vascular flow of the gastric fundus after arterial devascularization: an experimental study

Journal of Surgical Research 152, 128–134 (2009)

Vascular Flow of the Gastric Fundus After Arterial Devascularization:An Experimental Study

Marise Gomes, M.D., Ph.D.,*,† Eduardo Ramacciotti, M.D., Ph.D.,*,†,1 Fausto Miranda Jr., M.D., Ph.D.,‡Alexandre Cruz Henriques, M.D.,§ and Djalma José Fagundes, M.D., Ph.D.¶

*Fifty Medical Research, São Paulo, Brazil; †Jobst Vascular Center, Toledo, Ohio; ‡Department of Vascular, Escola Paulista deMedicina-UNIFESP, São Paulo, Brazil; §Department of Surgery, ABC School of Medicine, São Paulo, Brazil; and ¶Department of

Experimental Surgery, Escola Paulista de Medicina-UNIFESP, São Paulo, Brazil

Submitted for publication November 7, 2007

doi:10.1016/j.jss.2008.04.016

Background. The main complication of transhiatalsubtotal esophagectomy with esophagogastric recon-struction is anastomotic leak, which is responsible for alarge number of postoperative deaths. It is believed thatthis complication is due to gastric fundus ischemiacaused by the sectioning of the short gastric, left gastric,and left gastro-omental arteries. The literature, how-ever, presents controversies. An experimental study wasperformed with the aim of evaluating the vasculariza-tion of the gastric fundus following sectioning of thesearteries.

Materials and methods. Forty mongrel dogs weredistributed into 2 groups: a control group consisting of15 dogs subjected to surgical simulation and an exper-imental group consisting of 25 dogs that underwentsectioning of these arteries. Fluorescein testing, gas-tric mummification, and morphometric image analysiswere performed on both groups.

Results. In comparison with the control group, fluo-rescein testing on the experimental group demon-strated time-delayed fluorescence in the gastric fun-dus and partial coloring, (P < 0.001). Image analysis onthe mummified gastric samples demonstrated signifi-cant reduction in blood vessels in the gastric fundus ofthe experimental group (P < 0.001).

Conclusions. We conclude that sectioning of theshort gastric, left gastric, and left gastro-omental ar-teries causes reduction in blood circulation and in thequantity of blood vessels on the anterior side of thegastric fundus of dogs. © 2009 Elsevier Inc. All rights reserved.

1 To whom correspondence and reprint requests should be ad-dressed at Department of Vascular Surgery, Jobst Vascular Center,2109 Hughes Drive, Suite 400, Toledo, OH 43606. E-mail:
[email protected].
1280022-4804/09 $36.00© 2009 Elsevier Inc. All rights reserved.

Key Words: gastric arteries; gastric fundus; arterialdevascularization; experimental surgery.

INTRODUCTION

Subtotal esophagectomy is the standard surgicalprocedure for malignant or benign diseases of theesophagus. Esophageal resection in which the thoracicesophagus is replaced by the stomach is one of the bestalternatives for treating esophageal cancer [1–4].

Dehiscence of the gastroesophageal anastomosiswith anastomotic leak is the major postoperative com-plication. It is the leading cause of deaths occurring asa result of surgical treatment of esophageal carcinoma[1, 2, 5–9]. An anastomotic leak rate of up to 37% isdescribed in the literature, and 9.5% of the deaths dueto this operation are related to such leaks [9]. Whenanastomotic dehiscence does not cause death, it con-tributes toward worsening patients’ quality of life, hin-ders early resumption of oral feeding, requires painfullocal care, and increases the length of hospital stay [1].

It is believed that anastomotic dehiscence is mainlydue to ischemia of the gastric fundus [1, 5, 10, 11].Nonetheless, tension in the anastomotic suture, lack ofesophageal serous layer, infection, and inadequate sur-gical technique have also been described as factorsleading to this complication [1]. Adequate blood supplyand satisfactory length for the esophagus (to avoidtension on the anastomotic suture) are necessary con-ditions for the success of esophagogastric reconstruc-tion.

