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The differences in histological changes among pulmonary vessels divided with an energy device
Abstract
Tomoharu Yoshiya, Takahiro Mimae, Norifumi Tsubokawa, Shinsuke Sasada, Yasuhiro Tsutani, Kei Kushitani, Yukio Takeshima, Yoshihiro Miyata, Morihito Okada
INTRODUCTION MATERIALS AND METHODS
Interactive CardioVascular and Thoracic Surgery, ivy072, https://doi.org/10.1093/icvts/ivy072 Published: 16 March 2018 Article history
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CONCLUSIONS
Abstract
ACKNOWLEDGEMENTS
OBJECTIVES
REFERENCES
Histological changes after division of the pulmonary artery (PA) and the pulmonary vein (PV) using a vessel-sealing device are Comments (0)
not fully understood. The goal of the present study was to clarify histologically and immunohistochemically how division with the device affects the wall layers of the pulmonary vasculature.
METHODS This prospective cohort study analysed outcomes of 20 patients who underwent anatomical lung resection. After a single proximal ligation, the PA and the PV (diameter 2–7mm) were divided using a LigaSure Blunt Tip (LSB). Histological findings and thermal damage were evaluated in vascular specimens from resected lungs.
RESULTS The PA has a well-developed media with rich elastic fibres and a thin adventitia, whereas the PV has a thinner media and a thicker adventitia with abundant collagen fibres. Vascular division of the PAs and PVs appeared complete to the naked eye. However, in all divided PAs, the area adjacent to the sealed zone comprised only adventitia and thin disrupted media. Additionally, thermal energy generated by the LSB resulted in a wide area of thermal necrosis over the histologically fragile region in all cases. Conversely, the wall layers of all divided PVs were completely fused without disruption. Thermal spread and disruption did not significantly differ between small (2–4mm) and large (5–7mm) PAs [187 (150–253) vs 236 (190–275) µm, P=0.22; 180 (138–200) vs 210 (161–305) µm, P=0.22]. Histological changes differed significantly between the pulmonary vessels after division using the LSB.
CONCLUSIONS Surgeons should consider that dividing the pulmonary vessels with a vessel-sealing device might have more histological impact on the layers of the wall of the PA than on those of the PV, although it remains unclear whether these findings constitute a clinical risk.
Keywords: Histological changes , Pulmonary vessels , Vessel-sealing device Topic: pulmonary artery stenosis, pulmonary artery, lung, ventricular tachycardia, induced, heart valve bioprosthesis stenosis, collagen, p-aminosalicylic acid, pulmonary veins, lung volume reduction, aminosalicylic sodium, devices, medical, elastic fibers, adventitia, diameter Issue Section: Original Article
INTRODUCTION Early-stage lung cancers are now being diagnosed at a higher frequency than ever before due to the prevalence of computed tomography screening and advances in high-resolution computed tomography [1, 2]. Early diagnosis has led to widespread thoracoscopic surgery to treat early-stage non-small-cell lung cancer [3–5]. Furthermore, the incidence of radical segmentectomy for small lung cancers, which is often needed to treat the small pulmonary vessels, has increased. Open and endosurgical stapling devices have become the standard instruments for closing the large pulmonary vessels [6], whereas the small pulmonary vessels are manually ligated with a suture or divided using a vessel-sealing device (VSD). Advanced bipolar and ultrasound technologies are still being evaluated in various trials [7–9]. Safe division of the pulmonary vessels, especially the pulmonary artery (PA), during anatomical lung resection, is critically important. Few studies of the pulmonary vasculature divided using a VSD have compared structural differences and histological changes between the PA and pulmonary vein (PV). Lesser et al. [10] histologically assessed the PA after division using the LigaSure (LS). They stained vessel specimens from resected lungs with haematoxylin and eosin (HE). However, data derived using immunohistochemical and other histological stains such as the Elastica van Gieson (EVG) stain are scant. Therefore, the present study was designed to define structural differences between the PA and PV and to histologically and immunohistochemically clarify how division with a VSD affects wall layers of the pulmonary vessels.
