THE CONSTRUCTION OF FRESH AUTOGENOUS ARTERIAL GRAFTS
I. Use or THE SpLeNic ARTERY TO BRipcGe A Gar IN THE AORTA
Enviorr 8. Hurwirr, M.D., anp Aprian Kanxrrowirz, M.D., New York, N. Y.
(From the Surgical Research Laboratories, the Montefiore Hospital)

N JAN. 28, 1947, an experimental program was launched in the Surgical
O Research Laboratory of the Children’s Medical Center in Boston whieh
led directly to the first successful use of preserved homologous arterial grafts
in human beings by Dr. Robert E. Gross. In the comparatively short space of
time that has elapsed since this reinvestigation of the initial work of Carrel
and others* was instituted, a prodigious amount of effort has been expended in
various research centers to solve the many problems that have been raised.

Fresh autogenous venous grafts have satisfied the requirements for bridging
gaps in small and medium-sized arteries? and for constructing shunts in the
surgical relief of portal hypertension*® and superior vena caval obstruction’
as well as from the aorta to the coronary sinus.6 Although segments of fresh
autogenous inferior vena cava®!? and of preserved venous homografts” have
been employed successfully to bridge gaps in the aorta of the experimental
animal, use of this vessel in human beings has. not met with enthusiasm. The
inaccessibility of the inferior vena cava from the thorax and the high incidence
of untoward sequelae following caval ligation’! have been limiting factors in
autotransplants. Rupture of a vein graft in the surgical treatment of an ab-
dominal aneurysm has already been reported,* and Johnson and co-workers dem-
onstrated an aneurysmal bulge in an experimental vein graft to the aorta.

Preserved homografts of aorta and large arteries have supplied the most
satisfactory solution to date for the problem of bridging a gap in the aorta in
human beings. Blood vessel banks have been established in Boston,1° New York,"
Denver,** and other centers. The major difficulty in maintaining these banks,
with the exception of front line military hospitals,’ has been an inadequate
supply of acceptable donor material.

There have been two main lines of investigation to remedy this situation.
One of these has been concerned with improved techniques of preservation, so
that the safe period of storage of grafts before they must be discarded might
be prolonged. These have included refrigeration (Hufnagel,?° 2* Deterling and
associates’) and fixation by formalin (Peirce and co-workers”’) , glycerin,?* and
aleohol?? among others. The second, the possibility of augmenting the supply
by sterilization of contaminated grafts by high-voltage cathode ray irradiation,
is being explored in the laboratory of Dr. Gross (with human application al-
ready accomplished**) and by Hui and co-workers.?’

Functional success, with patent grafts, has thus been achieved with fresh
and preserved, venous and arterial, autogenous and homogenous (as well as
heterogenous”*) transplants. The disturbing fact, however, has been that, with

 

Received for publication, Dec. 6, 1951.
the exception of the fresh autogenous arterial graft, the cellular constituents of
the transplants disintegrate, the muscle cells of the media disappear, and fibrous
tissue replacement occurs, often with collagenous degeneration and calcification.
Gross?® has analyzed nineteen cases of coarctation of the aorta in which the
narrowed segment had been replaced by a preserved homologous graft. In one
patient calcification in the graft has been noted roentgenographically, and in
another there is presumptive evidence of thrombosis. While some of the tech-
niques of preservation are conducive to more severe changes than others, in
none does the graft present a normal or healthy histologic appearance. Miller
and associates®’ have confirmed the previous observations that only in the fresh
autogenous graft may one anticipate preservation of the histologic integrity of
the media.

The general acceptance at this time of the preserved arterial homograft
represents a compromise, with a transplant that might be mtact both func
tionally and anatomically as the ideal. The hope that survival of the cells of
a homograft might be enhanced by the adrenocorticotropic preparations has
been short-lived. To date, no adequate source of autogenous arterial tissue
for fresh aortie grafts has been devised. Recognition of the importance of de-
veloping a source of fresh autogenous arterial tissue from which gratts of large
diameter might be constructed led to a consideration of the possible use of the
splenic artery for this purpose. A long artery of moderate size, associated
with an organ that may be sacrificed without jeopardizing the welfare of the
subject, supplies the basis for these experiments.