Some authors have stated that the esophagus is arichly vascularized organ and is tolerant to sectioningof the main arterial pedicles. It can also be nourishedby only one artery without facing any vascular prob-
lems [12].
mailto:[email protected]

129GOMES ET AL.: VASCULAR FLOW OF THE GASTRIC FUNDUS AFTER ARTERIAL DEVASCULARIZATION

Other authors believe that sectioning the short gas-tric, left gastric, and gastro-omental arteries section,which is an essential procedure in subtotal transhiatalesophagectomy with esophagogastric reconstruction,causes ischemia in the gastric fundus [2, 5–8].

There is controversy in the literature regarding gas-tric vascularization. Few experimental studies on ani-mals have been published [12, 13]. The present studywas designed to evaluate gastric fundus vasculariza-tion using dogs, following sectioning of the short gas-tric, left gastric, and gastro-omental arteries section,by means of fluorescein testing, gastric mummification,and morphometric study via OPTIMAS, a software toolfor image analysis (Meyer Instruments, Inc., Houston,TX). The objective was to qualitatively and quantita-tively evaluate whether sectioning of gastric arteriescauses an effective reduction in blood circulation andthe quantity of blood vessels in the gastric fundus, orwhether circulation is supplied by collateral branches.

Demonstration of gastric fundus ischemia in thestomach of dogs subjected to sectioning of the shortgastric, left gastric, and gastro-omental arteries wouldreinforce the idea that anastomotic leak relating totranshiatal subtotal esophagectomy with esophagogas-tric reconstruction is caused by ischemia.

MATERIALS AND METHODS

The protocol was fully approved by the institution’s animal ethicscommittee. National Research Council’s guide for the care and use oflaboratory animals was followed. Forty healthy male and femaleadult mongrel dogs weighing between 15 and 25 kg were randomlyallocated within 2 groups:

Group A (n � 15), Control

These dogs were subjected to laparotomy and dissection to reachthe gastric arteries (without sectioning the arteries).

Group B (n � 25), Experimental Group

These dogs were subjected to laparotomy, dissection and section-ing of the short gastric, left gastric and gastro-omental arteries.

Evaluation of vascularization in vivo (fluorescein testing) and invitro (morphological study) was performed on both groups. All dogsreceived preanesthesia medication (intramuscular dose of 0.1mL·kg–1 of acepromazine) before being taken to the operation room.Intravenous pentobarbital sodium (30 mg·kg–1) was used to induceanesthesia. The animals were kept on spontaneous respiration usingan orotracheal tube.

Group A underwent laparotomy and dissection to reach the gas-tric arteries. Group B underwent laparotomy, dissection, and sec-tioning of the short gastric, left gastric, and left gastro-omentalarteries.

Following the surgical procedure, the vascularization of the ante-rior face of the stomach was evaluated in vivo by means of fluoresceintesting. This was performed in a darkened wooden box containingultraviolet light bulbs (Black Light Blue F1ST8BLB 15 Watts;Sankyo Denki Co., Ltd., Kanagawa, Japan), which was placed on topof the dog. An aqueous solution containing 10% fluorescein wasinjected into the group A dogs following dissection to reach the
gastric arteries, and into the group B dogs following sectioning of the
gastric arteries. The injection was administered into the right exter-nal saphenous vein, at a dosage of 1 mL·kg�1, with constant pressureon the syringe plunger. Fluorescein diffusion onto the surface of thestomach body and fundus was observed through an 8 cm hole on theupper wall of the darkened box. Under ultraviolet light, the fluores-cein displayed a greenish-yellow color on the gastric wall and waspurple in blood vessels. Nonvascularized regions did not displaycoloration. The color was recorded and time taken from starting theinjection and observing the fluorescence observed on the anteriorface of the stomach was measured using a digital stopwatch. Photo-graphic documentation was obtained using a conventional camera(Canon EOS 500; Canon, Inc., Tokyo, Japan) and digital cameras(Casio QV 10; Casio, Inc., Tokyo, Japan, and Mavica FD 95; SonyCorp., Tokyo, Japan).

