RESECTION AND END-TO-END ANASTOMOSIS OF THETHORACIC AORTA IN PUPPIES

TWO AND THREE-QUARTER YEAR FOLLOW-UP*

EDWARD B. C. KEEFER, M.D., FRANK GLENN, M.D.,AND CHARLES T. DOTTER, M.D.

NEW YORK, NEW YORK

FROM THE DEPARTMENTS OF SURGERY AND RADIOLOGY OF THE NEW YORK HOSPITAL-CORNELL MEDICAL CENTER

OPERATION FOR COARCTATION of theaorta should be done as early in life as isfeasible. An individual of two and a halfto three years of age no longer faces theoperative risk of infancy. The aorta in achild of this age is about 8 to 10 mm. indiameter, or one third to one half that ofthe adult. An anastomosis performed at anearly age produces a lumen of uniform sizewhich is normal for the child at this time,is temporarily sufficient for the growingchild and is a definite improvement overpartial or oomplete obstruction. Eventhough an additional procedure may benecessary at a later adult age, the progres-sive, damaging effects resulting from thecoarctation are probably delayed and de-creased in intensity. Early correction of thecondition may shorten the duration of hy-pertension and lessen detrimental effectsupon the myocardium, vascular system andassociated vital organs.

The collateral circulation is usually welldeveloped at two and a half to three yearsin the majority of cases. Rib notching hasbeen demonstrated at this age; its absence,however, does not imply that collateral cir-culation is not present. In a few cases,ischemia of the cord and paralysis areknown to have occurred when the aorta wasclamped for 50 minutes or longer. Suchparalysis may result from an inadequate

* Submitted for publication February, 1951.

blood supply to the cord, either from pro-longed occlusion of the aorta or from anes-thetic anoxia; both may occur. Therefore,in considering surgery in the earlier agegroup, the collateral circulation should beevaluated. The duration of aortic occlusionshould be kept at a minimum during theprocedure. Fortunately the complication ofparalysis is extremely rare and the possibil-ity of its occurrence does not necessarilyconstitute a oontraindication to surgery inyoung patients.

Operation is technically desirable be-fore irreversible atheromatous changesoccur in the vessel walls. A number of ad-vantages and disadvantages are listedbelow.

In the Younger Individual: The vessels are.less friable, more elastic and pliable. The inter-costals, being less friable, are easier to dissect anddangerous bleeding less likely to be encountered.Because of better pliability and elasticity a longergap can be bridged by primary suture under lesstension, and a potential increase in the extent ofthe coarctation occurring with growth may thus becircumvented.

In the Older Individual: The increased rigidityof the adult aorta necessitates compromising thediameter of the anastomotic area by removal of ashorter segment in order that no undue tension beproduced. While homologous grafts may be used,primary end-to-end anastomosis is preferable ifpossible.

The longer duration of hypertension andcoarctation in patients of 11 years' age or older mayresult in pathologic changes in the vessels to the

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extent that it is often difficult to suture the athero-sclerotic aorta.

Cerebrovascular accidents may occur.

Following surgical correction of the coarcta-tion, the coronary flow may be so diminished bythe resultant fall in blood pressure that the alreadyimpaired coronary vessel is unable to provide an

adequate blood supply to the myocardium.7Aneurysms of the intercostals may develop

which are subject to rupture and severe hemor-rhage without operation, during operation or fol-lowing operation.

Below the aortic constriction (Fig. 1),the intercostal arteries, with aneurysms anddistended by the collateral circulation whendivided and ligated, are more prone to rup-

ture at their distal tied end than at the prox-imal tied end adjacent to the aorta. This isperhaps not what would be expected, but isprobably due to the reversed blood flowthrough this part of the collateral circula-tion causing pressure on the blind end ofthe intercostals. Usually these vesselsthrombose with resultant obliteration oftheir lumen.

"I .:~

A(

FIG. 1.-Arrows show the direction of the col-lateral blood flow below the aortic constriction.Note effect on distal tied intercostal arterial wall.

4. Atheromatous changes were absenton microscopic examination one year post-operatively.

TABLE I.

