Lopez 2019
Lopez 2019
DOI: 10.1111/vsu.13344
Daniel J. Lopez DVM | Galina M. Hayes PhD, DACVECC, DACVS | Gilad Fefer BS |
Sarah A. McCalla DVM | Denise F. LaLonde-Paul LVT, BS, MPS |
James A. Flanders DVM, DACVS | Julia P. Sumner BVSc, DACVS
Department of Clinical Studies, Cornell
University Hospital for Animals, Ithaca,
Abstract
New York Objective: To compare the effect of three methods of subcutaneous tissue closure
on postoperative incisional complications and pain in cats.
Correspondence
Galina M. Hayes, Department of Clinical Study design: Single-center, randomized, blinded, controlled trial conducted in a
Studies, Cornell University Hospital for veterinary teaching hospital.
Animals, 930 Campus Rd, Ithaca, New York
Animals: Two hundred ninety-seven cats undergoing midline celiotomy for
14853.
Email: [email protected] ovariohysterectomy (n = 280) or other abdominal procedure (n = 17).
Methods: Cats (n = 297) were assigned to one of three subcutaneous
Funding information
Cornell Feline Health Center, Grant/Award
closure methods: simple continuous apposition with tacking to the rectus
Number: 4808859 fascia (n = 108, quilting [Q] group); simple continuous apposition (SC;
n = 94); no subcutaneous closure (NC; n = 95). Primary outcomes were
incidence of seroma formation, postoperative pain, and surgical site infection
or dehiscence. Active follow-up was obtained at 10 and 30 days
postoperatively.
Results: Baseline characteristics did not differ between groups. Seroma was less
common in the Q group (13.0%) than in the NC (27.3%) and SC (25.9%) groups
(P = .03). Compared with the other two groups, the relative risk of seroma forma-
tion in the Q group was 0.49 (95% CI = 0.28-0.86, P = .01). Median mechanical
pain thresholds were higher (indicating greater comfort) in cats with subcutaneous
sutures (Q and SC = 1.23 [interquartile range (IQR), 0.2-2.6 N], NC = 0.83 [IQR,
0-1.87 N], P = .04) on the day after surgery.
Conclusion: Closing subcutaneous tissues with a quilting closure pattern reduced
seroma formation in cats undergoing celiotomy.
Clinical significance: Placing a quilting suture pattern in the subcutaneous tissues
after celiotomy is a simple low-cost measure that reduces seromas in cats.
Abstaining from subcutaneous closure cannot be recommended because of
increased seroma formation and pain.
Veterinary Surgery. 2019;1–8. wileyonlinelibrary.com/journal/vsu © 2019 The American College of Veterinary Surgeons 1
2 LOPEZ ET AL.
admission, a drain or vascular access port was placed in the were blinded to treatment group assignment (D.J.L., D.F.L-P.).
subcutaneous tissues, the cat was severely fractious limiting The US Centers for Disease Control and Prevention criteria for
handling, or lack of informed owner consent. Perioperative SSI were used.21 Diagnosis of seromas was based on physical
analgesia was administered in all cases with medication examination findings of a focal area of fluctuant fluid swelling
selection at the discretion of the supervising clinician at the incision site with an intact body wall and absence of
acording to institutional protocols. The clinician was blinded heat/redness. When required, ultrasound examination or fine-
to group assignment. The study was approved by the Cornell needle aspiration cytology was used to differentiate seromas
University Hospital for Animals Institutional and Animal from herniations or incisional abscesses.
Care Use Committee (No 2017-0062). Pain was assessed within the first postoperative day by
Cats were enrolled through the Cornell University Hospital using the feline composite pain scale (FCPS)22 and peri-
for Animals Soft Tissue Surgery Service for senior veterinary incisional mechanical threshold testing with a force algometer
student ovariohysterectomy or resident/faculty-performed with a 2-mm diameter probe head23 (Prodplus; Topcat
abdominal procedures, through the second-year veterinary stu- Metrology, Little Downham, Cambridgeshire, United King-
dent ovariohysterectomy laboratory, or through Shelter Out- dom). Systolic blood pressure was measured by using a
reach Services (Ithaca, New York) ovariohysterectomy clinics. 9.7-MHz doppler ultrasound infant style probe and unit
Power analysis identified a group size of 89 as sufficient (Model 811-BTS; Parks Medical Electronics, Las Vegas,
to provide 80% power to detect a seroma incidence differ- Nevada). Incisional appearance was assessed by using a 0 to
ence of 2% vs 13%. Randomization was performed with a 100-mm modified cosmesis visual analog scale (VAS)24 that
computer-generated random treatment assignment (GMH, evaluated degree of skin apposition, incisional inflammation/
STATA; StataCorp, College Station, Texas), with stratifica- swelling, and incisional discharge. With this scale, a score of
tion based on the admitting service. Randomization was 0 represented the most undesirable situation, and a score of
stratified in this manner to ensure that no treatment group 100 represented the most desirable situation. Evaluators (D.J.
experienced significant differences in surgeon type. Inter- L., G.F., S.A.M.) were blinded to the intervention group.
vention group assignment was revealed via premade sealed The total surgical duration for the procedure (skin inci-
envelopes at the time of surgery. sion to final skin suture) and the duration for the incisional
closure (start of the linea to final skin suture) were recorded
intraoperatively.