After fluorescein testing, the dogs were subjected to total gastrec-tomy, which also included segments of 0.5 cm of the esophagusproximally and 0.5 cm of the duodenum distally. Following this, theanimals were sacrificed by means of a quick intravenous injection of20 mL of 19.1% potassium chloride.

Mummification of the stomach was performed after washing thegastric lumen in running water, to eliminate the contents. On thebench, adipose tissue fragments and residual omentum were care-fully removed. The proximal stump of the cleaned stomach was tiedup, and the stomach was insufflated with compressed air. Insuffla-tion was performed through a transparent plastic tube inserted intothe distal stump and connected to a compressed air cylinder with amanometer. The pre-established distension pressure was 20 mm Hg.

After reaching the standardized pressure, the tube was removedand the stump was tied up. Following this, the insufflated stomachwas brushed with turpentine (an organic solvent), to speed up thedrying process. It was hung on a pole using thread, in a ventilatedplace. Over the next 48 h, the brushing was repeated during thedaytime, every 4 h, until the stomach dehydration or mummificationwas concluded.

After concluding the mummification process and stomach dehy-dration, a 4 � 4 cm body sample and a 4 � 4 cm fundus sample werecut from the anterior face of the stomach. The samples were placedon a negative light box containing ultraviolet light bulbs (Black LightBlue F1ST*BLB 15 Watts; Sankyo Denki Co., Ltd.), in a darkroom,and they were photographed using digital cameras (Casio QV 10 andMavica FD 95), at a distance of 5 cm from the zoom lenses. Theimages acquired were labeled and recorded.

Observation and quantification of the vascularization of the body andgastric fundus samples were performed by means of the OPTIMASimage analysis program. This program counted pixels, correspond-ing to the blood vessels, in the red color spectrum. The percentageof vessels was calculated. Evaluation of fluorescein images andcounting of the blood vessels were blinded, by an independentreviewer.

Descriptive statistics was initially used to describe the sample.Wilcoxon test [14] for 2 non-independent samples was used to com-pare the time until fluorescence and percentages of blood vessels inthe body and gastric fundus within each of groups A and B. Mann-Whitney test [14] for 2 independent samples was used to compare thesame variables between groups A and B for both body and fundus. Allanalyses were conducted using tests with 95% confidence intervals,a P level of 0.05 or less being considered statistically significant.

RESULTS

Dogs of both groups (A and B) underwent fluoresceintesting to determine the occurrence or nonoccurrenceof fluorescence on the anterior face of the gastric bodyand fundus, and to evaluate whether sectioning thearteries would jeopardize the arrival of the dye in the
study areas. In the control group (A), the dye arrived

s a

130 JOURNAL OF SURGICAL RESEARCH: VOL. 152, NO. 1, MARCH 2009

over the whole gastric surface, on the body and fundus(Fig. 1). In the experimental group (B) fluorescencespread quickly and fully on the anterior face of thegastric body, and slowly and partially on the fundus(Fig. 2). The mean time taken to obtain fluorescence onthe body was 29.52 s, and on the fundus, 52.70 s.According to the Wilcoxon test (P � 0.001), the timetaken to obtain fluorescence on the fundus was greaterthan for the gastric body (Table 1).

