Pico₂ Monitoring of Transferred Jejunum Perfusion Using an Air Tonometry Technique After Hypopharyngeal Cancer Surgery

Abstract

This study aimed to investigate the usefulness of intraluminal Pco₂ (Pico₂) monitoring by air tonometry for the assessment of the vascular condition of the transferred jejunum after surgery for hypopharyngeal cancer.

Pico₂ in the transplanted jejunum of 24 patients was monitored using air tonometry after radical surgery for hypopharyngeal cancer from 2003 to 2010.

All but 1 patient, who removed the catheter before monitoring began, were monitored safely. Pico₂ in the transferred jejunum correlated with arterial Pco₂ (Paco₂) that was measured concurrently, and dissociation of Pico₂ from Paco₂ was observed in cases with vascular complication. In those cases without postoperative vascular complication, the Pico₂ value gradually increased for 3 hours but then decreased by 12 hours after surgery. Three patients experienced major vascular complication. All 3 patients had continuous elevation of Pico₂ >100 mm Hg, although vascular flow in 1 patient recovered by removal of a venous thrombosis and reanastomosis of the vein 7.5 hours after surgery. Four other patients who experienced elevation of Pico₂ had their skin suture released for decompression of their neck wound, resulting in a decrease in Pico₂ after treatment.

The current results demonstrated that continuous monitoring of Pico₂ by air tonometry accurately reflects the vascular condition of the transferred jejunum, and this method is one of the best options for postoperative monitoring of jejunum blood perfusion.

INTRODUCTION

Regardless of the development of multidisciplinary treatment, including chemoradiation or radiotherapy, either with or without surgery, advanced-stage hypopharyngeal cancer is associated with a poor prognostic outcome, and the 5-year survival rate of this disease remains below 50%.^1,2 Total pharyngolaryngectomy (TPL) or total pharyngolaryngoesophagectomy (TPLE) followed by reconstruction using free jejunum transfer is one of the standard treatments for advanced hypopharyngeal cancer and cervical esophageal cancer. In recent years, salvage surgery is often necessary for patients who fail after radiotherapy or chemoradiotherapy, which increases the surgical and postsurgical risk of complication. About 5% of patients still experience failed pharynx reconstruction, mostly due to vascular complication.^3–5 Early detection of vascular problems and prompt treatment are critically important because salvage of the transferred jejunum with the removal of thrombosis and reanastomosis is challenging in most cases. The jejunum is intolerant to ischemia because ischemia lasting >3 hours can result in irreversible damage to the jejunum.^6,7 Impaired vascular perfusion of the transferred jejunum may require secondary reconstruction using less suitable vessels, a gastric pull-up procedure to restore a failed jejunum interposition, or establishment of pharyngocervical skin and esophagocervical skin fissures. Patients who undergo these secondary surgeries can be in a more jeopardized situation because of leakage of saliva or digestive juices, leading to a higher risk of infection and delayed wound healing. Thus, accurate blood flow assessment of the transferred jejunum and early detection of insufficient perfusion is crucial for free jejunum reconstruction.

Tonometers, or gastric tonometers, have been developed for monitoring the splanchnic mucosal blood flow and have become extensively employed in clinical practice to monitor critically ill patients.^8,9 Recently, this technique has frequently been used in the detection and assessment of chronic gastrointestinal ischemia.^10–12 Tonometer catheters enable measurement of the pco₂ of the targeted organ by equilibrating the air in a silicone balloon placed on the catheter tip with the target luminal organ filled with secreted intestinal fluids. Formerly, pco₂ was measured using a saline-based method, but, at present, air-based and automated measurement of pco₂, known as air tonometry, is widely available, and this air tonometry technique has the great advantage of easy measurement and eliminating errors in manual fluid tonometry.⁸

Tonometry is considered to be useful in monitoring graft perfusion in an alternative model of intestinal autotransplantation,¹³ and hence we previously reported the usefulness of the saline-based tonometry for monitoring blood flow in the transferred jejunum after TPL or TPLE.¹⁴ This study therefore aimed to investigate the usefulness of intraluminal Pco₂ (Pico₂) monitoring by air tonometry as a new, easy-to-use, and alternative approach to evaluating blood flow in the transferred jejunum.