MATERIALS AND METHODS The objective of this prospective cohort study was to define histological changes of the PA and PV (2–7mm) divided with a LigaSure Blunt Tip (LSB) (Covidien, Neustadt, Donau, Germany). The Force Triad energy platform (Covidien) was set at an intensity of 2 bars. All patients scheduled for anatomical lung resection for primary lung cancer or metastatic lung tumour at the Hiroshima University Hospital were approached to enrol in the study. The exclusion criteria were age <20years, inability to consent to the study and undergoing preoperative radiation or chemotherapy. The institutional review board at Hiroshima University approved the study (eki 899), and all patients provided written informed consent to participate. One surgical team operated via a hybrid video-assisted thoracic surgery approach according to standard operating procedures, and the intraoperative techniques did not differ from standard resection procedures. Both the PA and PV were proximally ligated with suture material and then divided distally using the LSB. Of 20 patients, 8 were treated by segmentectomy and 12, by lobectomy. Large vessels (≥8mm in diameter) were divided with an endostapler. A combination of the endostapler and the LSB was used for the patients having a lobectomy and the LSB only was used for the patients having a segmentectomy. All specimen manipulations proceeded according to strict guidelines. The diameters of the vessels were measured immediately after the lungs were retrieved from the vessel adventitia to the adventitia exvivo using a caliper before formalin fixation in the operating room. Under the direct supervision of the attending thoracic surgeons, care was taken not to influence the pathological integrity of the resected lesions and their surrounding tissues and lymph nodes. Vessel stumps (22 PAs and 21 PVs) obtained from the resected lungs were fixed in 4% formalin, sectioned and stained with HE, EVG, Masson’s trichrome (MT) and -smooth muscle actin (-SMA) antibody using standard procedures (Table 1). Elastic fibres stained black and purple, and collagen fibres stained pink with the EVG stain. Brown smooth muscle cells were immunohistochemically detected using anti--SMA antibody Clone 1A3 (DAKO, Glostrup, Denmark). Smooth muscle cells stained red, and collagen fibre and fibrils stained light blue with MT. The length of disruption was measured from the edge of the sealed zone to the farthest point of disrupted media of the PA. Thermal spread on the PA and PV was also measured from the edge of the sealed zone to the farthest area stained red with MT. The length of the disruption and the thermal spread were analysed using the Wilcoxon rank sum test. Data for all patients were collected from electronic medical records.
Table 1: Characteristics of specific stains and pulmonary vessels Stain
Target
Colour
Elastica van Gieson
Elastic fibre
Black and purple
Collagen fibre
Pink
-smooth muscle actin
Smooth muscle cell
Brown
Masson’s trichrome
Smooth muscle cell
Red
Collagen fibre
Light blue
Pulmonary artery diameter (mm)
n=22
2
3
3
6
4
4
5
3
6
3
7
3
Pulmonary vein diameter (mm)
n=21
2
3
3
3
4
5
5
4
6
3
7
3
RESULTS Table 2 shows the clinicopathological characteristics of the 20 (men, n=12; women, n=8) patients (median age 70years; range 41– 89years). None of them had symptoms suggesting pulmonary hypertension or severe complications such as interstitial pneumonia, cystic fibrosis, chronic obstructive disease, heart disease and systemic vascular disease. Echocardiographic or radiographic findings were essentially unremarkable in all patients. The major histological type was adenocarcinoma followed by squamous cell carcinoma. All anatomical lung resections were straightforward with no intraoperative dehiscence or bleeding from the PA and PV. Repeated surgery for postoperative haemorrhage was not required, and no other severe complications arose. We divided 22 PAs and 21 PVs ranging from 2 to 7mm in diameter (Table 1).