Weight at: PostoperativelyPuppy No. Date of Date of Length P.O. -- Age atand Sex Operation Death Dog Lived Operation 1 Week 2 Months 1 Year 2 4 Years Operation

Finnegan 9 5/27/48 7/7/48 41 days 2.6 lbs. 3.2 lbs. .... ... 3-4 wks.793 9 6/1/48 6/30/48 29 days 6.6 lbs. 7.2 lbs. .... .... .... 6-8 wks.794 9 6/1/48 7/13/48 42 days 6.4 lbs. 6.6 lbs. .... .... .... 6-8 wks.795 ei 6/2,/48 5/24/49 356 days 7.5 lbs. 7.5 lbs. 11.2 lbs. 28.5 lbs. .. 6-8 wks.796 e 6/3/48 6/25/48 22 days 8.0 lbs. 9.0 lbs. .... .... .... 6-8 wks.797 9 6/3/48 .... 8.2 lbs. 7.1 lbs. 15.0 lbs. 34.0 lbs. 27 lbs. 6-8 wks.798 9 6/3j/48 .... .... 7.1 lbs. * 7.9 lbs. 14.3 lbs. 34.0 lbs. 25.5 lbs. 6-8 wks.

In a previous paper on this subject,' our

findings suggested the following:1. The technical aspects of thoracic

aorta anastomosis in puppies could be ac-

complished without mishap.2. The diameter of the lumen at the site

of anastomosis in dogs did not keep pace ingrowth with the rest of the aorta.

3. No demonstrable roentgenologic evi-dence of compensatory collateral circula-tion was found in any case at one year post-operatively.

A recent report2 by another investigatorreporting on a larger series of puppies cor-roborates these early findings.

On May 27 and June 1, 2 and 3, 1948,end-to-end anastomosis of the thoracic aortawas performed successfully on a consecu-tive series of seven puppies. The anasto-mosis was placed distal to the great vesselsof the aortic arch. One of these puppieswas three weeks old (2.6 pounds) and theother six were from one litter approximatelysix to eight weeks old and weighing

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F i 2 Fic.FIG. 2.-Suture line, puppy Finnegan, viewed from within, 41 days postoperatively.FIG. 3.-Suture line, puppy No. 793, viewed from within, 29 days postoperatively. In this

case and that shown in Figure 2 there is no observable silk present. Same metric scale asFigure 2.

from six to eight pounds. This one entireseries, admittedly small, was unselected.We believed it significant that no operativeor immediate postoperative death occurredand that no gross abnormalities were foundat the site of anastomosis (Table I, Figs. 2to 5). No demonstrable spinal cord anoxiaor hind leg paralysis developed. The oper-

ative technic was not difficult, anastomoseshaving, been performed successfully on

three puppies by the same surgeon on thesame day. Anastomoses were made with a

single, continuous, everting (intima-ap-proximating) mattress suture3-6 of 5-0 Dek-natel arterial silk on a minimal traumaneedle No. 155. Care was taken to leave as

little silk as possible on the intimal surface(Figs. 2 and 3). As small a cuff as possiblewas made to minimize the amount of con-striction at the site of anastomosis (Fig. 4).Positive pressure in the lungs was main-tained by inflation with room air; no in-creased oxygen concentration was used. Itwas unfortunate that four of these dogsdied 22 to 42 days postoperatively from in-testinal infestation, inanition and terminalpneumonia (probably distemper). The su-

ture lines in these four animals were satis-factory (Figs. 2 to 5).

At present, two years and nine monthsfollowing the original anastomosis, we areable to report clinical, roentgenographic

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and blood pressure findings not previouslyso evident.

Dog No. 798, with demonstrable coarc-tation, is asymptomatic at rest, but follow-ing exercise develops symptoms compatiblewith a diminished cardiac reserve. Theseinclude labored, gasping respirations,frothing around the mouth, cyanosis of the

tongue mucosa, tachycardia, prostration,coma, and generalized convulsions consist-ing of purposeless running motions of thelegs, rigidity of the neck, and jaw musclesin spasm with the mouth open. All symp-toms disappear on rest (returning animal tocage) only to recur with exercise (allowinganimal to run). These clinical symptoms

iTrrz.I_

Fic.. 4 Fi (G. r

FIG. 4.-Suture line, puppy No. 794, viewed from without, 42 days postoperatively. Significant constriction is not apparent.

FIG. 5.-Suture line, puppy No. 796, viewed from within, 22 days postoper-atively. A small amount of silk suture material is visible. Same metric scale asFigure 4.

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have developed gradually and appear to beincreasing in severity. Dog No. 797, on

which a similar operative procedure was

performed on the same date, does not showthese symptoms on exercise.

Retrograde aortogram was performed 2years and nine months postoperativelyunder Nembutal anesthesia by injecting 10cc. of 70 per cent Diodrast rapidly into the

patible with these roentgen ray find-ings. In dog No. 797, the constriction isnot as severe in comparison with the size ofthe adjacent aorta (Fig. 7). Less dilatationabove and below the artificial coarctationsuggests less obstruction and probably indi-cates that the suture line has increased indiameter (Table II). This increase has notkept pace with the growth of the remain-

iw ...