EXPERIMENTAL METHOD

Large mongrel dogs, averaging 50 pounds in weight, were anesthetized with
intravenous veterinarian Nembutal. The peritoneal cavity was entered through
a liberal left paramedian musele-splitting incision. The spleen was mobilized
and all of its attachments divided, to the pedicle. The tail and body of the
pancreas were dissected from the splenic artery, and the artery ligated at as
high a level as possible. This usually resulted in a length of available splenic
artery measuring from 6 to 10 em. between the proximal ligature and the hilus
of the spleen where the artery breaks up into branches. Autotransfusion with
splenic blood was effected by squeezing the spleen, following which the vein was
ligated and the spleen resected, with a long pedicle.

At a separate table, the splenic artery was isolated from the vein, and the
remainder of the tissue discarded. The artery was split longitudinally, an
attempt being made to include any branches in the line of the incision. The
opened artery was divided transversely into 3 (or 4) equal segments. The
panels thus created were then fashioned into the tubular graft by the steps
illustrated in Fig. 1. Each longitudinal suture line consisted of a continuous
over-and-over stitch of No. 00000 Deknatel silk, to which petrolatum had been
applied, on a small straight atraumatie needle. The saline drip to prevent dry-
ing of the tissue was of great importance.

4
The lower portion of the abdominal aorta was mobilized, usually with
division of 1 or 2 pairs of lumbar branches. The aorta was occluded by, and
divided between, 2 multitoothed’ clamps of the Potts type, with resection of a
segment up to 1 em. in length. This gap was bridged by the tubular graft just
constructed. The graft was anchored into place at each end. Each circumfer-
ential suture line consisted of a continuous everting mattress suture of No. 00000

 

Cc. D.

Fig. 1—Fabrication of tubular graft: A, 7 cm. length of splenic artery isolated from
hilus and vein; B, artery split in long axis, being divided transversely into equal panels:
C, suture line commenced with first 2 panels; D, tubular graft almost completed.

Deknatel silk on a small round atraumatic needle. Care was taken to straddle
the end of each longitudinal suture as it was reached. Following completion
of the anastomosis, the transplant was irrigated with saline solution introduced
by a needle into the aorta, and tested for leaks. Large leaks were repaired by
interrupted sutures. The graft was wrapped in compressed Gelfoam,* size 100,

*Supplied through the generosity of The Upjohn Company, Kalamazoo, Mich.

5
and the distal occluding clamp released, followed by gradual release of the
proximal clamp while the graft was gently compressed for several minutes. The
Gelfoam usually became bloodstained quickly. When active bleeding had been
eliminated, metal dura clips were placed as markers for roentgenographie iden-
tification, the posterior parietal peritoneum was united over the graft. and the

 

Fig. 2.--Fabricated tubular graft sutured into gap in abdominal aorta: A, graft anchored to
each end of aorta; B, second circumferential anastomosis almost complete.

peritoneal cavity was closed in layers. No anticoagulants were used, either
locally or systemically. Each dog received an infusion of 1,000 cc. of 5 per
cent glucose in water intravenously during the operation, and 300,000 units of
penicillin per day for the first 3 postoperative days (Fig. 2).

6
After the technique had been acquired, splenectomy and construction of
the graft consumed about one hour. By mounting the artery panels in the jig
contrived by one of us (A. K.), it was possible for one man to carry out the
entire fabrication of the graft alone. While he was thus occupied, the rest of
the team mobilized the lower abdominal aorta, from below the renal arteries
almost to the aortic trifureation.

EXPERIMENTAL RESULTS

A total of 30 dogs was utilized for these observations. Technieal pitfalls
accounted for many early failures. An analysis of the experiments in 3 con-
secutive groups of 10 each emphasizes the importance of evolving a definitive
technique. In the first group of 10 there were 4 good grafts, with only 2 lone-
term survivors; of the second 10, 6 grafts were satisfactory and 4 dogs did
well; in the final 10 there were 8 good grafts with 6 survivors. The discrep-
ancy between the 18 good grafts and 12 long-term survivors is accounted for
by 6 postoperative deaths due equally to distemper, aspiration pneumonia, and
anesthesia.

