Everting versus Inverting Gastrointestinal Anastomoses:
Bacterial Leakage and Anastomotic Disruption
JoHN A. RUSCA, M.D., GEORGE H. BORNSIDE, PH.D.,
ISmORE COHN, JR., M.D.
From the Department of Surgery, Louisiana State University School of Medicine,
New Orleans, Louisiana
MOST investigations of intestinal anasto-
moses have been concerned with the his-
tology or tensile strength of the healing
anastomosis. Few have focused any atten-
tion on the microbiological problems re-
lated to spillage of intestinal contents dur-
ing the anastomosis or the leakage of bac-
teria through the completed anastomosis.
This study was designed to obtain a better
understanding of the microbial dynamics
during and after the performance of evert-
ing and inverting anastomoses.
Our studies were stimulated by the re-
ports of Ravitch and his colleagues 2 7, 8
which indicated that everting and invert-
ing anastomoses were essentially equivalent
in many respects, including their tendency
to break down and lead to fatal peritonitis
if the anastomotic area were wrapped with
an impermeable sheet so that normal peri-
toneal defense mechanisms could not aid
in "cleaning up" the anastomotic area.
In an attempt to pinpoint more accu-
rately the source and extent of bacterial
leakage, we divided our investigation into
two different phases, each designed to
study one portion of the leakage associ-
ated with an intestinal anastomosis. Since
intestinal anastomoses in dogs could be ex-
Presented at the Annual Meeting of the South-
ern Surgical Association, December 9-11, 1968,
Boca Raton, Florida.
Presented at the meeting of the Southern Sur-
gical Association, Boca Raton, Florida, December
9-11, 1968.
Suipported in part by Grant Al 01600 and
Grant FR-00272 from the National Institutes of
Health.
727
pected to heal under most conditions, it be-
came obvious that a proper study of micro-
biological changes would require special
technics designed to emphasize minor
variations. Both phases therefore include
the introduction of technics designed to
study a single facet of everting and invert-
ing intestinal anastomoses.
A study of bacterial leakage after an in-
testinal anastomosis would have to be done
using an exogenous "marker organism"
since bacterial spillage occurs with any
anastomosis, no matter how aseptic the sur-
geon's technic. The first phase was thus an
evaluation of the amount of leakage of a
non-resident "marker organism" injected
into the bowel after the anastomosis was
completed. The second phase, a study of
the effects of bacterial spillage during the
anastomosis would have to rely on some
special mechanism, since normal spillage
usually is not associated with any delete-
rious effects. If the area of the anastomosis
could be isolated from the peritoneal de-
fense mechanism, as suggested by Ravitch,
then the sequelae of this spillage might be
evaluated. The two portions of this investi-
gation should extend our knowledge of the
microbial dynamics of inverting and evert-
ing intestinal anastomoses.
Leakage from the Completed
Anastomosis
Mature mongrel dogs, 9 to 21 Kg., were
utilized. The animals were fasted for 24
hours prior to operation. All procedures
were conducted under aseptic technics,
 RUSCA, BORNSIDE AND COHN
728
) rbacteria injecdte
alcohol spog
alcohol
(,//1
cultured \g lgued
gentian violet
FIG. 1. Sequence of steps for injecting bacteria
into segmiient of ileunl proximal to the anastomosis.
The area to be injected is seen through eye-hole
of drape, and is only exposed part of bo A el. The
sequential steps are: bowel cleansed with alcohol,
bacteria injected, bowel wiped again, tissue adhe-
sive to injection site, site marked with gentian
violet, and contact culture obtained from the site.
with all personnel in caps, masks, gowns
and gloves. The animals were anesthetized
with the intravenous use of 1 ml./Kg. of a
3%c sodium nembutal solution. The animals
were shaved, prepared with alcohol and
Joprep, and draped in a sterile fashion.
Through a midline lower abdominal inci-
sion, a spot in the ileum 45 cm. proximal
to the ileocecal junction was located. This
area was milked free of its contents and
rubbershod intestinal clamps were placed
across the bowel. The intestine was divided
and a section of the ileum at this point was
removed for bacteriological culture.