2.2 | Data collection and outcomes
The primary outcomes were the incidence of seroma and
SSI/dehiscence within the follow-up period and postopera-
2.3 | Statistical analysis
tive pain severity assessed on the first postoperative day. Continuous data were assessed for normality by using a Sha-
Secondary outcomes were the surgical time required for piro Wilk test. Normal data are reported as mean ± SD, and
incisional closure and incisional appearance assessed on the nonnormal data are reported as median (interquartile range
first postoperative day. Baseline data on cat age, body condi- [IQR]). Differences between all three treatment groups in con-
tion score (BCS), blood pressure, weight, illness severity tinuous baseline or outcome data were assessed by using an
(APPLE [acute patient physiologic and laboratory evalua- ANOVA test when data were normal or a Kruskal Wallis
tion] score),19 abdominal procedure performed, and surgeon equality of populations rank test where data were not normal.
experience were collected. Post hoc two-group comparisons were made by using a t test
Active follow-up to document incisional complications was when data were normal or a Wilcoxon rank-sum test when
performed at 10 and 30 days postoperatively with owners and data were not normal. Differences in categorical outcomes
referring veterinarians. At the 10-day time point, owners were between treatment groups were evaluated by using the χ2 test
encouraged to return to the hospital for in person administration when cell numbers were >5 and Fisher's exact test when cell
of a previously validated questionnaire20 and direct evaluation numbers were ≤5. The Wald approximation was used to cal-
of the incision. Owners unable to return were contacted by tele- culate 95% confidence intervals (95% CI) for proportions. All
phone, and the questionnaire was administered. A total of five analyses were performed in Stata 15 (StataCorp).
attempts at contact were made before an animal was considered
lost to follow-up. When the cat received treatment with the pri-
mary care veterinarian during the postoperative period, the vet-
3 | RESULTS
erinarian was contacted, and the details of findings and care
3.1 | Recruitment, participants, and follow-up
administered were obtained. The investigator applying the
questionnaire as well as the owner/caregiver and referring vet- Cats were recruited from Sept 12, 2017 until April 10, 2019
erinarians responsible for care during the postoperative period (Figure 2). The study was concluded after sufficient
4 LOPEZ ET AL.
FIGURE 2 CONSORT (Consolidated Standards of Reporting Trials) flow diagram of cat enrollment, treatment allocation, follow-up, and
analysis during the study period
enrollment to satisfy power calculations. Cats were recruited (NC) group vs eight of 108 (7.4%) and nine of 94 (9.6%)
from three sources: (1) cats presenting to the Cornell Univer- in the quilting (Q) and simple continuous (SC) groups
sity Hospital for Animals Soft Tissue Surgery Service for (P = .01), respectively. There were no group differences in
either elective ovariohysterectomy by a fourth year veteri- loss to follow-up by the 30-day time point, with loss of
nary student (n = 79) or for other nonspay abdominal proce- 32 of 108 (29.6%) in the Q group, 30 of 95 (31.5%) in the
dure performed by a resident or boarded surgeon (n = 17); NC group, and 34 of 94 (36.2%) in the SC group
(2) cats presenting for a second-year ovariohysterectomy (P = .60). Loss to follow-up resulted from either cat death
teaching laboratory (n = 89); or (3) cats presenting for prior to the 10-day evaluation or inability to contact the
ovariohysterectomy performed by either an experienced owner. The two deaths that occurred were unrelated to
shelter clinician, resident, or board-certified surgeon incisional complications and resulted from (1) euthanasia
(n = 112) in association with Shelter Outreach Services. secondary to hypovolemic shock and gastric outflow
Postoperative outcomes were assessed a median of 17 hours obstruction after pyloric mass removal and (2) euthanasia
(IQR, 15-19) after surgery. After hospital discharge, follow- secondary to unresponsive vasodilatory septic shock post
up occurred at a median of 10 days (IQR, 10-12) and cholecystectomy.