Table 2: Clinicopathological characteristics of the patients
Patients (n=20)
Median age (years), (range)
70 (41–89)
Male gender
12
Procedure
Segmentectomy
Right
3
Left
5
Lobectomy
Right
7
Left
5
Histology
Adenocarcinoma
15
Squamous
3
Combined small
1
Metastatic tumour
1
Pathological stage
IA
10
IB
3
IIA
2
IIB
3
IIIA
1
Intraoperative bleeding from divided pulmonary vasculature
None
Median blood loss (ml)
48
Blood transfusion
None
30-Day postoperative bleeding
None
Structural differences between the PA and PV were clarified using various stains (Figs 1 and 2). The intima of the PA seemed to thicken with age (Fig. 1A–D). The first layer of concentric elastic fibres in the PA is the internal elastic lamella that surrounds the lumen (Fig. 1A and C). The media of the PA included rich elastic fibres that stained black and purple with the EVG stain (Fig. 1C). Moderately developed smooth muscle cells that stained brown with -SMA antibody were interwoven among the elastic fibres (Fig. 1B and C). Collagen fibrils stained light blue with MT were located among the red smooth muscle cells (Fig. 1D). The media was delineated on the inside and outside by internal and external elastic lamellae. The adventitia outside the external elastic lamella consisted of thin collagen fibres that stained light blue with MT (Fig. 1D). In contrast, the PV comprised a thinner media and a thicker adventitia with abundant collagen fibres compared with the PA (Fig. 2).
Figure 1:
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Normal structure of the pulmonary artery. Staining with haematoxylin-eosin (A), -smooth muscle actin antibody ( B), Elastica van Gieson (C) and Masson’s trichrome (D). Arrowheads indicate the internal elastic lamella. Double-headed arrow indicates the media. The pulmonary arterial media consists of moderately developed smooth muscle cells (B) and abundant elastic fibres (C). The relatively thin adventitia consists of collagen fibres (D). Magnification in all panels, ×40.
Figure 2:
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Normal structure of the pulmonary vein. Staining with haematoxylin-eosin (A), -smooth muscle actin antibody ( B), Elastica van Gieson (C) and Masson’s trichrome (D). The double-headed arrow indicates the media. The pulmonary vein comprises thinner media (B, C) and thicker adventitia with abundant collagen fibres (D). Magnification in all panels, ×20.
The intima and much of the disrupted media had invaginated into the lumen of all PAs (Fig. 3A–F). The adventitia and a little media remained at the sealed zone (Fig. 3C and E). The area adjacent to the sealed zone comprised only adventitia and thin media (Fig. 3B and D–F). Thermal energy generated by the LSB caused thermal necrosis of fragile areas stained red with MT (Fig. 3F). In contrast, all PVs were completely fused after sealing with the LSB (Fig. 4A–F), and fragile areas were not found in the vicinity of the sealed zones, although the adventitia was thermally damaged (Fig. 4F).
Figure 3:
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Histological findings of the pulmonary artery divided with an energy device. Staining with haematoxylin-eosin, ×20 (A), ×100 (B); Elastica van Gieson, ×20 (C), ×100 (D); -smooth muscle actin antibody, ×40 ( E); Masson’s trichrome, ×40 (F). The singleheaded arrow indicates the sealed zone, which comprises the adventitia and some media (A, C and E). The intima and the most disrupted media have invaginated into the lumen (A–F). The double-headed arrow indicates the area adjacent to the sealed zone, which consists of a small amount of media and thin adventitia (B, D, E and F). The red area stained with Masson’s trichrome indicates thermal damage (F).
Figure 4:
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Histological findings of the pulmonary vein divided with an energy device. Staining with haematoxylin-eosin, ×20 (A), ×40 (B); Elastica van Gieson, ×20 (C), ×40 (D); -smooth muscle actin antibody, ×40 ( E); Masson’s trichrome, ×40 (F). The pulmonary vein has a much thicker adventitia, and is completely fused without disrupted or vulnerable areas despite the thermal effects (A–F). Double-headed arrow indicates the intima and the media (B, D, E and F).
Thermal spread did not significantly differ between the PA and PV [220 (140–275) vs 225 (173–347) µm, respectively, P=0.32; Fig. 5A]. The median length of the disrupted PA media was 190 (116–305) µm (Fig. 5B). Thermal spread and disruption did not significantly differ between small (2–4mm) and large (5–7mm) PAs [187 (150–253) vs 236 (190–275) µm,
P=0.22; 180 (138–
200) vs 210 (161–305) µm, P=0.22; Fig. 5C and D]. There was no difference in thermal spread between small (2–4mm) and large (5–7mm) PVs [208 (173–227) vs 272 (190–347) µm, P=0.18; Fig. 5E]. Conversely, fragile areas were not evident in PAs divided after manual ligation with suture material without using the LSB (Fig. 6).
