Nechay et al.

BMC Surgery (2020) 20:116

https://doi.org/10.1186/s12893-020-00735-6

RESEARCH ARTICLE Open Access

Thermal effects of monopolar

electrosurgery detected by real-time
infrared thermography: an experimental
appendectomy study
Taras V. Nechay1*, Svetlana M. Titkova1, Mikhail V. Anurov1, Elena V. Mikhalchik2, Kirill Y. Melnikov-Makarchyk1,
Ekaterina A. Ivanova1, Alexander E. Tyagunov1, Abe Fingerhut3,4 and Alexander V. Sazhin1

Abstract
Background: Monopolar energy (ME) is routinely used in appendectomy. This study aimed to investigate the
degree of lateral thermal spread generated by ME and to evaluate the thermal injury sustained by the close-lying
tissues.
Methods: Appendectomy with a monopolar Maryland dissector was performed in 8 rabbits (at 30 and 60 W power
settings). A high-resolution infrared camera was used to record tissue heating during the intervention. After autopsy
macroscopic changes were evaluated and tissue samples were subjected to myeloperoxidase (MPO) assay and
histological examination.
Results: No significant differences in the extent of thermal spread, MPO activity and histological signs of
inflammation were observed between groups. Regardless of the power settings, the heat spread exceeded 2 cm
laterally along the mesoappendix when application time exceeded 3 s. The spread of heat through tubular
structures in both groups caused a significant temperature rise in the nearby intestinal loop, resulting in perforation
(n = 3) and necrosis (n = 1).
Conclusions: Application time is critical in thermal spread during appendectomy aided by ME. Tubular anatomic
structures can enhance thermal injury on distant tissues. The observed effects of ME bear clinical relevance that
need further investigation.
Keywords: Appendectomy, Monopolar electrosurgery, Complications after appendectomy, Thermography, Lateral
thermal spread

* Correspondence: tnechay@mail.ru; rsmu@rsmu.ru

1
Pirogov Russian National Research Medical University, Ostrovitianov str. 1,
Moscow 117997, Russia
Full list of author information is available at the end of the article

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Nechay et al. BMC Surgery (2020) 20:116 Page 2 of 12

