Vol. 22, No.
4 April 2000 V
CE Refereed Peer Review
FOCAL POINT
★Primary intestinal healing occurs
by direct bridging of the cut
intestinal layers with fibrous
connective tissue when good
apposition of wound margins
is achieved.
KEY FACTS
■ The submucosa has a high
collagen content and is
responsible for anchoring
intestinal sutures.
■ The greater omentum plays a
vital role in healing intestinal
wounds.
■ Growth factors are important
in regulating fibroplasia and
angiogenesis in healing intestinal
wounds.
■ Intestinal wounds heal best with
sutures that are placed relatively
close together under moderate
tension.
■ The risk for anastomotic leakage
is significantly increased in the
presence of peritonitis.
Healing of Intestinal
Anastomoses *
University of Illinois
Bradley R. Coolman, DVM, MS
Nicole Ehrhart, VMD, MS
Sandra Manfra Marretta, DVM
ABSTRACT: Intestinal wounds heal in three overlapping phases that are similar to the healing
pattern of other tissue. The lag phase begins immediately and is characterized primarily by lo-
cal inflammation that lasts approximately 4 days. The proliferative phase, or period of fibropla-
sia, begins around day 3 and lasts until day 14 after the wound was incurred. Intestinal wound
strength approaches that of normal bowel by the end of the proliferative phase. The matura-
tion phase occurs from days 10 to 180 after the wound was incurred and is associated with
collagen cross-linking and a slow gain in strength.
I
ntestinal wounds may heal directly across the defect if intestinal layers are in
close contact with each other (primary healing) or by indirectly bridging the
defect with increased amounts of collagen and neovascularization if intestinal
layers are inverting, everting, or overlapping (secondary healing). Secondary
healing of intestinal anastomoses is most common with all types of suture pat-
terns. Many factors influence intestinal healing. Factors controlled by veterinary
surgeons include blood supply, tissue handling, suture material, and anastomotic
technique. Patient factors that influence intestinal healing include age, nutrition-
al status, and presence of infection.
ANATOMY
The basic microscopic anatomy of the canine alimentary tract is similar from
the stomach to the large intestine.1,2 The intestinal wall consists of four layers: the
tunica mucosa, tela submucosa, tunica muscularis, and tunica serosa1,2 (Figure 1).
The mucosa consists of epithelial lining, supportive lamina propria composed
of loose reticular fibers, and muscularis mucosa (thin layer of smooth muscle).1,2
The epithelial surface is covered with innumerable villi that increase the absorp-
tive surface area of the gut. The thickness of the epithelium and the nature of villi
vary from region to region in the canine gastrointestinal (GI) tract. The lamina
propria is composed of loose connective tissue meshed in a reticular fiber frame-
work. Within the lamina propria are blood and lymph vessels, fibrocytes, smooth
muscle cells, leukocytes, plasma cells, and mast cells. The muscularis mucosa is
composed of thin inner circular and outer longitudinal layers of smooth muscle,
*A companion article entitled “Historical Perspective of Intestinal Anastomosis in Veteri-
nary Surgery” appeared in the March 2000 (Vol. 22, No. 3) issue of Compendium.
Small Animal/Exotics Compendium April 2000

which allow the mucosa to roll same as that of other tissue.4–9

1,2
into folds. However, intestinal wounds
The submucosa connecting regain strength more rapidly
the mucous membrane to the than do cutaneous wounds.4,5
tunica muscularis consists The healing process can be
mainly of coarse, loosely wo- loosely divided into three over-
ven, collagenous and elastic lapping phases: lag, prolifera-
fibers with a submucosal plexus tive, and maturation.4–9
of nerves, blood vessels, and lym- The lag phase of healing,
phatics.1,2 Because of its high which begins immediately after
content of connective tissue, the wound is incurred and lasts
the submucosa provides most for about 4 days,4–9 is charac-
of the strength for the GI tract terized by immediate vascular
and is used for anchoring su- constriction, fibrin clot forma-
tures during intestinal surgery.3 tion, inflammation, and ep-
Biochemical analysis shows Figure 1—Photomicrograph of the histologic layers of the ithelial migration. This phase
that the submucosa contains canine small intestine. (Trichrome Masson stain; original is the most critical period for
68% type I collagen, 20% type magnification, ×10) intestinal wound healing be-
III collagen, and 12% type V cause the anastomotic sutures
collagen.4 provide nearly all wound
The tunica muscularis con- strength during this period.
