–sized patch of the same material, as well as a sterile plastic button, with the assistance of two angiocaths. The loop of suture is then tied down to itself onto the button, resulting in excellent lateral displacement of the patch.

The posterior mediastinum between the thoracic spine and the inferior vena cava or esophagus is the area where patch ruptures occur, with abdominal contents herniating into the chest. This is due to a lack of strong mediastinal tissue available to anchor the patch. Our group of surgeons have developed the following three potential solutions: (1) a suture anchoring the patch to the anterior spinal ligament, (2) a tongue of extra patch material folded inferiorly along the lumbar spine in simulation of the diaphragmatic crus, and (3) a composite of two patches of 2-mm Gore-Tex stapled together in the middle with a thoracoabdominal (TA) stapler to create a dynamic patch at the center with less tension at the lateral suture lines. The first technique uses the dense spinous ligament to anchor the posterior mediastinal portion of the patch and decreases the free defect between the anterior suture line at the inferior vena cava and the thoracic spine to a few centimeters. The second technique allows the medial portion of the patch to partially displace into the chest, but prevents visceral herniation unless the entire tongue becomes displaced into the chest. The last technique allows the prosthetic patch to “give” without rupture if the patient experiences abdominal distention.

Diaphragm incisions are straight forward, but require the surgeon to have an understanding of the course of the neurovascular bundles of the phrenic nerve. These branches frequently run on the undersurface of the muscle. Circumferential and central tendon incisions are generally safe. Radial incisions should be oriented to pass between the open arms of the anterior and posterior branches of the phrenic nerve in a posterolateral manner (toward the line of the tip of the scapula).

Diaphragms can be partially or completely resected. Muscle resections require the surgeon to have an understanding of the crural anatomy, the pleural attachments, and the peritoneal attachments. Particular attention should be made to the branches of the phrenic vessels, especially the venous branches draining the hepatic veins. A clever system of attaching the prosthetic patch to the lateral chest wall has been developed by Sugarbaker et al. That technique is described in this chapter.