Many of the early failures were attributable to necrosis in the eraft due
to excessive pressure by the jig holders; the placing of the sutures in the fabri-
eation of the graft in such a way that too much or too little tissue wes included,
or strands of adventitia inadvertently carried along; drying of the panels;
improper construction of the anastomotic suture lines; and the laek of Gelfoam.
The completed technique included careful adjustment of the jig holders, metieu-
lous plaeing of all sutures, a continuous saline drip to keep the panels moist
during fabrication of the graft, and a backing for the graft of compressed Cel-
foam. By observing all of these details, there was only 1 unsatisfactory experi:
ment in the last 8 consecutive dogs, and that was due to clumsiness on the part
of the operator in performing the anastomosis.

The average diameter of the pulsating abdominal aorta measured 11 mm.,
and that of the splenic artery 3 mm. The 3 panel grafts employed in the early
experiments were uniformly smaller in caliber than the aorta, but the + panel
eratts employed Jater made a niee fit. There was usually a sufficient length of
spleme artery available to permit construction of a tubular graft up to 2 em.
long. In only 1 instance was the splenie artery so thin and narrow that a
satisfactory graft was not ereated. Pancreatitis following mobilization of the
splenic artery oecurred only onee, with aeute gastric dilatation leading to the
death of the animal.

Hemorrhage from rupture of the graft oecurred 6 times in the first 14
experiments, and this was eliminated as the technique became standardized.
There were 4 instances of thrombosis of the graft, of which 1 was associated
with infeetion and the other 3 with the traumatie causes already discussed.

Use of the splenic artery in 30 dogs thus resulted in 18 satisfactory aortie
grafts. Of the 12 failures, 11 were due to avoidable factors that were eliminated
as the experiments progressed, and in only 1 dog was the artery itself unsuitable
for the fabrication of a tubular graft.
Functional evaluation of the grafts has been based upon the postoperative
course and upon aortography. Retrograde aortagrams were made soon after
operation and before sacrifice on every animal. In no ease had the caliber of
the graft lessened in the interval between examinations, the longest-term survi-
vor to be sacrificed to date having survived 6 months. Aortography was done
by injecting 30 «ce. of 35 per cent Diodrast rapidly in retrograde fashion into
a cannulated femoral artery and taking rapid films with the Fairchild 914 by
914 inch magazine roll camera (Fig. 3).

Anatomical evaluation of the transplants was based on gross and histologic
observations. In all the specimens examined within 4 months after operation,
there was a distinct difference between the color of the intima of the eraft and

 

A. B.

Fig. 3.—Retrograde aortagrams 2 weeks after insertion of A, 3 panel, and B, 4 panel arterial
autografts.
that of the host aorta. A tan in the early specimens was gradually replaced by
a pearly gray in the older ones, so that by 6 months after operation the color
of the intima was uniform. In dogs dying within the first 10 days after opera-
tion the intimal surface was shaggy, and the sutures bare. Small flat mural
thrombi were not uncommon, more often attached to the graft panels than to
the sutures. The importance of the speed and force of blood flow in the aorta
in minimizing thrombus formation cannot be overemphasized. By the tenth
postoperative day the circumferential sutures and the ends of the longitudinal
sutures were partly covered by endothelium in 2 specimens, with bare areas in
the central portions of the longitudinal sutures and a few tiny shallow uleera-
tions in the panels. Two additional specimens examined on the fifteenth and

8
sixteenth days, respectively, showed almost complete smooth covering of the
sutures. with small shaggy patches in the central part of the graft. Studies
have been conducted on 5 grafts examined at 2, 3, 4 (2 dogs) and 6 months after
insertion. No thrombi or ulcerations were present, and the intimal surface of
the transplants, including the suture lines, was completely covered by endo-
thelium. Straightening of parts of the longitudinal suture lines in the six-
month specimen indicates that some of the loops have pulled out of the panels
in these areas; the silk is still covered by endothelium (Fig. 4). Additional
dogs are being maintained for long-term survival observations.

The thickness of the graft, which at the time of insertion was considerably
less than that of the aorta, gradually increased with the organization of the
Gelfoam. passing through a stage of excessive thickness to a final state in which
the walls of host and graft had approximately equal measurement.

A.

 

B.