sists of a relatively thick inner Most intestinal dehiscence oc-
circular layer and a thinner out- Mucosa curs during the lag phase.4–6,10,11
er longitudinal layer of smooth Submucosa Increased inflammation pro-
Muscularis circular
muscle.1,2 The inner circular longs this phase and delays in-
Muscularis longitudinal
layer serves to segment and Serosa testinal wound healing.
mix ingesta, whereas the outer The proliferative (or repara-
longitudinal layer primarily tive) phase of healing begins
functions to propel ingesta on day 3 and lasts until day
through the GI tract. 1 The 14.4–9 Logarithmic prolifera-
serosa consists of a thin layer tion of fibroblasts occurs in
of connective tissue that cov- this period, during which
ers the muscular coat.1,2 A lay- large amounts of collagen are
er of mesothelial cells that produced. Wound strength
composes the peritoneum Figure 2—Primary healing of the intestinal wall as achieved increases rapidly; and by day
covers the outer surface. The with direct apposition of the submucosal layers. (Adapted 14, the strength of wounded
serous coat adheres closely to from Jansen A, Becker AE, Brummelkamp WH, et al: The intestine approaches that of
the muscular coat; the com- importance of the apposition of the submucosal intestinal normal bowel.7,8 Studies have
bined layers are often referred layers for primary wound healing of intestinal anastomosis. shown that the increased
Surg Gynecol Obstet 152:51–58, 1981; with permission)
to as the seromuscular layer.2 wound strength during the
Blood supply to the intesti- proliferative phase parallels
nal wall comes from the arcuate mesenteric arteries that the rising collagen content of wounded tissue.7,8 Healing
penetrate the tunica muscularis, branch off to create a wounds have a higher proportion of type III collagen
subserosal plexus and intermuscular plexus, and then than normal tissue does.8
continue into the tela submucosa where they form the The maturation phase proceeds from days 10 to 180
submucosal plexus.1,2 The submucosal vascular plexus after the wound is incurred.4–9 This phase of wound
provides the primary blood supply to the GI tract.2 Ar- healing is less important from a clinical standpoint be-
terioles from the submucosal plexus supply the tunica cause bowel strength is already adequate to prevent
mucosa and give rise to the capillary network in the in- leakage or dehiscence. During the maturation phase, a
testinal villi.1,2 slow increase in wound strength is observed as the col-
lagen fibers reorganize, mature, and return to normal
OVERVIEW OF INTESTINAL WOUND HEALING proportions.7,8
The basic healing pattern of intestinal wounds is the Jansen and colleagues12 performed experiments on small

ROLE OF SUBMUCOSA ■ INTESTINAL BLOOD SUPPLY ■ HEALING PHASES

Compendium April 2000 Small Animal/Exotics

intestine healing in dogs and infection.13–17 Thus many sur-

reported that histologic wound geons recommend wrapping
healing depended on the accu- intestinal anastomoses with the
racy of apposing the layers of Mucosa omentum during surgery. The
bowel wall. These researchers Submucosa
omentum must be viable to as-
Muscularis circular
compared conventional dou- sist healing—free omental
Muscularis longitudinal
ble-layer, hand-sewn inverting Serosa grafts have been shown to be
anastomoses with those created ineffective.5,16 Leakage rates of
using a magnetized anastomot- experimental anastomoses are
ic ring apparatus that inverted high in dogs when the omen-
and compressed the mucosa tum has been removed, espe-
and submucosa, resulting in di- cially when everting suture pat-
rect apposition of both submu- terns are used.18,19 However,
cosal layers and sloughing of protection from the omentum
trapped mucosa. Direct bridg- enables healing of severely
ing of the defect and rapid compromised intestinal anasto-
restoration of epithelium was moses that would otherwise