A one-layer, open anastomosis was per-
formed, using either an inverting or an
everting stitch. Simple, vertically placed,
interrupted through and through stitches
of 3-0 silk were used for the everting anas-
tomosis. An interrupted Connell stitch of
3-0 silk was used for the inverting anasto-
mosis. Subsequently, a sterile eye sheet was
placed so as to cover the operative field,
inistrulmenits aind tray, leavinig visible onEl
ani area of the ileum 25 cm. proximal to
Annals of Surgery
May 1969
the anastomosis (Fig. 1). All other areas
were thus protected from any spillage of
the bacterial culture. The visible area of
the ileum was cleaned with an alcohol
sponge. At this point, an overnight broth
culture of Serratia marcescens containing
approximately 109 bacteria per ml. was
sponge
brought onto the field. Five ml. of this sus-
pension were injected into the lumen of
the bowel through a 30 gauge needle with
moderate pressure so that none of the S.
marcescens contaminated the field. The
needle was withdrawn and the area
cleansed with Joprep and alcohol, marked
with gentian violet, and sealed with methyl
2-cyanoacrylate monomer tissue adhesive.
The needle site was cultured using a 65
by 13 mm. plastic contact plate (RODAC,
Falcon Plastics) containing Trypticase Soy
Agar (BBL) firmly touched to the area.
The eye sheet and other sterile coverings
were removed, and the surgeon changed
his gloves to insure against any subsequent
contamination. The culture of S. marces-
cens was milked to the area of the anasto-
mosis. The bowel was returned to the ab-
domen, which was closed in two layers.
S. marcescens was used as a marker or-
ganism since it usually is not found in the
gastrointestinal tract of the dog. Cultures
of the transected bowel provided assurance
that this species was not present when the
anastomosis was performed. The contact
plates were incubated at room temperature
for 48 hours to allow the S. marcescens to
produce its characteristic red pigmented
colonies during growth. The number of red
colonies was counted and recorded. Other
bacteria known to have been spilled during
the anastomosis were noted on the contact
plates. However, they were neither identi-
fied nor counted.
Fifty dogs were used. They were chosen
at random for placing in the inversion or
eversion anastomosis group and in the
group to be re-explored at 2, 4, 6, 12, or
24 hours. The original injection site, anasto-
XVolume 169
Number 5
EVERTING VERSUS INVERTING GASTROINTESTINAL ANASTONIOSES 729
TABLE 1. Number of Pigmented Colonies of Serratia marcescens on Contact Plates
Indicating Leakage from Anastomoses
E-erting Anastomosis Inverting Anastomosis
Initial Re-exploration Initial Re-exploration
Time of Re- Dog Site of Site of Anasto- Perito- I)og Site of Site of Anasto- Perito-
exploration No. Injection Injection mosis neum No. Injection Injection mosis neum

Hours
11 () 1 1 4 16 0 0 0

48 () () 0 0 49 1 1 1 2
2 29 3 0 0 2 0 0 ()
27 (3 14 120 17 1 0 2 ()
9 1 () 0 0 39 0 0 0 0
41) () () 0 1 14 () 0 (1

6 () () 0 12 1 0
4 7 () () 1 45 12 0 9 ()
32 () 0 0 0 24 1 0 () 0
3 () 0 0 0 33 () () 0

35 () 0 28 () () ()
5 () 1 15 4 0
6 22 () () 4 0 0 () ()
19 0 () 0 () 25 () () ()
31 0 0 1 () 46 0 0 0 ()
12 6 () () () 37 0 0 0 ()
34 2 0 0 50 0 0 0
12 13 I ( I 1 19 23 1 () 0 ()
21) 0 () () () 43 0 0 0
42 1 0 30 0 44 0 () 0
30 I 0 0 8 0 0 () ()
36 () 16 17 1() 18 1) 0 120 0
24 41 (0 0 0 21 0) 0 0

26 3 () 1 0 38 () 0 0 ()
l () 0 () 47 0) 0 0 0

mosis, and peritoneum were sampled with
contact plates when each animal was re-
opened. The animals were not used fur-
ther in this investigation.