Background and paramedical teams” [13]. Most experimental and clin-

Electrosurgical techniques for tissue dissection and ical studies have evaluated the degree of lateral thermal
hemostasis have long become an essential component of spread at high or maximum electrosurgical unit (ESU)
surgical routine. Of 230 million surgical interventions power settings by a histological examination [14]. How-
performed globally every year, the majority rely heavily ever, there were certain limitations to the experimental
on electrical energy [1, 2]. Both patients and surgeons design of these studies: they were conducted in vitro using
benefit from electrosurgery since it significantly in- bovine and porcine muscle samples, whose overall resist-
creases the cutting speed and improves the quality of ance differed from the resistance of the intestinal wall and
hemostasis. Conversely, it also can cause complications. the mesoappendix in vivo. Besides, the lack of blood sup-
In spite of the continuous evolution of the technology, ply may have affected thermal spread in the samples.
the incidence of serious adverse events during or follow- Laparoscopic appendectomy is a common surgical pro-
ing electrosurgery (2–5 for 1000 patients), shows no ten- cedure that often involves the use of a monopolar electro-
dency to decline [1, 3]. Most often, such complications surgical energy [15]. According to the World Society of
arise from monopolar energy and account for 53% of all Emergency Surgery (WSES), monopolar electrocoagulation
undesirable effects associated with electrosurgery [1]. and bipolar energy are “the most cost-effective techniques
Apart from direct injury, the dangers of monopolar elec- for mesoappendix dissection, even if more experience and
trosurgery include residual heat injury, direct coupling, technical skills are required to avoid potential complica-
capacitive coupling, and antenna coupling [4], all of tions and thermal injuries” [16].
which can be potentially traumatic for a patient under As lateral thermal damage is more pronounced in pa-
certain conditions [5, 6]. These effects are well described tients with an inflamed appendix [17, 18], and drawing
with the goal of avoiding high-risk scenarios for surgical on the literature [12], we hypothesized that lateral ther-
energy-based device-related complications. Several re- mal spread would be greater with higher power settings
sources are available regarding this topic, including The and that the heating of nearby tissue, including the
Society of American Gastrointestinal and Endoscopic cecum and the mesoappendix, could lead to complica-
Surgeons (SAGES), Fundamental Use of Surgical Energy tions. The aim of this study was to investigate the lateral
(FUSE) program, and others. Despite this, numerous thermal spread during monopolar-aided appendectomy
surveys of surgeons show significant knowledge gaps in at different ESU power settings using real-time infrared
the safe use of widely used energy-based devices [7]. thermography and to evaluate the severity of thermal in-
Thus, Malik has found a “high level of ignorance regard- jury to the affected tissue.
ing the procedure and indications of basic electrosurgical
equipment” [8]. Feldman shows lack of knowledge in basic Methods
electrosurgical principles among members of SAGES board Animals
having discovered only 59% percent of correct answers on The experiment was conducted in 8 male Soviet chin-
the safe use of electrosurgery test among them [9]. Despite chilla rabbits weighing from 3770 to 4240 g (mean
advances in electrosurgical devices, a monopolar electrosur- weight was 3981 ± 174 g) obtained from University vivar-
gical unit invented back in 1926 by William T. Bovie re- ium. The animals were kept in separate cages under
mains one of the most available and widely utilized surgical standard conditions at 20–22 °C, 40–50% humidity and
instruments [10]. 12:12 h light/dark regime with free access to food and
Inadvertent damage and delayed injury to nearby tis- water. Before surgery, the animals were allowed to accli-
sue resulting from the lateral spread of thermal energy mate for 7 days. All animal studies were performed fol-
can be sustained during any type of electrosurgery. The lowing the ARRIVE guidelines and conducted in strict
degree of thermal spread depends on the type of instru- accordance with the Guide for Care and Use of Labora-
ment used, its power settings and application time [11]. tory Animals, Pirogov Russian National Research Med-
Monopolar energies cause a rise in temperature to a po- ical University, Moscow.
tentially critical level at a 1-cm distance from the top of an
electrosurgical instrument even when the applied power is Power sources
low [12]. Moreover, monopolar diathermy generates In this work, we used the Alsa EXCELL NHP 250/D
greater lateral thermal spread than more advanced elec- ESU with a constant voltage and power output, equipped
trosurgical instruments used for dissection and hemostasis with start pulse and high frequency leakage controls.
during laparoscopic appendectomy [11]. Borie described Cutting and coagulation were performed in the Pure
876 complications of surgical energy-driven devices for 7 (non-modulated sinusoidal current for the cut without
years, most of them (70%) caused by monopolar energy. any coagulating effect) and Soft (modulated low-voltage
The main reason, highlighted by author was “persistent current with a strong deep effect and no superficial
misunderstanding of appropriate usage within the medical carbonization) modes, respectively.
Nechay et al. BMC Surgery (2020) 20:116 Page 3 of 12

The experiment mg/kg, intravenous). During the necropsy, we looked for

The rabbits were fasted for 12 h prior to surgery but had the visible signs of intraperitoneal inflammation and tis-
free access to water. The surgical procedures were per- sue adhesions in the peritoneal cavity. The serosal sur-
formed under general anesthesia with an intravenous injec- face of the cecum wall was examined for any signs of
tion of ketamine (Ketamin 10%, Sanofi-Ceva, Dusseldorf, perforation, edema or discoloration. To assess the sever-
Germany) and xylazine (Rompun 2%, Bayer, Leverkusen, ity of tissue adhesions, a modified Vetere grading scale
Germany) under sterile conditions. The animals were [19] was used: 0 points – no adhesions, 1 point – thin,
placed on a surgical table in a supine position. The skin easily separable adhesions, 2 points – thick, difficult to
was shaved, cleaned and sterilized, and an 8-cm long separate adhesions.
midline laparotomy was performed. The appendix was de-
livered into the wound. Appendectomy was carried out fol- Histological analysis
lowing the standard technique: the mesoappendix was All samples were collected after euthanasia of the ani-
separated from the appendix from tip to base using a 5 mm mals. The schematic representation of sample collection
monopolar Maryland dissector with operating part 16 for the histological analysis is presented in Fig. 1.
mm × 2 mm for each branch (KELLY dissecting and grasp- Two areas of the cecum sized 1х1 cm (А1, adjacent to
ing forceps, Maryland, Karl Storz, Germany) connected to the stump, and А2, laterally and adjacent to A1) were ex-
the ESU. The size of the mesenteric tissue grasped by the cised during the necropsy and fixed in formalin for 24 h.
dissector did not exceed 4 mm. The animals were distrib- Sample A0 excised from a region of the large intestine
uted into two groups depending on the applied power lying at a distance exceeding the potential spread of heat
mode: cutting and coagulation at 30 W (LP group) AND (10 cm) from the surgical site was used as a reference. The
cutting and coagulation at 60 W (SP group). The tissue was collected samples were paraffinized and later cut into 5-
desiccated as opposed to fulguration, i.e. the electrode was μm slices. The obtained tissue sections were stained with
in direct contact with the tissue. The duration of a single hematoxylin-eosin and Van Gieson stain to assess thermal
application was not strictly limited and depended on the damage to collagen fibers. Standard light microscopy was
time required to achieve the desired effect. We only performed using a Motic BA-400 Trinocular microscope
counted the number of applications and their total time. (Motic China Group Co., Ltd., China). The images were
The unburied stump was ligated with Polyglycolide 3/0 su- processed in Motic Images Advanced 3.2 software. The
tures. After appendectomy, the abdominal wound was severity and extent of cell infiltration and tissue edema
closed by sutures. The animals were monitored after sur-
gery and brought back to the vivarium as soon as they
awoke from anesthesia. The animals were allowed to drink
water on the day of surgery; solid food was introduced on
the following day.