described when good apposi- Figure 3—The secondary intestinal healing that occurs leak.14,17
tion of submucosal, muscular, with everting intestinal anastomoses. (Adapted from Macrophages are important
and serosal layers was achieved Jansen A, Becker AE, Brummelkamp WH, et al: The im- during wound debridement
using the anastomotic ring ap- portance of the apposition of the submucosal intestinal in the lag phase of healing.4
paratus (Figure 2).12 This pat- layers for primary wound healing of intestinal anastomosis. They also produce humeral
tern was described as primary Surg Gynecol Obstet 152:51–58, 1981; with permission) growth factors that modulate
intestinal healing.12 fibroplasia and angiogenesis
In cases of poor apposition in healing wounds. Important
of intestinal layers (hand- growth factors produced by
sewn everting, inverting, and macrophages include trans-
overlapping anastomoses), a forming growth factor-β (TGF-
different pattern of healing β), platelet-derived growth fac-
was observed. The anasto- tor (PDGF), epidermal growth
Mucosa
moses bridged with increased Submucosa
factor (EGF), and many cy-
amounts of collagen tissue, Muscularis circular tokines.20,21 By producing these
the vascular pattern was irreg- Muscularis longitudinal humeral factors, macrophages
ular with increased neovascu- Serosa play an important role in con-
larization from the submu- trolling the metabolism of
cosal plexus, and bridging of wounds.
the epithelial defect in the The healing of experimental
mucosal layer was prolonged wounds is reportedly facilitat-
(Figures 3 and 4). This type ed by TGF-β, PDGF, and
of wound healing with indi- EGF.20 Topical application of
rect bridging of the anasto- TGF-β accelerates intestinal
motic defect was called sec- wound healing in pigs.4 Ex-
ondary intestinal healing. 12 perimental intestinal anasto-
The researchers concluded moses created in rats with en-
that direct apposition of sub- Figure 4—The secondary intestinal healing that occurs hanced macrophage function
mucosal layers is required for with inverting intestinal anastomoses. (Adapted from had increased collagen cross-
primary intestinal healing. Jansen A, Becker AE, Brummelkamp WH, et al: The im- linking and greater tensile
The greater omentum is im- portance of the apposition of the submucosal intestinal strength at day 3 than did un-
portant in the healing of GI layers for primary wound healing of intestinal anastomosis. treated controls.20 However, in
wounds.5,13 The omentum seals Surg Gynecol Obstet 152:51–58, 1981; with permission) this study, the wound concen-
the anastomotic suture line, trations of TGF-β and PDGF
provides an external vascular supply, establishes lymphatic were lower in rats with enhanced macrophage function
drainage, gives rise to granulation tissue, and helps control than in controls.20 The researchers concluded that in-

INVERTING ANASTOMOSIS ■ DIRECT AND INDIRECT BRIDGING ■ GROWTH FACTORS

Small Animal/Exotics
testinal wound healing clearly depends on combinations
of many growth factors and cytokines and that acceler-
ated healing may depend on stimulation of certain fac-
tors and inhibition of others.
FACTORS AFFECTING
INTESTINAL WOUND HEALING
Increased inflammation in intestinal anastomoses
prolongs the lag phase of healing and delays the return
of strength at the suture line.22,23 Inflammation activates
collagenases in the intestinal wall that, along with pro-
teolytic enzymes from granulocytes, degrade existing
collagen and weaken the foundations in which anasto-
motic sutures are placed.4,5,23 Numerous factors affect
intestinal wound healing. Factors under the surgeon’s
control are monitoring the blood supply, handling tis-
sue gently, and choosing the appropriate suture materi-
al and anastomotic technique. Other factors that affect
healing include age of the patient, its nutritional status,
and presence of infection and concurrent diseases.