Results
The fifty animals studied were divided
into five groups of 10 dogs. Each of these
groups was assigned to one of the five pe-
riods at which it was to be re-explored-2,
4, 6, 12, or 24 hours. Each group of 10 ani-
mals was further subdivided into an evert-
ing and an inverting anastomosis group of
five animals (Table 1).
The injection site was cultured immedi-
ately after the injection in all animals, and
again at the time of re-exploration. S. mar-
ceseen.s was grown from the injection site
of 15 dogs immediately after the injection
and cleansing of the bowel. It would thus
appear that in most instances the organisms
either were not spilled or that the body
defense mechanisms were able to dispose
of the small numbers spilled. This obser-
vation is further strengthened by the ab-
sence of S. marcescens at the injection site
in all but four animals cultured at re-explo-
ration-three at 2 hours and one at 24
hours, which probably come from leakage
at the anastomosis.
Leakage occurred at the anastomosis, as
determined by positive cultures for S. mar-
cescens, in seven animals with everting
anastomoses and four animals with invert-
ing anastomoses. The marker organism was
found on the peritoneum in seven animals
with everting anastomoses and one animal
with an inverting ainastomosis. In four of
these animals, all wvith everting ainasto-
moses, the marker wvas found both at the
anastomoses and on the peritoneum.
730 RUSCA, BORNSIDE AND COHN
,, P/astic
Sutured to mesentery
FiG. 2. Technic of wrapping the intestinal anas-
tomosis with plastic sheet, and anchoring the plas-
tic to the mesentery.
The total amount of bacterial leakage
under any circumstances appears to be
quite small. In view of the 5 x 109 organ-
isms injected, the highest colony counts of
120 represent only minimal leakage. Since
we accepted the presence of even a single
colony as evidence of leakage, this tended
to emphasize the possibility of leakage
under conditions where this amount of
spillage would be of no clinical importance.
The presence of S. marcescens at either
the anastomosis or on the peritoneum was
taken as an indication of leakage from the
anastomosis and not from the injection site.
On this basis, leakage occurred from 10
everting anastomoses (40%) and from
four inverting anastomoses (16%). This
difference is not statistically significant (chi
square with Yate's correction = 2.48; P be-
tween 10%7o and 15%o).
Bacterial leakage would appear to be of
no consequence after completion of either
an inverting or an everting anastomosis.
Spillage during Performance
of the Anastomosis
A second study using 81 dogs employed
the methods already described for inverting
and everting anastomoses. A single thick-
ness of supple, sterile, 48 gauge polyethyl-
ene plastic sheeting was placed around the
anastomosis (Fig. 2). The 4" by 4" plastic
was secured as a tubular sleeve over the
intestine and extended 11/2" to 2" on either
side of the anastomosis. The plastic was
sutured to the mesentery using 3-0 silk
Annals of Surgery
May 1969
placed so as not to compromise blood sup-
ply to the anastomosis. The intestine was
returned to the abdominal cavity and the
abdomen closed in two layers.
Postoperatively each dog was allowed
water after 24 hours and food after 48
hours. No antibiotics were given to any
animal except as an irrigating fluid de-
scribed below. No other special precautions
were taken. Animals were autopsied within
24 hours of death and moribund animals
were sacrificed for convenience. Animals
which lived 3 or more weeks after the op-
eration were considered to have recovered
and were sacrificed to ascertain the condi-
tion of the anastomosis.
The anastomoses were wrapped with
solid plastic in 22 dogs. In 17 dogs the
plastic was perforated with a 15 gauge
needle (approximately 60 holes/square
inch) as a means of permitting access of
peritoneal defense mechanisms to the anas-
tomotic site.
In 30 dogs, normal saline or 17o kana-
mycin or both in amounts of 500 ml. and
100 ml., respectively were used to irrigate
the completed anastomosis and its envelop-
ing plastic wrap. Irrigation was utilized to
decrease the amount of bacterial contami-
nation following completion of the open
anastomosis. In three of these dogs, 1 gram
of kanamycin in 10 ml. normal saline was
injected intraluminally into a 20 cm. seg-
ment of bowel isolated between rubber-
shod clamps. Twenty minutes later the
bowel was divided and re-anastomosed in
this area.
Nine animals served as controls in order
to ascertain the effects of the plastic alone,
and soiling the peritoneum with a piece
of ileum only. Two germfree animals were
used to evaluate an inverting anastomosis
wrapped with solid plastic.