FIG. 1. Photograph of dog stomach in experimental group, insidinjection; no fluorescence on the anterior gastric face. (B) 10 s after ththe injection; fluorescence (��): anterior face of gastric body. (D) 30

FIG. 2. Photograph of dog stomach in control group, inside the da
without fluorescence on the anterior gastric face. (B) 30 s after the fluo
The time taken to obtain fluorescence on the bodywas similar for groups A and B. The mean time toobtain fluorescence on the body of group A was 30.00 s,and for group B, 29.52 s. On the gastric fundus, themean time to obtain fluorescence in groups A and Bwere quite different, thus showing that the arrival ofcontrast dye on the gastric fundus of group B wasdelayed in comparison with group A. The mean time toobtain fluorescence on the fundus of group A was

he dark box. a � Body and b � Fundus. (A) Before the fluoresceinnjection; fluorescence (�): anterior face of gastric body. (C) 20 s afterfter the injection; fluorescence (��): anterior face of gastric body.

box. A � Body and B � Fundus. (A) Before the fluorescein injection;

e te i

rk
rescein injection; fluorescence on the entire anterior gastric face.


30.00 s, and for group B, 52.72 s. According to theMann-Whitney test, the time taken to obtain fluores-cence on the fundus of group B was greater than forgroup A (P � 0.001).

TABLE 1

Time Taken, in Seconds, to Obtain Fluorescence onthe Anterior Face of the Gastric Body and Fundus inGroups A and B, Following Fluorescein Injection

Group A Group B

Body Fundus Body Fundus

31 31 30 3828 28 30 4132 32 28 4340 40 35 4723 23 30 4030 30 21 4332 32 22 4730 30 35 6229 29 40 6127 27 20 4331 31 40 9029 29 23 4531 31 21 5030 30 38 6027 27 22 45

24 4337 7350 9640 7038 6423 4518 3721 5032 4420 41

Mean value 30.00 30.00 29.52 52.72Standard deviation 3.62 3.62 8.60 15.70

FIG. 3. Photographs of samples of gastric fundus from a dog in
samples were placed 5 cm away from the lens, under ultraviolet illumi
Using image analysis via the OPTIMAS program onimages from mummified samples, the mean propor-tions of blood vessels in the gastric body were 19.19%for group A and 20.54% for group B. In the gastricfundus of group A (Fig. 3) the mean was 17.51%, and ingroup B, 8.04% (Fig. 4). This showed that there was adistinct reduction in the percentage of vessels in theanterior face of the gastric fundus of the dogs subjectedto sectioning of the gastric arteries. The Wilcoxon testshowed that there was a smaller percentage of bloodvessels in the gastric fundus for both groups (Z calcu-lated for group A � 3.41 and Z calculated for group B �4.37, P � 0.001). However, the magnitude of the sig-nificance in the experimental group was much greater.The Mann-Whitney test (Z calculated for group A �1.45 and Z calculated for group B � 5.21, P � 0.001)showed that the gastric fundus in group B had a lowerpercentage of blood vessels, thus confirming the previ-ous test result (Table 2).

DISCUSSION

The idea of studying the vascularization of thegastric fundus following sectioning of the short gas-tric, left gastric, and left gastro-omental arteriescame from the controversy in the literature regard-ing anastomotic leaks resulting from esophageal sur-gery. Sectioning of these arteries is usually neces-sary to mobilize the stomach up to the cervicalregion, in patients who undergo esophagectomy withesophagogastric reconstruction. However, a greatnumber of authors believe that sectioning of thesearteries leads to gastric fundus ischemia and conse-quent dehiscence of the esophagogastric anastomosis[2, 5– 8]. Other authors believe that sectioning the

e control group, taken using a Mavica FD 95 digital camera. The
th nation. (A) 20% blood vessels. (B) 19% blood vessels.

mi


gastric arteries does not cause any harm to stomachirrigation because of the rich anastomotic network ofmucous and submucous layers [12].