PATIENTS AND METHODS

Twenty-nine patients underwent total TPL or TPLE for hypopharyngeal cancer from 2003 to 2010. Twenty-five patients had a tonometry catheter (TRIP gastric catheter; GE Healthcare, Helsinki, Finland) inserted through the nose, so that the silicone balloon of the catheter tip was placed in the transferred jejunum during the operation (Figure 1). The catheter was connected to Tonocap (Datex-Ohmeda, Helsinki, Finland), and Pico₂ was measured continually and automatically. Approval of the protocol including the use of clinical data was obtained from our institutional review board. The patients’ consent to undergo Pico₂ measurement was obtained before insertion of the catheter.

FIGURE 1.

(A) Tonometry catheter was inserted through the nostril during surgery. The silicone balloon of the catheter tip was placed in the transferred jejunum. (B) Neck x-ray revealed the correct location of the catheter. White triangles indicate the shape of the silicone balloon, and the arrows indicate the markers of the catheter.

With regard to postoperative management, all patients stayed at least 1 night in the intensive care unit with ventilatory support; 23 cases were maintained under synchronized intermittent mandatory ventilation, whereas 2 cases were maintained under continuous positive airway pressure. Most patients were taken off the ventilator and returned to the general ward the day after surgery. All patients were treated with prostaglandin E1 0.1 μg/kg/min or Lipo-PGE1 120 μg/d for 1 week.

We started measuring Pico₂ after transfer to the intensive care unit. Pico₂ was recorded every hour up to 24 hours after the operation, then every 1 to 3 hours up to 48 hours after the operation, and finally every 3 to 6 hours up to 72 hours after the operation. Arterial Pco₂ (Paco₂) was measured 1 to 10 times, as necessary, during postoperative management.

Based on our previous data,¹⁴ neck skin sutures were removed for decompression of the transferred jejunum when the Pico₂ value exceeded 70 mm Hg. When Pico₂ was >80 mm Hg, we reopened the patient's neck wound to check the condition of the jejunum and vascular anastomosis.

Paco₂ and the corresponding Pico₂ were statistically assessed with regard to their correlation using Pearson correlation test. CO₂ in patients without vascular trouble was analyzed, whereas those with vascular trouble were evaluated individually to review the efficacy of our treatment for the transferred jejunum.

RESULTS

Patients’ Data and Characteristics

One of the 25 patients was excluded because his catheter was pulled out before measurement of Pico₂. Clinical data and Pico₂ values for 24 cases were analyzed. Clinical data of the 24 patients are summarized in Table 1. The average duration of catheter placement was 96 hours (13–135 hours) because 1 patient pulled out the catheter 13 hours after surgery. No problems were observed with regard to measuring Pico₂.

TABLE 1.

Patient's Characteristics

Pico₂ of the Transferred Jejunum Correlates With Paco₂

Pico₂ value is influenced by the respiratory status and blood oxygenation of the patient. The oxygenation level of each patient can be expected to vary because of individual differences in preoperative lung function. Therefore, we at first analyzed the correlation between Pico₂ and Paco₂ that was measured concurrently with Pico₂ measurement. In 17 patients without vascular complication of the transferred jejunum during their postoperation course, Pico₂ correlated significantly with Paco₂ (Figure 2). On the other hand, Pico₂ in patients with vascular trouble and who had skin decompression treatment showed no correlation with Paco₂ (data was not shown). These data suggest that the Pico₂ value reflects the blood flow of the jejunum mucosa in the normal postoperative course, and dissociation of Pico₂ from Paco₂ is a convincing indicator of vascular complication.

FIGURE 2.

Pico₂ and Paco₂ correlated significantly in 17 cases without vascular complication. Paco₂ was measured concurrently with Pico₂. Pico₂ = intraluminal Pco₂.