Results
Control studies summarized in Table 2
exonerated several potential trouble spots
Volume 169 EVERTING VERSUS INVERTING GASTROINTESTINAL ANASTOMOSES 731
Number 5
by demonstrating that fatal peritonitis was TABLE 2. Control Procedures Demonstrating
not produced by any of the following: plas- Absence of Peritonitis
tic wrapped about normal ileum, an invert- No. Perito-
ing anastomosis adjacent to wrapped nor- Plastic Wrapped Dogs nitis
mal ileum, a free 1 cm. ileal segment from
a donor dog placed in the peritoneal cavity
Normal ileum 1 0
to provide exposed mucosa comparable to Normal ileum adjacent to invert-
that of an everting anastomosis. A similar ing anastomosis 2 0
challenge with mucosa bound to normal Inverting anastomosis in germfree
dog 2 0
ileum beneath plastic wrap was non-lethal
also. Normal ileum having donor ileal
segment with exposed mucosa
Everting anastomoses led to fatal perito- bound beneath the plastic wrap 1 0
nitis from anastomotic disruption in 10 of Normal ileum; (donor ileal seg-
11 animals wrapped with solid plastic ment free in peritoneal cavity) 1 0
(Table 3). If the anastomosis was wrapped No plastic wrap; (donor ileal seg-
with solid plastic and irrigated with normal ment free in peritoneal cavity) 2 0
saline and/or 1%o kanamycin, peritonitis
followed in 14 of the 17 animals. Peritonitis TABLE 3. Peritonitis after Wrapping Anastomoses
occurred also in the one dog with intra- with Plastic Sheets
luminal administration of kanamycin prior
Everting Inverting
to an everting anastomosis wrapped with anastomosis anastomosis
solid plastic.
No. Perito- No. Perito-
Inverting anastomoses wrapped with Treatment Dogs nitis Dogs nitis
solid plastic produced no sequelae in any Solid wrap 11 10 11 0
of the 11 animals so treated (Fig. 2). When Solid wrap and irriga-
an inverting anastomosis was wrapped with tion with saline and/
or kanamycin 18 15 12 2
solid plastic and irrigated with normal sa- Perforated wrap 7 0 10 0
line and/or 1%o kanamycin, only two of 12
dogs developed fatal peritonitis. Two dogs
pre-treated with intraluminal kanamycin studying intestinal anastomoses under nor-
prior to an inverting anastomosis and solid mal intraperitoneal conditions.
plastic wrap did not develop any difficulties.
Thus, peritonitis occurred in 25 of 29 Discussion
dogs with everting anastomoses wrapped Halsted's 1887 paper on intestinal su-
with solid plastic, as compared with only
2 of 23 dogs with inverting anastomoses. ture,6 stated the problem then as now:
By contrast, peritonitis did not occur in
"The chief danger of infection of the
any of the 17 dogs when the anastomosis
peritoneal cavity is manifestly from the
contents of the intestine, in case they find
was covered with a perforated plastic re-
gardless of whether an inverting or evert- their way through the wound in the intes-
tine or along the lines of suture. There is
ing anastomosis was employed. a possibility of the escape of intestinal con-
These results indicate clearly that the tents at the time of the operation, but this
inverting anastomosis had a distinctly supe- is a danger which can be readily guarded
rior ability to tolerate conditions of stress. against and one which is much less likely
The similarity in response of the two types to be attended by serious results than the
of anastomoses when a perforated plastic escape of intestinal contents into the peri-
was used, highlights the difficulties of toneum subsequent to the operation."
 RUSCA, BORNSIDE AND COHN
732
EVERTING NVERT ING
~~%
0 0
I7I
I7
18
M Perfor/its
IM No peritonitis
FIG. 3. Incidence of peritonitis in three types
of experiments with everting and inverting anasto-
moses. Solid plastic wrapped group at top, per-
forated plastic wrap in center, and solid plastic
wrap with irrigation at bottom.