...........

i

F(c;. 6

FIG. 6.-Retrograde aortogram. Dog No.Significant coarctation is shown.

FIG. 7.-Angiocardiogram. Dog. No. 797,narrowing is demonstrate .

left carotid artery of dog No. 798 (Fig. 6).An angiocardiogram was also done at thistime in dog No. 797 by injecting a fore-legvein with 14 cc. of 70 per cent sodiumUrokon (Fig. 7). In dog No. 798, a coarc-

tation very suggestive of the adult type inhumans is well demonstrated (Fig. 6). Thediameter of this constriction appears toremain the same as at one year and ninemonths ago or is perhaps smaller (TableII). The degree of constriction at present isgreater in relation to the size of the prox-

imal and distal aorta. The increased bloodpressure values (Fig. 9B) are also com-

I..

798, two years and nine months postoperatively.

two years and nine months postoperatively. Slight

ing aorta. In this animal a much less severe

degree of coarctation is probably develop-ing at a slower rate. These dogs will bekept for further long-term study.

Comparison of the blood pressure trac-ings in the carotid and femoral arteries withsimilar studies done one year and ninemonths ago in these two dogs suggests thata definite length of time is required fordemonstrable hypertension to develop(Figs. 8 and 9). The rate of its develop-ment was slow, possibly due to the fact thatat the time the anastomosis was created thecaliber of the aorta was uniform throughout

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KEEFER, GLENN AND DOTTER

FIG. 8

Fic. 8.-(A) Top: Carotid and femoral arterial direct blood pres-

sure tracings on dog No. 797, one year postoperatively. Dampening,apparent on these tracings, is probably responsible for the pressure dif-ferential, since it is not present in later curves. (B) Bottom: Carotidand femoral arterial direct blood pressure tracings on dog No. 797, twoyears and nine months postoperatively. Systolic pressures are virtuallyidentical.

FIG. 9.-(A) Top: Carotid and femoral arterial direct blood pres-

sure tracings on dog No. 798, one year postoperatively. (B) Bottom:Carotid and femoral arterial direct blood pressure tracings on dogNo. 798, two years and nine months postoperatively. Curves were

recorded directly from exposed arteries and the pressure differentialis thought to represent the effects of physiologically significant coarcta-tion of the aorta.

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and constriction occurred only as the dogsgrew. We may thus assume that if a coarc-

tation is repaired at two and a half to threeyears of age in a child, its immediate detri-mental effects will be completely alleviated.If, through growth following the operation(as in dog No. 798), the suture line fails tokeep pace with the adjacent aortic lumenand physiologic evidence of coarctation re-

curs, a second operation may be done. Eventhough this occurs, the changes should beless severe. An important factor is the rate

earlier operation permanent detrimentaleffects of coarctation may be partially atten-uated, sparing the individual until adult sizeis reached and an adequate caliber anasto-mosis can be done. The risk of two sur-

gical procedures done before severe cardiacand vascular pathologic changes have had a

chance to develop is probably justifiable andshould be considered instead of one proce-dure delayed until irreversible changes haveoccurred. Recent improvements in anes-

thesia and surgical management now permit

TABLE II.-Anastomotic Suture Line Diameter.

At Death 1 Year P.O 2% Years P.O.At Operation Approx. 2 Mos. P.O. Approximate Approximate

Dog Number Outside Diameter Insicfe Diameter Inside Diameter Inside Diameter

Range Range793, 794 and 796 4-6 mm. 5-6.5 mm. ........ ........

797 4.5 mm. ........ 7.5 mm. 8 mm.798 4.0 mm. ........ 5.5 mm. 4 mm.

The one and two year plus follow-up measurements are estimates taken from the roentgen rays.The roentgenographic studies were done using a uniform technic and magnification kept to a mini-mum. Allowance has not been made for rotation of the vessel due to animal position and changes indistention of the vessel from respiratory variations in pressure and systolic and diastolic blood pressure.

of growth of the human aorta. The increaseof the caliber of the aorta by growth duringintrauterine and the first two and a halfyears of life is rapid in comparison to thegrowth after this age, a fact probably asso-

ciated with the rapid and tremendous in-crease in body size occurring during theearlier period. If obstruction exists, espe-

cially complete obstruction, correction isindicated as soon as possible thereafter.