Pico₂ Measurement Elucidates the Vascular Condition of the Jejunum After Transplantation

This tonometry system enabled monitoring of the oxygenation status of the transferred jejunum automatically and seamlessly, and also enabled us to presume an event happening to the transferred tissue in the postoperative process. Figure 3 exhibits the averages of serial Pico₂ in those cases without postoperative vascular complication. The P_ico₂ value gradually increased for 3 hours, then decreased within 12 hours postoperation. From 12 to 72 hours after surgery, average Pico₂ values were between 40 and 50 mm Hg. Vascular problems after free jejunum transfer mostly ensue within 4 to 72 hours^15,16; thus, the increase in Pico₂ coincided with this hazardous period. This transient increase in Pico₂ may represent a congestion of the transferred jejunum induced by compression of the operated tissue, and this subacute change of operation field has the possibility of increasing risk of blood flow obstruction leading to jejunum necrosis.

FIGURE 3.

In cases without complications, Pico₂ values gradually increased for 3 hours but then decreased up to 12 hours postoperation. From 12 to 72 hours after surgery, the average Pico₂ value was between 40 and 50 mm Hg. Error bars indicate the standard error. Pico₂ = intraluminal Pco₂.

Pico₂ Measurement Enables Vascular Complication of the Transferred Jejunum to be Avoided

Three patients experienced major vascular complications. Pico₂ in all 3 patients was elevated to above 100 mm Hg and their vascular condition was evaluated in the operating room because of such continuous elevation. Jejunum blood flow in 1 patient recovered by removal of a venous thrombosis and reanastomosis of the vein 7.5 hours after the initial surgery (Figure 4A). However, transplants in the other 2 patients needed to be sacrificed (Figure 4B and C). In the patient with vessel reanastomosis, his elevated Pico₂ decreased temporarily after restoration of vessel patency, but started to increase again 12 hours after the initial surgery, but the removal of skin sutures and decompression resulted in normalizing the Pico₂ level. He had no trouble in his postoperative course subsequently (Figure 4A).

FIGURE 4.

Three of the 24 patients experienced major vascular problems. Pico₂ in all the 3 patients rose >100 mm Hg, and their vascular condition was evaluated in the operating room. The white arrows indicate the time at which they returned to the operating room. The transplanted jejunum in 1 patient (A) was rescued by removal of venous thrombosis and reanastomosis of the grafted vein. However, transplants of the 2 other patients (B and C) needed to be sacrificed. In the case with vessel reanastomosis, elevated Pico₂ at one time decreased after restoration of vessel patency but started to increase again at 12 hours after the initial surgery (black arrow). However, removal of the skin suture and decompression resulted in normalizing the Pico₂ level. Pico₂ = intraluminal Pco₂.

Four other patients from among the 24 cases who had elevated Pico₂ had their skin suture released for decompression of the transferred jejunum (Figure 5A–D). Pico₂ in all 4 cases decreased after removal of their skin suture, and they did not experience any postoperative complications, except for 1 patient who experienced salivary leakage and fistula formation that recovered following conservative treatment. The maximum elevation of Pico₂ in these cases was observed about 3.5 to 43 hours after the surgery when it was coincident with the hazardous period of the jejunum transfer. Moreover, Pico₂ elevation started from >12 hours after the surgery in 3 of the 4 patients (Figure 5A, C, and D), which was deviated from normal Pico₂ transition (Figure 3). The Pico₂ transition of these cases indicated that cervical skin suture has the possibility of compressing jejunum perfusion continuously, and removal of the suture and release of the neck wound pressure may improve blood flow in the transferred jejunum.

FIGURE 5.

Four other patients who had elevated Pico₂ had their skin suture released for decompression of the transferred jejunum. Pico₂ in all 4 cases decreased after removal of the skin suture. Black arrow indicates the time at which their skin sutures were removed. Pico₂ = intraluminal Pco₂.