Even though the problem was outlined
this clearly in Halsted's early writings, little
has been added since then to clarify the
importance of bacterial leakage during or
after the operative procedure. In the pres-
ent study, we have attempted to define the
role of bacterial spillage during the opera-
tive procedure and the leakage of micro-
organisms through the suture line in the
period following the anastomosis as a
means of determining what influence these
organisms might have on the subsequent
healing of the anastomosis.
While our interest has centered on the
microbial dynamics associated with an in-
testinal anastomosis, we have taken advan-
tage of the opportunity to study simultane-
ously the relative features of an inverting
and an everting anastomosis. The reputed
advantages of the everting technic have
been responsible for the continuing interest
in this form of intestinal anastomosis, in
spite of the fact that most clinicians do
not use it and in spite of the repeated dem-
onstrations of the advantages of the invert-
ing technic.
This study indicates that leakage is not
a major factor once a technically satisfac-
Annals of Surgery
May 1969
tory anastomosis has been completed, re-
gardless of whether it be an inverting or
100 an everting anastomosis. This is consistent
with the findings of Getzen, Roe, and Hol-
loway 4,5 whose studies of the histology of
inverting and everting anastomoses demon-
strated sealing with either fibrin or epithe-
lium within 4 hours after operation. Thus
I0 one would conclude that the occasional
anastomotic disruption is not related to the
"normal" bacterial leakage after the anasto-
mosis, but rather to a technically unsatis-
12 factory anastomosis.
Since most intestinal anastomoses heal
without difficulty under normal circum-
stances, special conditions must be used
to detect minor differences between invert-
ing and everting anastomoses. Ravitch and
his colleagues were the first to explore small
bowel healing when the anastomosis was
wrapped with a plastic sheet. The idea was
conceived as a method to evaluate the role
of adhesions in bowel healing, but rapidly
developed into a technic for comparing mi-
crobiological problems of inverting and
everting anastomoses. "With either invert-
ing or everting anastomosis there is an al-
most universal disruption of the suture line
if the region of the anastomosis is lightly
wrapped with a sheet of pervious or imper-
vious foreign material" is a conclusion of
one report and is repeated in another.2 It
seems to us that their data do not support
this statement. Ravitch, Rivarola and Van-
grov 8 reported 25 polyethylene-wrapped
everting anastomoses, with peritonitis de-
veloping in all 25. In contrast, peritonitis
developed in only three of nine similarly
wrapped inverting anastomoses. Canalis
and Ravitch 2 reported on 60 intestinal
anastomoses, all wvrapped with plastic, two
groups with everting and three with invert-
ing anastomoses. In the two groups with
everting anastomoses, 23 of the 24 animals
died of peritonitis. By contrast, in the three
groups wvith inverting anastomoses, 28 of
36 dogs died. In four of the eight survivors
V'olume169 EVERTING VERSUS INVERTING GASTROINTESTINAL ANASTOMOSES
Number 5
there was a possibility that the plastic wrap
was displaced. Although these differences
are not statistically significant, they suggest
that the two forms of anastomoses are not
equivalent, and that the everting anastomo-
sis is less stable than the inverting.
Our studies indicate that when the anas-
tomotic line is effectively isolated from the
remainder of the peritoneal cavity by a
solid plastic wrap, the everting anastomosis
leads to a fatal peritonitis almost uniformly
while the inverting anastomosis leads to
survival. When the plastic wrap is per-
forated so that isolation is no longer effec-
tive each form of anastomosis is equally
good.
The cause of anastomotic disruption in
this study lies in the isolation of the anasto-
mosis from the surrounding peritoneum and
its defensive mechanisms. Seclusion of the
anastomosis is complete when solid plastic
is used, as the peritoneum quickly adheres
about the edges of the plastic. Contamina-
tion of the area surrounding the anastomo-
sis is produced when any open anastomosis
is performed. Under normal circumstances
the peritoneum can handle this initial insult
without difficulty since bacterial leakage
ceases once the anastomosis is complete. If
an inverting anastomosis is wrapped with
solid plastic this relationship is not seriously
compromised, since serosa-to-serosa contact
of the bowel reproduces the continuity of
the bowel surface. However, when the
everting technic of anastomosis is used, an-
other factor is introduced and the animals
do not survive.