32 days (IQR, 31-42) postoperatively. The baseline characteristics of each treatment group are
No animals received a closure pattern that differed from presented in Table 1. There were no between-group differ-
study protocol; all analyses were by intent-to-treat. No cats ences in age, BCS, weight, illness severity, or baseline sys-
received a postoperative bandage of the surgical site. tolic blood pressure. There were no between-group
Treatment allocation by group stratification and follow-up differences in procedure type or urgency, whether prophy-
at 10-days and 30-days postoperatively are presented in lactic antibiotics were given, or the experience level of the
Figure 2. There were no group differences in the propor- surgeon.
tion of cases receiving veterinary evaluation at 10 days
postoperatively compared with owner evaluation (P = .28;
3.2 | Primary outcomes
Table 1). There were group differences in the proportion
of cases lost to follow-up at the 10-day time point, with Primary outcomes, including incisional complications and
the loss of 18 of 95 (18.9%) animals from the no closure postoperative pain measurements, are presented in Table 2.
LOPEZ ET AL. 5
TABLE 1 Baseline characteristics of cats in the quilting, no closure, and simple continuous subcutaneous closure groups
Note: Data are mean ± SD or median (IQR) except when indicated otherwise.
Abbreviations: APPLE, acute patient physiologic and laboratory evaluation; BCS, body condition score, BW, body weight; IQR, interquartile range; SBP, systolic
blood pressure.
Abbreviations: FCPS, feline composite pain scale; IQR, interquartile range; N, Newtons; PROD, Prodplus; Topcat Metrology; SSI, surgical site infection.
All seromas were identified within 10 days of surgery. mechanical threshold was higher in the sutured (1.23 N
The incidence of seroma was lower in the Q group [IQR, 0.2-2.6] compared with the unsutured (0.83 N [IQR,
(13.0%, 95% CI = 6.4-19.6) compared with the other two 0-1.87] group (P = .04). No between-group differences in
groups (NC = 27.3%, 95% CI = 17.3-37.2; SC = 25.9%, feline composite pain scale were identified. There was no
95% CI = 16.6-35.2). When compared with the NC and difference between treatment groups in the incidence of
SC groups combined, the Q group had a relative risk for SSI/dehiscence at any time point.
seroma of 0.49 (95% CI = 0.28-0.86; P = .01). The inci-
dence of seroma in the NC and SC groups was similar,
with a relative risk for seroma in the SC group of 0.95 3.3 | Secondary outcomes
(95% CI = 0.57-1.58; P = .84) compared with the NC
group. The secondary outcomes are presented in Table 3. Apposi-
There was some variation in median mechanical pain tion scores were lower for the Q group compared with the
thresholds between the three treatment groups (P = .11). NC and SC groups (P = .02). No other differences were
However, when sutured techniques (Q and SC) were com- noted in wound scores. There was no difference in incisional
pared with the unsutured technique (NC), median closure time between groups.
6 LOPEZ ET AL.
TABLE 4 Association between the incidence of seroma and surgeon experience within treatment subgroups
Nonstudent
Student surgeon, P- 4 | DISCUSSION
Pain variable surgeon, n = 168 n = 112 value
Pain score 3 (2-5) 0 (0-1.5) <.001
In this study, we evaluated the effect of various subcutane-
ous closure techniques on incisional complications and post-
PROD 0.81 (0.08-1.75) 1.5 (0-2.87) .01
algometer (N) operative pain in cats undergoing celiotomy using a
randomized, blinded, controlled, clinical trial. The trial was
Note: Data are median (IQR).
appropriately powered with well-balanced treatment groups
Abbreviations: N, Newtons; PROD, Prodplus; Topcat Metrology.
and was performed in a setting that included a diverse set of
surgical skill levels (students, residents, board-certified sur-
3.4 | Subgroup analysis
geons, and shelter clinicians). Use of a quilting pattern in the
Analysis of treatment subgroups within categories of sur- subcutaneous tissues was found to reduce in half the inci-
geon experience is presented in Table 4. Point estimates of dence of seroma in cats undergoing midline celiotomy com-
seroma incidence in the Q group remained approximately pared with other closure techniques, with minimal
50% of those in the NC and SC groups, regardless of associated increase in surgical time.
whether the surgeon was a student or an experienced clini- The quilting pattern has been previously evaluated in
cian. Reduction in group size due to stratification led to loss human patients undergoing surgery for ventral hernia
of power to maintain significance (P = .13) for this outcome. repair,4 abdominoplasty,5,12 port site closure after single port
When procedures were restricted to those performed by an laparoscopy,6 latissimus dorsi breast reconstruction,7,9 mas-
experienced clinician, the median incisional closure time tectomy and axillary lymph node dissection,8,10,14 and man-
was 2 minutes shorter in the NC group at 4 minutes com- agement of traumatic skin avulsion injuries,11 with findings
pared with the Q (6 minutes) and SC (7 minute) groups similar to those of this study. These cited researchers found
(P = .02). When treatment groups were combined, cats that the quilting pattern reduced seroma incidence and sever-
undergoing ovariohysterectomy by a student surgeon had ity compared with standard appositional closure and reduced
higher pain scores (P < .001) and a lower mechanical the requirement for postoperative closed suction drainage. A
LOPEZ ET AL. 7
previous study in which the quilting pattern was compared The strengths of this study are inherent to the randomized
to standard apposition for closure of subcutaneous tissues blinded design, which provides a high level of evidence.