Blood Supply
Delivery of adequate blood supply and tissue oxygen
is essential for healing intestinal anastomoses.4 Because
hydroxylation of lysine and proline during collagen syn-
thesis depends on adequate oxygen delivery, inadequate
blood supply delays collagen formation.4 Intrinsic vascu-
lature must be preserved, and tissue of questionable via-
bility or with marginal perfusion should be removed.
Cutting the bowel edges at a 60˚ angle from the mesen-
teric border has been recommended to ensure adequate
blood supply at the antimesenteric aspect.6 Hypovo-
lemia and severe anemia can compromise oxygenation
and should be corrected before surgery. However, mild
normovolemic anemia does not impair oxygen transport
and has no effect on intestinal wound healing.4
Surgical Technique
Appropriate surgical technique dictates that surgeons
handle tissue gently, use fine instruments, dissect tissue
sharply, ensure adequate hemostasis, and avoid tissue
necrosis. Tissue must remain moist, and spillage of in-
testinal contents must be avoided. Although experi-
mental anastomoses in healthy dogs heal with widely
spaced sutures (up to 16 mm apart),24 improved healing
patterns are achieved by placing sutures relatively close
(2 to 4 mm) under moderate tension.25 Knots should
be tied securely but should not strangulate or cut into
tissue. Careful tissue handling and meticulous surgical
technique minimize damage to critical blood vessels as
well as tissue edema and necrosis.23 In addition, mobi-
lizing bowel ends adequately is important to prevent
BLOOD AND OXYGEN SUPPLY ■ TISSUE HANDLING ■ INFLAMMATORY RESPONSES
Compendium April 2000
tension on the anastomosis—tension can decrease per-
fusion and predispose wound dehiscence.26
Suture Material
There is no ideal suture material for intestinal anasto-
mosis. Both absorbable and nonabsorbable sutures of
synthetic and natural origins have been successfully
used.4,5,23 The suture should be strong enough to pro-
vide mechanical support but fine enough to minimize
tissue trauma and inflammatory response to a foreign
body. Because the intestine rapidly regains strength, su-
ture materials only need to retain holding strength for a
maximum of 10 to 14 days after anastomosis.23
Suture material is a foreign body and thus can pro-
duce an inflammatory response.23 Chromic gut causes
an increased inflammatory response, is rapidly degrad-
ed by phagocytosis, and is therefore not recommended
for intestinal anastomosis.4,5 Multifilament sutures have
increased tissue drag that can increase tissue damage
and inflammation caused by friction during place-
ment.23 In addition, multifilament materials produce a
scaffold in which microorganisms can proliferate and
thus should be avoided in the bowel.4,5 Synthetic ab-
sorbable monofilament (i.e., polydioxanone, polygly-
conate) and synthetic nonabsorbable monofilament
(i.e., nylon, polypropylene, stainless-steel) sutures are
associated with the least amount of inflammation and
are thus best suited for anastomosis.4,5,23 Because of the
rapid return to normal strength, nonabsorbable sutures
have no advantage over slowly absorbable synthetic su-
ture material. Suture sizes of 3-0 to 5-0 are recom-
mended for closing GI wounds in small animals.5,6
Suture Pattern
The suture pattern significantly affects the amount of
inflammation and anastomotic healing. Inverting su-
ture patterns are the most widely used patterns in hu-
man intestinal surgery.4 Inverting patterns form an im-
mediate serosal seal and are associated with fewer
adhesions than may occur with everting patterns.7,23
However, the inverted cuff of tissue typically loses its
blood supply, becomes edematous, and eventually un-
dergoes necrosis. The larger the inverted cuff of tissue,
the more severe the inflammatory reaction and the
greater the risk for luminal obstruction.7 Secondary
healing patterns are typically observed with inverting
anastomotic techniques.12
Everting suture patterns cause less initial narrowing
of the intestinal lumen than do inverting techniques.