DISCUSSION

Free transferred tissues need to be monitored carefully and accurately since graft failure often leads to severe complications in head and neck cancer patients who often have poor nutrition or are in poor physical condition due to their tumor or previous therapy. TPL with free jejunum transfer is the standard surgical treatment for advanced hypopharyngeal cancer, but monitoring vascular flow in the transferred jejunum is difficult because the transferred jejunum is covered by cervical skin.¹⁵ Two conventional methods for monitoring the buried flap are transcutaneous Doppler ultrasound monitoring of the pedicles¹⁷ and monitoring flap.¹⁸ Even if the experienced surgeon tries to find the pedicle using ultrasonography, it is sometimes impossible to exclude the local vascular system with certainty, which can lead to a misunderstanding of the intestinal blood flow.¹⁵ It is sometimes difficult to use a monitoring flap to estimate the condition of the blood flow because of torsion or tension of the perforator, or an unclear determination of the monitoring flap.¹⁸ Furthermore, the change in color of the jejunum resulting from ischemia requires a long interval after vascular obstruction.¹⁹

The current results demonstrate that continuous monitoring of Pico₂ by air tonometry accurately reflects the vascular condition of the transferred jejunum, and this method is one of the best options for postoperative monitoring of jejunum blood flow. In the present study, Pico₂ of the transferred jejunum correlated significantly with systemic Paco₂ that was measured concurrently. The average Pico₂ value in patients with a normal postoperative course was 45.4 mm Hg, and the dissociation of Pico₂ from Paco₂, together with the continuous elevation of Pico₂, reflected occlusion of the anastomotic vein. The Pico₂–Paco₂ gradient is considered to be the most sensitive and specific parameter of gastrointestinal perfusion, independent of systemic metabolic and respiratory changes.¹⁰ There is no consensus on the normal Pico₂ value for the transferred jejunum and the critical level of Pico₂ indicating mucosal malperfusion. Otte et al¹⁰ reported that the average Pico₂ of healthy volunteers was 4.9 kPa (36.8 mm Hg), whereas Kolkman et al⁸ reviewed the upper limit of normal values for Pico₂ and found it to be 6.5 kPa (49 mm Hg) in the gastric tonometry and 1.2 kPa (9 mm Hg) for the Pico₂–Paco₂ gradient. In an alternative animal model of intestinal autotransplantation, histological change of the intestinal mucosa started to be observed at 11.2 mm Hg of the gradient of Pico₂–Paco₂, and extensive mucosal damage was observed at 32.9 mm Hg.¹³ An increase in Pico₂ of >60 mm Hg indicated the development of compromised perfusion in the series in which saline-based tonometry was employed.¹⁴ From these data and our average Pico₂ data, it is feasible that Pico₂ >60 mm Hg is critical for the transferred jejunum. This Pico₂ measurement by air tonometry is a compelling technique for estimating the blood flow of the transplanted jejunum.

Pico₂ monitoring has the potential to contribute to early detection of vascular complications, which may enable a staged strategy for the graft vessels of the transferred jejunum. In the present study, an elevated Pico₂ level of >60 mm Hg is considered abnormal, and it is highly indicative of vascular complications of the transferred jejunum based on our previous data.¹⁴ In patients with continuous elevation of Pico₂ >70 mm Hg, we decided to remove the surgical skin suture for decompression of the jejunum and their vessels before checking their vessels in the operating room. Intestinal blood flow is vulnerable to the surrounding pressure,²⁰ and one of the main reasons for vascular occlusion after reconstruction surgery is the excessive pressure to the graft vessels caused by a tight wound closure, hematoma, or extrinsic compression from tapes or strips around the neck.^21,22 In this study, the Pico₂ value of those patients with decompressed cervical wound decreased after treatment, and we believe that some of these cases were prevented from having jejunum vascular occlusion. In the case that wound compression is highly predicted, like a patient receiving chemoradiotherapy, the neck wound might be left open to weigh the timing of wound closure based on Pico₂ value. Further accumulation of patient data and a prospective study is needed to clarify whether skin decompression is effective or not, and to determine appropriate criteria for Pico₂ levels in the staged treatment of impaired vascular perfusion of the transferred jejunum.

In conclusion, Pico₂ measurement with a gastric tonometer is useful for monitoring the transferred jejunum blood flow and early detection of vascular complications. As Pico₂ >60 mm Hg is considered to indicate abnormal blood flow of the jejunum, the Paco₂–Pico₂ gap should be assessed, and patients with continuous increase in Pico₂ need to have their graft vessel status checked urgently. Cervical skin decompression may contribute to restoring jejunum perfusion.