Certain conclusions may be drawn fromthese findings. During the first three years

in the life of the two living dogs (compar-able to a human life-span of 15 to 20 years)the aorta became progressively more con-

stricted as the adjacent segments increasedin size with growth. The hypertension alsoprogressively increased. The dogs, althoughlitter mates, did not show the same degreeof involvement; one showed a far greaterdegree of anatomic and physiologic coarcta-tion. It might be assumed from this that by

such surgery in children with less risk thanpreviously encountered.

Less limitation of the growth of theanastomotic area might have resulted bythe use of interrupted sutures or catgut su-

tures8 rather than continuous silk suture as

was used in this series of dogs. This prob-ably also applies in human beings. Otherfactors to be considered in this problem in-clude muscle tone, elasticity and histologicstructure of the aortic wall proximal anddistal to the site of coarctation. In theyoung vessel, muscle tone, strength andelasticity of the wall are able to preventdilatation and maintain a relatively uniformcaliber. As the tissues grow older, enlarge-ment due to the above factors and/orgrowth occurs and a variation in caliber re-

sults. This produces disturbances of thehemodynamics with irregularities in pres-

sure and rate of blood flow and gives rise topathologic changes in the vascular wall sim-ilar to that seen in aneurysms.

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CONCLUSIONS

A follow-up study of two dogs in whichend-to-end anastomosis of the thoracicaorta was done two years and nine monthsago during the first eight weeks of life re-vealed in one dog a developing coarctationcomparable to the adult type seen in hu-mans. To our knowledge, the experimentalproduction of a defect such as is shown indog No. 798 has not been previously re-corded. The animal exhibits clinical symp-toms, hypertension and roentgenographicfindings related to coarctation of the thor-acic aorta. It is suggested that the creationof this defect in the experimental animalmay offer a new method for the study ofhypertension and cardiac physiology. In asecond dog (No. 797) the changes pro-duced were less impressive; with growth, anincrease occurred in the size of the lumenat the site of anastomosis.9-11 A still longerterm evaluation of the problem is needed.The following conclusions may be drawn.

1. The aorta probably increases in cal-iber in the anastomotic area. Such enlarge-ment is variable in degree however, anddoes- not keep pace with the growth of theadjacent aorta.

2. With growth and/or dilatation of theaorta adjacent to the artificial coarctation,the resultant roentgenograpbic and bloodpressure changes resemble those seen inhuman patients with coarctation of theaorta.

3. For reasons discussed above, it issuggested that earlier surgical correction ofcoarctation of the aorta in human patients is

desirable even though a second procedurewill be necessary in certain cases.

BIBLIOGRAPHYGlenn, F., E. B. C. Keefer, C. T. Dotter and

J. M. Beal: Observations on ExperimentalAortic Anastomosis. Proc. Soc. Exp. Biol. &Med., 71: 619, 1949.

2 Brooks, J. W.: Aortic Resection and Anastomosisin Pups Studied after Reaching Adulthood.Ann. Surg., 132: 1035, 1950.

3 Gross, R. E., and C. A. Hufnagel: Coarctationof the Aorta; Experimental Studies Regardingits Surgical Correction. New England J.Med., 233: 287, 1945.

4 Crafoord, C., and G. Nylin: Congenital Coare-tation of Aorta and Its Surgical Treatment.J. Thorac. Surg., 14: 347, 1945.

5 Blalock, A., and H. B. Taussig: The SurgicalTreatment of Malformations of the Heart.J. A. M. A., 128: 189, 1945.

6 Blalock, A., and E. A. Park: The Surgical Treat-ment of Experimental Coarctation of theAorta. Ann. Surg., 119: 445, 1944.

T Humphreys, G. H.: Personal communication.8 Smith, S., F. R. Johnson and W. L. Riker: Ab-

sorbable Sutures in the Surgery of MajorBlood Vessels. Presented in the Forum onFundamental Surg. Prob., Chicago, October18, 1949.

9 Lowenberg, R. I., and H. B. Shumacker, Jr.:Experimental Studies in Vascular Repair.Strength of Arteries Repaired 'by End-to-endSuture with Some Notes on Growth of Anas-tomosis in Young Animals. Arch. Surg., 59:74, 1949.

10 Hurwitt, E. S., and S. A. Brahms: Observationson the Growth of Aortic Anastomoses inPuppies. Ann. Surg., 133: 200, 1951.

Johnson, J.: Reference to work on pigs. Indiscussion of paper10 at the Forum on Fun-damental Surgical Problems. Thirty-fifthAnn. Clin. Congress Am. College Surg., Chi-cago, October 18, 1949.

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