Fig. 4.—-Gross appearance of fabricated tubular grafts A, 65, and B, 195 days after implanta-
tion. Suture lines are smoothly covered by endothelium, and partly pulled straight in B.

The histologic appearance of these grafts constitutes the crux of the entire
study. The very thin intimal layer of the original splenic artery was replaced
by a fine endothelial covering resting on a fairly dense layer of connective
tissue. The subendothelial fibrosis varied markedly from 1 specimen to another,
and in different parts of the same specimen; it may represent, in part, organiza-
tion of blood clot. The anastomotic junction was occupied by a wedge of fibrous
tissue with a thin overlying endothelial layer.

Preservation of the integrity of the media was the most striking charae-
teristic of the grafts. In animals sacrificed at 2 months, 4 months, and at 6

9
 

Fig. 5A, Survival of media of fresh arterial autograft, postoperative 137 days. B, Col-
lagenous degeneration of media of fresh aortic homograft, postoperative 83 days. (Masson
stain, original 180.)

10
months the thickness of the media was the same as in the original splenic artery.
A slight to moderate increase in connective tissue was revealed by the Masson
stain, but survival of most of the muscle cells of the media was the rule. This
is in direct contrast to the fate of the media in homografts, where collagenous

A,

 

B,
*
Fig. 6.—A, Normal splenic artery, and B, splenic artery—aortic graft 195 days after
insertion, Note subendothclial fibrosis, survival of media, and extensive thickening of ad-
ventitia (organized Gelfoam). (Masson stain, original 180.)

degeneration and connective tissue replacement occur uniformly. Pibrillation
and thinning of the elastic tissue laminae were also less in the autografts than
in the homografts (Fig. 5).

In 2 dogs, sacrificed 3 and 4 months postoperatively, it was noted that the
integrity of the media was distorted to a far greater degree than in the other

il
specimens. The thickness of the media was considerably diminished, and there
was a substantial reduction in the number of surviving muscle cells. In these
specimens also the intimal layer was much thicker than in the others, suggesting
a more intense reaction, possibly traumatic. Compromised survival of the media
in these specimens may have been on the basis of compression between thick
intimal and dense adventitial layers. This suggestion receives support from
study of adjacent areas in a 3 month transplant: the media is intact beneath
a thin intima, and markedly changed in the region of a thick intima. Nourish-
ment of the innermost layers of the media by oxygenated blood in the lumen of
the vessel is also indicated by a comparison of these two zones, in which the
adventitia is of uniform thickness and the appearance of the media is correlated
with changes in the intima.

A remarkable transformation of the thin adventitia of the graft to a thick
dense laver of connective tissue accompanied the organization of the Gelfoam.
This was in progress in a 2 month specimen, and complete at 3 months. The
newly formed outer wall was liberally supplied with blood vessels in all of the
specimens (Fig. 6).

The homologous transplants utilized for comparison with this group of
fabricated autografts were obtained from a series of aortic grafts carried out
by one of us (E. 5. H.) with Dr. Robert E. Gross in the surgical research labora-
tory ot the Children’s Hospital, Boston, in 1947. Resection of a segment of
the abdominal aorta in dogs was performed under the same conditions as in the
present experiments. The gap was bridged by a fresh segment of aorta taken
from donor dogs in 10 animals, with 2 deaths. Transplantation of aortic seg-
ments preserved for 6 hours in Ringer’s solution at ordinary icebox tempera-
tures was performed 9 times, with 2 deaths. The technique of anastomosis was
constant in all the operations. The dogs were sacrificed after periods ranging
from 2 months to 1 year postoperatively; in cach series there were 5 grafts
classified as good to excellent. The degeneration of the media and replacement
by fibrous tissue in these specimens conform to the biologie behavior pattern
described by others for fresh and preserved homotransplants.”: 1% ™ 31-34

DISCUSSION

At the third annual meeting of the Society for Vascular Surgery in At-
lantie City on June 5, 1949, Dr. Julian Johnson and his co-workers’ presented
the use of autogenous femoral vein grafts to construct shunts in 2 patients
with cyanotic heart disease. In the discussion which followed this paper it
was stated by Dr. Gross, and generally agreed, that the repair of blood vessel
defects should be accomplished by direct end-to-end approximation of the ves-
sel, by a fresh autogenous graft, or by a preserved homograft, in that order of
preference. The lack of availability of arterial tissue has prevented the use of
fresh autogenous arterial grafts for bridging gaps in the aorta. This was re-
emphasized by various discussants at the seventy-first annual meeting of the
American Surgical Association in April, 1951.