Figure 5:
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Box plot comparisons of histological changes induced by an energy device. (A) Thermal spread in pulmonary arteries and veins: 220 (140–275) vs 225 (173–347) µm; P=0.32. ( B) Length of disruption in pulmonary arteries and veins: 190 (116–305) vs 0µm; P =not calculated. (C) Thermal spread between small (2–4mm) and large (5–7mm) pulmonary arteries: 187 (150–253) vs 236 (190–275) µm; P=0.22. ( D) Length of disruption between small (2–4mm) and large (5–7mm) pulmonary arteries: 180 (138–200) vs 210 (161–305) µm; P=0.22. ( E) Thermal spread between small (2–4mm) and large (5–7mm) pulmonary veins: 208 (173– 227) vs 272 (190–347) µm; P=0.18.
Figure 6:
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Pulmonary artery (7mm) divided after suture ligation without the LigaSure Blunt Tip. Staining with haematoxylin-eosin, ×40. Arrowhead points to suture material.
DISCUSSION Histological and immunohistochemical stains revealed histological fragility with thermal damage on the wall layers of all PAs after division with the LSB. The intima and much of the disrupted media had invaginated into the lumen. Bipolar electrosurgical radiofrequency energy caused thermal damage on the area adjacent to the sealed zone that comprised only adventitia and thin media. In contrast, the wall layers of all PVs were fused without disruption and invagination, and the area adjacent to the sealed zone seemed robust. Lesser et al. [10] used only HE stain to evaluate the PA after division with a LS and found disruption and invagination in all divided PAs. They also noted that the LS sealed only the adventitia of the PA. However, we found that part of the media remained at the sealed zone, which was stained with -SMA and EVG stain. Electron microscopic findings of PA branches sealed with Harmonic Ace+ Shears in a human ex vivo model demonstrated various microscopic sealing patterns [7]. One-third of the sealed PAs presented invagination of the media and absence of melting. The frequency of incomplete fusing might be higher in an in vivo model with pulsatile PA blood flow because the PAs obtained from resected lungs were inflated with normal saline and were sealed ex vivo unlike in the present study. These findings indicate that any VSD could cause the invagination of the disrupted wall layers. Thermal spread caused by Harmonic Ace, LigaSure V, EnSeal and Thunderbeat was examined in the abdominal muscular artery of 10 female Yorkshire pigs [11]. Milsom et al. reported that thermal spread, which was defined as the width of collateral denatured tissues in grasped vessels on both sides of the instrument jaw, was <2mm with any VSD and was the lowest for the Harmonic Ace and Thunderbeat instruments, probably because of rapid ultrasonic dissection. Additionally, larger vessels had significantly more thermal spread. Our quantitative assessments of thermal spread between small and large divided PAs did not differ, which might have been associated with the small sample. Disruption of the media in the PA could be partially due to the fact that they function as an auxiliary pump like other elastic arteries and have a specialized anatomy. The media of the PA mainly contains elastic fibres, smooth muscle cells and Types I and III collagen fibrils [12]. These fibrils in the media are circumferentially oriented and play an important role in maintaining the mechanical properties of primary load-bearing vessels. Types I and III collagen connect elastic fibres with smooth muscle cells. Reduced amounts of Type III collagen [13] and abnormal fibrillin production [14] are associated with the development of aortic dissection in patients with Ehlers–Danlos syndrome Type IV. An animal model of this syndrome with a mutation of the gene encoding Type III collagen had no collagen fibrils, and the major vessels tended to rupture [15]. Lesser et al. [10] speculated that excessively high pressure during closure using the LS crushes vascular walls and thus causes disruption and invagination of the PA walls. Additionally, our findings indicate that the thermal energy of a VSD might play an important role in dissecting the collagen network and cause tears in the media. Developmental differences between the PA and other elastic arteries should be considered to understand the vulnerability of the PA. A linear correlation between the internal diameter of the pulmonary trunk and the left and right PA and body length was identified [16]. However, the thickness of the media and the packing density of the elastic fibres in the media of the 3 vessels did not increase