FIG. 4. Photographs of samples of gastric fundus from a dog in thsamples were placed 5 cm away from the lens, under ultraviolet illu

TABLE 2

Percentages of Blood Vessels on the Anterior Face ofthe Gastric Body and Fundus in Groups A and B, Ob-tained Through the Image Analysis Process

Group A Group B

Body Fundus Body Fundus

16.06 14.96 20.55 5.2821.60 14.50 18.69 7.8919.42 18.70 19.74 4.9419.92 16.44 22.53 10.8514.35 12.66 19.41 5.2615.75 15.00 20.92 6.5515.60 14.90 22.03 9.4518.70 17.90 24.59 9.8717.98 17.00 21.82 10.3319.90 19.30 19.77 7.4920.00 19.00 15.78 7.8520.32 19.70 24.83 13.9721.45 20.78 19.98 7.2724.03 20.99 21.08 9.2322.73 21.03 21.24 6.78

16.82 7.6924.57 9.4622.48 9.0819.29 7.3622.08 8.7020.11 7.7520.98 5.4416.43 5.3520.00 8.0017.54 8.49

Mean value 19.19 17.51 20.54 8.04
Standard deviation 2.79 2.68 5.69 2.07
The gastric blood vessels in dogs are anatomicallysimilar to those of human beings, and they offer easysurgical access and adequate diameter for carrying outthe procedures proposed. Dogs have been used as anexperimental model in other studies relating to stom-ach vascularization because of this similarity [15].

Since 1942, when the first study using fluorescein toinvestigate blood circulation was carried out, this drughas been widely used, clinically and experimentally[16]. Fluorescein can be applied as a method for eval-uating tissue viability in severe open fractures in or-thopedics, for evaluating the circulation in the retina,optical nerve, and cornea diseases in ophthalmology,and for evaluating early and late viability of trans-planted tissue in plastic surgery. It can also be used fordetermining the positions of intestinal loops in gastro-enterological surgery and for delimiting the optimalamputation level in vascular surgery.

On the basis of the successful results obtained via thefluorescein method for evaluating ischemia, and becauseof the great diffusion of this drug, this was the contrastmedium chosen. The recommended dosage is 1 mL·kg�1

or 20 mg·kg�1 of the sodium salt of fluorescein at a con-centration of 10% in aqueous solution, administered in-travenously [16]. This dosage and administration routeenable optimal visibility of fluorescein on the stomachsurface, thus making it possible to evaluate the dynamicbehavior of the blood circulation using ultraviolet illumi-nation. The dogs in the Control group underwent fluores-cein testing to determine the normal fluorescence colora-tion on the anterior face of the gastric body and fundus,and to measure the time interval from the start of fluo-rescein injection to the appearance of fluorescence on the

xperimental group, taken using a Mavica FD 95 digital camera. Thenation. (A) 20% blood vessels. (B) 8% blood vessels.

e e

surface of the gastric body and fundus.


When group A underwent fluorescein testing, thegastric body and fundus showed a fluorescent greenish-yellow color, and the blood vessels showed a purplecolor. In another experimental study on dogs relatingto the irrigation of the lesser gastric curvature follow-ing after proximal gastric vagotomy, the normal vas-cularization of dog stomachs under ultraviolet light,after fluorescein injection, also showed greenish-yellowfluorescence.

It was considered that the dye circulation was uni-form when the time interval from the start of thefluorescein injection to the appearance of fluorescencewas the same for both regions analyzed. In the controlgroup, the injected fluorescein spread quickly and uni-formly all over the anterior face of the stomach, fromthe lesser to the greater curvature. The times taken toobtain fluorescence in the gastric body and fundus ofgroup A were the same, and the mean time was 30 s.Statistical analysis of this result was discarded be-cause of the identical nature of the gastric body andfundus data.

The dogs in the experimental group underwentfluorescein testing to determine whether fluores-cence did or did not occur on the anterior face of thegastric body and fundus, and to evaluate whethersectioning of the arteries would compromise the ar-rival in the study areas. In this group, fluorescencespread quickly and fully on the anterior face of thegastric body and slowly and partially on the fundus.The time taken to obtain fluorescence on the funduswas longer than for the gastric body, and this leadsto the idea that ischemia caused by sectioning thearteries was present.