However, everting patterns are associated with in-
creased adhesion formation and greater incidence of
anastomotic leakage.7,23 Many published studies have
compared inverting and everting anastomoses through-
Compendium April 2000
out the GI tract.27–37 It is clear that with everting anas-
tomoses, the role of the omentum and other peritoneal
defense mechanisms is increased because of the need to
seal the anastomosis and assist in healing.17–19 Although
everting patterns do not initially impinge on intestinal
lumen, stenosis of the anastomosis may result from ex-
traluminal adhesions and increased fibroplasia.4,5
Ideally, approximating anastomotic patterns for end–
to-end anastomoses would cause no luminal obstruc-
tion, have minimal adhesions, and result in primary in-
testinal healing. However, mucosal–mucosal apposition
results in eversion of extramucosal intestinal layers.37
Published studies document that approximating anas-
tomotic techniques generally result in eversion of the
mucosa, extensive adhesions, and secondary patterns of
healing in the intestine.38–40 Simple continuous patterns
for intestinal anastomosis are associated with better
gross and histologic apposition of intestinal layers and
have similar clinical results compared with simple inter-
rupted patterns.39,41
Single- Versus Double-Layer Anastomoses
Although Lembert, Halsted, and Connell all recom-
mended one-layer anastomoses, two-layer closures of
intestine became more common after Czerny modified
the Lembert technique.23 Double-row inverting tech-
niques became popular because they were believed to
provide more security against leakage.23 However, two-
layer anastomoses have been shown to cause more tis-
sue strangulation and edema, greater inflammatory
response, greater loss of collagen content, delayed heal-
ing, and higher rates of bowel obstruction than do sin-
gle-layer closures.4,23,42 Thus single-layer anastomotic
closures are preferred for most applications.4,5,43
Stapled Anastomoses
Mechanical stapling devices can also be used to create
inverting or everting end–end, end–side, or side–side
intestinal anastomoses.37,44–54 Reported advantages of
stapled anastomoses over hand-sewn techniques include
decreased tissue manipulation, shorter surgical time,
preservation of vascular supply, and superior initial
strength. 37,44–53 Mechanical stapling devices have been
successfully used for small and large intestinal anasto-
moses in dogs and cats.51–54
Experiments have shown that stapled anastomoses heal
with minimal inflammatory response and have greater
initial wound strength than do sutured anastomo-
ses.37,44,45,48,49 However, published studies reporting less
inflammation with stapled intestinal anastomoses com-
pared stainless-steel staples with chromic gut, which is
known to cause an intense inflammatory response.44,48,51
One study found that hand-sewn intestinal anastomoses
APPROXIMATING PATTERNS ■ MECHANICAL STAPLING ■ BIOFRAGMENTABLE ANASTOMOTIC RING
Small Animal/Exotics
had greater strength, increased lumen diameter, and
more rapid healing than did stapled anastomoses.50
Early reports concluded that stapled everting GI
anastomoses generally healed by primary intention in
contrast to hand-sewn inverting anastomoses, which of-
ten healed by secondary intention and had a marked
inflammatory response.18,37,44,48 This nomenclature is
confusing because the primary-intention healing de-
scribed in these reports is not the same process as the
primary intestinal healing described by Jansen and col-
leagues.12 All stapled intestinal anastomoses result in ei-
ther eversion or inversion of intestinal wall, depending
on the technique and instrument used.53 Therefore,
healing of stapled anastomoses will proceed by indirect
bridging by collagen fibers, or secondary intestinal
healing.12
Sutureless Intestinal Anastomoses
A biofragmentable anastomotic ring (BAR) for intesti-
nal anastomoses was first described by Hardy and
coworkers.55 This intraluminal device is made from ab-
sorbable polyglycolic acid and barium sulfate to render it
radiopaque.55–59 The BAR creates an inverting anastomo-
sis in which the cut intestinal ends are compressed by the