along with an increase in the internal diameter during physiological development [17]. In contrast, those of the ascending aorta increased linearly along with a concomitant increase in blood pressure and internal diameter [18]. Those of the pulmonary trunk in children with pulmonary hypertension who underwent transposition of the great arteries also adapted to high pressure like the aorta [19]. Therefore, the structural features of the PA at birth would apparently be maintained by low pressure combined with increased blood flow. The PA sealing study in an ex vivo human model showed that patients with higher PA pressure had higher bursting pressure after vascular energy sealing [8]. This finding suggests that the media became thicker due to prolonged increased intraluminal pressure. Two intraoperative partially dehisced PVs were described by Schuchert et al. [20], which were divided with a LigaSure Impact (Dolphin tip), which has a smaller curved jaw that produces a 3.3- to 4.7-mm seal. They considered that the causes were comparatively thinner vessel walls and associated reduced collagen content of the PV. However, we showed here that all PVs have thicker adventitia comprising abundant collagen fibres. After the dehiscences in the initial 12 patients, they used a LS Atlas with a larger jaw, applying a 6-mm wide seal for the next 199 patients, and no arterial and venous dehiscence occurred. Tsunezuka et al. [21] described intraoperative bleeding 20min after LS sealing of a left A
1+2
a+b (diameter: 7mm). They concluded that sealing
under wet surroundings resulted in a 1-mm unsealed portion at the edge and that contact with a suction device caused intraoperative bleeding. Liberman et al. [8] compared the ability of 4 contemporary energy sealing devices to seal the PA in a human ex vivo model. Two sealing failures with the LS and the EnSeal were manifested by leakage immediately after dividing the PAs (diameter: 6.78mm, 8.3mm, respectively). Goudie et al. [22] examined PA sealing using a Harmonic Ace +7 during a video-assisted thoracic surgery lobectomy in a canine survival model. One 10-mm PA branch had a partial sealing failure immediately at the time of sealing, although a resealing at the stump using the device was successful. Suture ligation of the PA could also result in disruption due to small changes in tension or force vectors. Therefore, we attempted to sample some PAs divided only with a suture ligation during this study. Histological evaluation of a few large (diameter 7mm) PAs that we were able to assess showed that the area adjacent to the ligated zone was intact. However, it was extremely challenging to obtain evaluable specimens of small arteries, so the most effective method of dividing the PA—a suture ligation or a VSD—remains controversial. On the other hand, our histological findings and quantitative assessments revealed that thermal damage and disruption could extend to the trunk of the PA if the proximal stump of a divided PA branch was contiguous with the trunk. To avoid damage to the PA trunk, surgeons should apply VSD at a sufficient margin from the root of the PA branch because intra- and postoperative bleeding caused by an injury to the PA trunk can be catastrophic. In addition, adding a proximal ligation with absorbable suture materials that cause less inflammation and granuloma at arterial tissues around ligations [23] might be acceptable, considering the patient’s age, complications and whether to take a steroid or an anticoagulant.
Limitations The present histological study evaluated the distal stumps of 22 PAs and 21 PVs after division with a single commercial product, the LSB, and burst pressure was not measured. Additionally, we did not demonstrate histological changes and differences between the pulmonary vessels in an animal model of long-term survival. Whether or not sealed PVs are less fragile than sealed PAs could not be definitively concluded from histological findings alone. Larger samples with all energy devices in a uniform population will be needed in future studies.
CONCLUSIONS Histological changes significantly differed between the pulmonary vessels after division with the LSB. It remains unclear whether these findings indicate a clinical risk. However, surgeons should consider that dividing pulmonary vessels with VSDs might have more histological impact on the layers of the wall of the PA than on those of the PV.
ACKNOWLEDGEMENTS We appreciate the important contributions of Takeshi Mimura and Masaoki Ito to data analysis. Conflict of interest: none declared.
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