The time taken to obtain fluorescence on the gastricbody was similar for groups A and B. On the gastricfundus, the mean times taken to obtain fluorescence ingroups A and B were quite different, with a delay in thearrival of contrast on the gastric fundus of group B, inrelation to group A. This result showed that bloodcirculation on the fundus was taking place via an al-ternative route, probably through the rich anastomoticnetwork of the gastric submucosa and mucosa [15]. Ingroup B, fluorescence on the gastric fundus occurredonly partially in all of the dogs, thus showing thatblood circulation is insufficient, in comparison withgroup A, in which fluorescence occurred fully. Theseresults revealed that the collateral branches of theanastomotic network of the gastric submucosa and mu-cosa only partially supplied the blood circulation forthe gastric fundus of the dogs that underwent partialsectioning of the stomach arteries.

Diaphanization is a method that is acknowledged tobe efficient for studying the vascularization of the vis-cera and organic structures. However, it involves largequantities of chemical substances that are highly toxic
and very difficult and dangerous to handle. Further-
more, it requires an open environment with good ven-tilation and several days (around 20) for completion,thus making this process excessively expensive andslow. For all these reasons, an efficient alternativemethod for studying gastric vascularization, which wasfaster and cheaper, was used.

Simple observation of mummified specimens underdirect viewing made it possible to qualitatively evalu-ate the vascularization of the gastric body and fundus.It was seen that the vessel concentration varied insome areas. However, quantitative evaluation of theseareas was necessary, to determine whether or not therewas any reduction in vascularization in the gastricfundus. An objective method of image analysis wasneeded. In 1992, a quantitative morphometric studywith analysis of the microcirculation in prostate carci-noma by means of the OPTIMAS [17] program waspublished. Since then, many other authors have usedthe same image analysis program [18].

The stomachs of the dogs in groups A and B wereremoved and mummified to allow samples to betaken from the anterior face of the gastric body andfundus. These specimens were photographed and ex-amined using the image analysis program. In thecontrol group, this procedure was performed to stan-dardize the normal percentage of blood vessels in thegastric body and fundus. In the experimental group,this analysis was performed to verify whether theproportion of blood vessels would be the same as ingroup A, or whether it would be different because ofsectioning of the short gastric, left gastric, and leftgastro-omental arteries.

Analysis via OPTIMAS on images of the mummi-fied samples showed a reduction in the proportion ofvessels in the anterior face of the gastric fundus ofthe dogs that underwent sectioning of the gastricarteries. This leads to the hypothesis that ischemiaof the fundus secondary to sectioning the arterieswas present.

These results show that the anastomotic network ofthe gastric submucosa and mucosa layers was unableto fully supply the partial vascularization of the stom-ach in the acute phase of the experiment.

From this preliminary result, the intention is tomove on to a second stage in this research, to studyvascularization of the gastric fundus after a predeter-mined period of time, using more advanced methods,such as directly measure of tissue oxygenation, cellularnecrosis, or other measures of ischemia or cell deathwith the aim of observing whether or not late revascu-larization occurs. Such observations will allow a con-clusion to be reached regarding whether or not esopha-gogastric anastomosis in a separate operation wouldprevent anastomotic leak [1].

Cervical anastomotic leak following esophagectomy
with esophagogastric reconstruction is a serious com-


plication that has not yet been solved, despite constanteffort from researchers to solve it.

CONCLUSIONS

1. Sectioning of the short gastric, left gastric, and leftgastro-omental arteries gave rise to reduced blood cir-culation on the anterior face of the gastric fundus ofdogs, as seen via fluorescein testing.

2. These sectioning of arteries leads to a reduction inthe quantity of blood vessels on the anterior face of thegastric fundus of dogs, as seen via morphometric imageanalysis.

ACKNOWLEDGMENTS

The authors thank Mr. Fernando Pereira Gomes, electronic engi-neer, who provided all technical support for this experimental study.

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vascular flow of the gastric fundus after arterial devascularization: an experimental study

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