after celiotomy in dogs also provided evidence of a reduc- Groups were well balanced on all measured variables, which
tion in seromas and postoperative pain.13 While the current makes it less likely that a silent variable influenced our
study found that subcutaneous tissue closure by any method results. Group size was driven by power analysis. However,
reduced postoperative pain compared with no closure, the despite these strengths, several limitations should be noted.
best method of subcutaneous closure for optimizing that Differential loss to follow-up at 10-days was unexpectedly
benefit could not be confirmed. The mechanism of pain identified in the NC group and may have introduced infor-
reduction with suturing is unknown but may reflect mation bias if the loss was related to the presence or absence
decreased movement and stretch of the subcutaneous relative of incisional complications. Incisional complications were
to the surrounding tissues. Withholding subcutaneous tissue identified through a combination of physical examinations
and/or owner questionnaires, which could have resulted in
closure resulted in an increased incidence of seroma, and
variation in the sensitivity of detection of complications
pain and cannot be recommended. The results of this study
within groups. However, group bias is an unlikely con-
appear to provide evidence to counter the commonly held
founder in this study because all parties were blinded to
misconception that feline subcutaneous fat should not be
group assignments. A high proportion of the cats in this
apposed because of the risk of steatitis.
study were operated on by student surgeons, which may
The suture pattern illustrated in Figure 1 was selected to
limit extrapolation of findings to cats undergoing other
allow implementation in a clinical setting, balancing speed,
abdominal procedures with experienced surgeons. However,
and clinical familiarity, while achieving the goal of anchor-
incisional lengths of student surgeons may more accurately
ing the superficial to deep layers. However, dead space
represent an exploratory celiotomy for experienced sur-
could likely be obliterated with other suture configurations.
geons, and point estimates of treatment group seroma inci-
The mechanism of action for reduction of seroma formation
dence varied minimally between student surgeons vs
with a quilting pattern likely involves the reduction of dead
nonstudent surgeons. This finding provides evidence that the
space between the external rectus fascia and the subcutane-
effect of subcutaneous tissue closure technique may be
ous tissues by apposition and stabilization of the two layers-
maintained across incision size and experience; however,
a principal that dates back to Halsted.25 Other preventive
lack of power within subgroups limits the ability to defini-
strategies include closed suction drainage, use of fibrin glue,
tively confirm this effect. Finally, the low incidence of
and bandaging.5,7 While drains may result in harm through
SSI/dehiscence in this population resulted in the loss of
increased SSI risk,26 quilting is a low cost, simple interven-
power to detect differences between treatment groups to a
tion that does not increase the requirement for postoperative
post hoc power of 31%.
care in the way that drains and bandages may. The lower
In conclusion, a quilting suture pattern of the subcutane-
cosmetic apposition visual analog score assigned to incisions
ous tissue reduced seroma formation with minimal increase
with a quilting pattern was contrary to our clinical impres-
in surgical time compared with other techniques in cats
sion, and we were unable to identify a plausible explanation.
undergoing midline celiotomy. Failing to close the subcuta-
The statistical difference detected between groups may not
neous tissues cannot be recommended because this practice
be clinically significant, reaching only 6 of 100 points on the
resulted in the highest point estimates of seroma incidence at
scale of 0 to 100. Indeed, the minimal clinically important
10 days postoperatively and increased postoperative pain the
difference on a similar wound cosmesis scale has previously
day after surgery. Widespread application of a quilting pat-
been recommended at 15 points.27 In addition, the difference
tern to cats undergoing celiotomy may improve animal wel-
observed in our study did not appear to impact clinical
fare and reduce client emotional distress. Quilting patterns
healing because the incidence of SSI/dehiscence did not dif-
may also be indicated for other procedures, particularly
fer between the three groups.
those in which there is risk for seroma formation.
The higher pain scores after procedures performed by
student surgeons compared with experienced surgeons may
be intuitive but has not been previously identified in cats. In C O N F L I C T O F I N T ER ES T
a randomized trial of ovariohysterectomy in dogs random-
ized to experienced vs student surgeons, duration of surgery, The authors declare no conflicts of interest related to this
blood loss, and C-reactive protein levels were all greater in study.
the inexperienced group.28 The increased pain noted in cats
operated on by student surgeons may have been associated
with longer incisions, a variable unfortunately not measured OR CI D
in this study. Galina M. Hayes https://orcid.org/0000-0002-1365-3284
8 LOPEZ ET AL.
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