device and eventually undergo necrosis, which results in
fragmentation of the device and passing with feces.55–59
The immediate anastomotic strength of the BAR is
higher than that of sutured or stapled intestinal anasto-
moses, and the bursting strength during the lag and
proliferative phases of healing is similar.56–58 Healing is
equivalent to hand-sewn and stapled inverting anasto-
moses (secondary intestinal healing), but less micro-
scopic inflammation and foreign body reaction occur
during the maturation phase of healing because the im-
plants fragment and pass within 12 to 23 days.56 The
BAR is histologically associated with increased muscu-
lar inversion and fewer adhesions than occur with ap-
positional sutured anastomoses.59 The lumen diameter
of the healed BAR anastomosis is similar to that of oth-
er anastomotic techniques.55,59
Age
The incidence of anastomotic complications in hu-
mans increases with advancing age.4 Although this associ-
ation may be secondary to concurrent diseases more com-
mon in older patients, research has shown that advanced
age alone does not suppress the tensile strength, bursting
strength, or collagen content of intestinal anastomoses.60
Retrospective studies of GI wound dehiscence in dogs
found no association between age and dehiscence rate.10,61
Nutritional Status
Both prolonged and short-term malnutrition diminish
Small Animal/Exotics
anastomotic healing.4 The reason for decreased GI heal-
ing in malnourished patients probably results from hy-
poproteinemia, lack of amino acids needed for collagen
synthesis, and decreased immunocompetence associated
with malnutrition.4 Early enteral nutrition should be pro-
vided to GI surgical patients when possible because it
helps prevent ileus and sustains the intestinal barrier,
thereby helping prevent bacterial translocation.4,5 Total
parenteral nutrition should be considered in patients with
severe malnutrition and when nutrient requirements can-
not be met by enteral feeding for prolonged periods.62
Infection
Peritonitis and local infection lead to a higher rate of
anastomotic dehiscence by increasing inflammation and
promoting collagenase activity.7,22,63,64 In one study,63 exper-
imental infection resulted in lowered bursting pressures
and collagen content for ileal anastomoses. Dogs with
peritonitis have a significantly higher rate of GI wound
dehiscence.10 The risk for anastomotic leakage is reported-
ly increased by a factor of 20 for small intestinal anas-
tomoses in the presence of peritonitis.64 Humans with
peritonitis requiring intestinal surgery generally have a
temporary enterostomy until the infection is controlled.4,22
However, primary healing of GI anastomoses in the pres-
ence of generalized peritonitis has been documented.64
SUMMARY
To optimize GI wound healing, surgeons should use
atraumatic technique and attempt to accurately align the
transected layers of bowel wall. Single-layer, approximat-
ing, or mildly inverting anastomoses completed with 3-0
to 5-0 synthetic monofilament sutures in simple interrupt-
ed or simple continuous fashion are preferred. Sutures
should be inserted 2 to 4 mm from the wound edge,
through the submucosal layer of bowel wall, spaced at 2-
to 4-mm intervals, and placed under moderate tension for
optimal anastomotic healing. Anastomoses created with
automated stapling devices also have good clinical results
in small animals. Advanced age, poor nutrition, and infec-
tion may all increase the risk for intestinal wound dehis-
cence.
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About the Authors
When this article was submitted for publication, Dr. Cool-
man was chief surgical resident at the College of Veteri-
nary Medicine, University of Illinois, Urbana, Illinois. He is
currently affiliated with Veterinary Surgical Services, Fort
Wayne, Indiana. Drs. Ehrhart and Manfra Marretta are af-
filiated with the Department of Veterinary Clinical Sci-
ences, College of Veterinary Medicine, University of Illi-
nois, Urbana, Illinois. Drs. Ehrhart and Manfra Maretta are
Diplomates of the American College of Veterinary Sur-
geons, and Dr. Manfra Marretta is a Diplomate of the
American Veterinary Dental College.