If the histologic integrity of the media of a graft is of importance—and it
is difficult to think that it would be unimportant—this demonstration of the

12
feasibility of constructing autogenous arterial grafts may have potential clinical
application. In a series of observations based on 17 autopsies on adult human
beings in the Pathology Laboratory of the Montefiore Hospital,* the circumfer-
ence of the splenic artery measured 1 to 1.5 em. in 68 per cent of the examina-
tions, the circumference of the thoracic aorta measured 5 to 7 em. in 71 per cent,
and that of the abdominal aorta 4 to 5 em. meters in 60 per cent. Approximately
10 to 12 em. of splenic artery were estimated as being surgically accessible.
These relative measurements are comparable to those in the dog, and indicate
the suitability of this tissue for aortie grafts. The splenic artery is accessible
from either the abdomen or the left side of the chest.

The observations made in these experiments would tend to confirm the con-
cept that the intimal surface of the graft is replaced by cellular elements from
the host, and that the ingrowth of endothelium commences from the host at
each end of the graft. This seems more likely than the formation of endo-
thelium from the organization of blood elot in situ as suggested by Wylie and
associates.*> Support is also lent to the impression of Sako and co-workers*é
that the longitudinal suture lines may act as struts along which the growth of
endothelium may be accelerated. These authors transplanted tubular grafts,
constructed from pericardium and from fascia, between the divided ends of
the thoracic aorta in dogs. Thickening and dilatation of the transplants oc-
eurred, with the deposition of atheromatous material.

The density of the newly formed adventitia, resulting from organization
of the Gelfoam, compared favorably with that described by Wvylie®® following
the use of fascia lata as a support around weakened arteries. The importance
of the adventitia in terms of the bursting strength of an artery has been doeu-
mented by Winternitz and co-workers.*7 Organization of the Gelfoam in these
experiments suggests the usefulness of this material in reinforcing vaseular
suture lines, transplants, and blood vessels that have been subjected to surgery.
This behavior of Gelfoam contrasts with the persistence of the substance in the
intracranial cavity, where it has been found almost unchanged as long as 2
years after insertion.®®

The growth of anastomotic suture lines®® and of fresh autogenous aortie and
vena caval grafts has been demonstrated? Growth of the fabricated auto-
eraft is under investigation. It is not suggested that the splenic artery affords
the only or the best source of tissue for a fabricated autogenous arterial graft.
Excessive tortuosity and advanced atherosclerosis may eliminate this vessel at
times. Other sources of arterial tissue merit consideration.

SUMMARY

1. A technique has been devised for the fabrication of fresh autogenous
arterial transplants from segments of the splenic artery.

2. Tubular grafts may be fashioned to any required diameter.

3. Grafts constructed from segments of the splenic artery have been used
to bridge a gap in the abdominal aorta in a series of dogs.

 

*By Dr. Stanley Altman.

13
4. An adequate functional result has been obtained, with long-term patency
of the grafts and survival of the animals.

5. Preliminary histologic observations, in survival studies up to 6 months
postoperatively, indicate preservation of the integrity and survival of the muscle
cells in the media of the grafts.

6. These fresh autogenous arterial grafts are functionally equal to, and
anatomically superior to, aortic homografts.

7. The disadvantages of splenectomy and the time required to construct
the graft are offset in part by eliminating the problems of supply, sterilization,
preservation, and the biologic specificity of tissue proteins.

8. Fresh autogenous vein grafts are ideal for bridging gaps in arteries of
small to moderate size. The use of fabricated fresh autogenous arterial grafts
is recommended for defects involving the aorta.

We are grateful to Dr. Harry Zimmerman, Chief of the Laboratory Division of the
Montefiore Hospital, for his guidance in interpreting the histologic preparations, and to Dr.
Joel Schwartzman of the Department of Roentgenology for his help in aortography.

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