The only obviously different factor be-
tween the two types of anastomoses is the
rim of protruding mucosa when the evert-
ing technic is used. This everted mucosa
may 1) alter the peritoneum's response to
infection, or, 2) it may serve as a focus for
some new activity.
Several findings show that everted mu-
cosa alone does not alter the ability of the
peritoneum to combat contamination:
733
1. the safety of the everting technic
when it is employed under normal circum-
stances;
2. the lack of serious reaction to the in-
traperitoneal placing of an everted segment
of intestine;
3. previous experiments in which a ster-
ile, isolated, open loop of small bowel was
allowed to drain into the peritoneal cavity.3
The difficulty, therefore, does not lie in an
alteration in the response of the peritoneum.
The everted mucosa may serve as a focus
for an activity that would not be detected
when anastomoses were compared under
ordinary conditions. The extruded mucosa
may become a nidus for infection as a re-
sult of bacteria lodged within the mucosal
folds and protected by the impervious plas-
tic sheet from the normal peritoneal de-
fenses. Bacterial growth which can flourish
in the everted mucosa leads to the destruc-
tion of the anastomosis with ensuing fatal
peritonitis. Although it might seem that ir-
rigation with saline or antibiotics would
eliminate this complication, even copious
irrigation would not be able to eliminate
all the bacteria in the folds of intestinal
villi, and therefore failure of this technic
to alter the results is not surprising. The
combined data for experiments with and
without irrigation strengthens the case for
the relative superiority of the inverting
anastomosis as compared with the everting
technic under conditions of stress.
Previous studies of other facets of anas-
tomotic technics in our laboratories have
confirmed the superiority of the inverting
technic. One study compared various types
of anastomoses in the common duct.1 Oth-
ers studied tissue adhesives for intestinal
anastomoses.1Y-11 The everting anastomosis
was not recommended in these studies
since anastomotic disruption occurred more
frequently than with other types of anas-
tomoses.
A study of the microbial dynamics of in-
verting and everting intestinal anastomoses
734
4RUSCA, BORNSIDE AND COHN RUG,May
has provided additional information re-
garding the healing process of the two
kinds of anastomoses and the mechanism
by which bacterial action might lead to
disruption of the anastomosis. Bacteria are
spilled during either type of open anasto-
mosis. Peritoneal defenses can protect the
animal from this spillage provided it is not
excessive, is not continuing, and is not iso-
lated from normal peritoneal defense mech-
anisms. If, however, there is a nidus of
mucosa in which bacterial growth can con-
tinue uninterrupted, then the anastomosis
may be destroyed. Such conditions exist in
the everting technic when it is shielded
from peritoneal defenses by the impervious
plastic, or when it is in locations outside
the peritoneal cavity, e.g., the thorax and
below the peritoneal floor. Irrigation with
saline or antibiotics may be helpful, but is
not sufficient unless there is the additional
safeguard of the peritoneal defenses to com-
plete the job of bacterial eradication. Re-
gardless of which type anastomosis is used,
there is essentially no leakage from the
anastomotic site once a technically satisfac-
tory anastomosis has been completed. Thus,
any difficulties must be related to events
occurring during the performance of the
anastomosis.
Evidence from a study of microbial dy-
namics indicates the inverting intestinal
anastomosis is safer than the everting
technic.
Summary
The microbial dynamics of intestinal
anastomoses have received inadequate at-
tention. Special technics were used to study
the role of bacteria spilled during anasto-
moses and in leakage afterwards. A pig-
mented, non-resident, marker bacterium
(Serratia marcescens) was used to demon-
strate that there is essentially no leakage
Annals of Surgery
1969
after completion of a technically satisfac-
tory inverting or everting anastomosis.
Wrapping an intestinal anastomosis with
either a solid or a perforated plastic film
provided a technic for determining the role
of bacteria spilled during performance of
open inverting and everting anastomoses.
Wrapped everting anastomoses had a
greater tendency to disrupt.
The results demonstrate the importance
of the normal peritoneal defenses in pro-
tecting open anastomoses from the minimal
spillage accompanying the usual procedure,
and emphasize the superiority of the in-
verting intestinal anastomosis.
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3. Cohn, I., Jr.: Strangulation Obstruction.
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4. Getzen, L. C.: Clinical Use of Everted Intes-
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