Intraoperative thermography
Real-time thermography was performed using the science
grade FLIR A655sc camera with 30 Hz frequency, thermal
sensitivity of < 50 mK and a resolution of 640 × 480 pixels.
The camera was mounted 1 m above the surgical site.
The obtained thermal images of the cecum, where tissue
was later collected for further histological examination
and the enzyme assay, were processed in FLIR ResearchIR
MAX Version 4.40.6.24. We also investigated how heat
spread from the mesoappendix to the adjacent organs and
noted the time required for tissue cooling. The critical
threshold temperature for cell damage was assumed to be
42 °C. All surgical interventions were recorded on a high-
definition video camera (Canon 7D) mounted on a tripod
at the same angle and distance as the infrared camera; the
recording was synchronized with thermography.

Euthanasia of research animals Fig. 1 A schematic representation of material sampling for

histological analysis (A0-A2) and measurement of MPO activity in
On day 5, the animals were anesthetized and then sacri-
tissue samples (M0-M2)
ficed with an overdose of barbiturates (Narcoren®, 100
Nechay et al. BMC Surgery (2020) 20:116 Page 4 of 12

were calculated from the micrographs. All samples were hemostasis or good quality of cut (р = 0.112). Maximal
studied by a histologist blinded to the experiment. duration of a single application reached 9.7 (1.5) s in LP
group and 5.03 (1.55) s in SP group (p = 0.03). The num-
Tissue myeloperoxidase assay ber of applications was the same in both experimental
Samples M1 and M2 were collected from the regions ad- groups. Extensive lateral thermal spread during electro-
jacent to A1 and A2 and tested for myeloperoxidase coagulation was observed in all animals. Regardless of
(MPO) levels. A tissue region distant to the cecum was the power settings, the heat spread more than 2 cm lat-
used as a reference (Fig. 1). MPO activity was measured erally along the mesoappendix when application time
in the samples of the intestinal wall. Briefly, the frozen exceeded 3 s. No significant differences in the extent of
samples of the intestinal tissue were homogenized in thermal spread were observed for low and standard
0.01 M PBS (pH 7.4) containing 0.2% Triton X-100 using power settings. The highest temperature of the cecum
a Potter-Elvehjem tissue grinder. The homogenates were recorded during the surgery was 61.3 °C (Fig. 2).
centrifuged at 900 g for 30 min. Then, equal volumes of The cecum temperature increased when the mesoap-
1% hexadecyl trimethyl ammonium chloride solution in pendix coagulation site was 1 cm away from the cecum,
PBS were added to each supernatant, and MPO activity correlating with coagulation time and showing no de-
was determined. The supernatant (50 μL) was mixed pendency on power settings.
with 150 μL of 0.1 M sodium citrate buffer (pH 5.5) con- It took 12 to 42 s for the cecum to cool down to the
taining 0.1 mg/mL− 1 of O-dianisidine chloride and point below 42 °C, the critical cell damage temperature
0.001% H2O2 used as a substrate for MPO activity. After cutoff used in this study. The analysis of thermal images
incubating the mixture for 5 min, the reaction was revealed that intense heating of the mesoappendiceal fat
stopped with 1 ml of 35% orthophosphoric acid. Absorb- during the dissection of the mesoappendix caused a
ance was measured at 460 nm. MPO activity was calcu- temperature rise in the cecal wall as late as 3–5 s following
lated based on the extinction coefficient of 20,040 the application of monopolar energy. It took 30 s for the
M−1cm− 17. The Lowry assay was used to quantitate the mesoappendix heated over 100 °C during dissection to
total protein content in the supernatants. MPO activity cool down to 42 °C. The cooling pattern was not linear:
was expressed as nM/mg of protein. the higher the temperature of the heated tissue in com-
All animals were weighed before operation and on parison with the temperatures of the animal’s body and
post-operative day 5. No antimicrobial prophylaxis was the environment, the faster the cooling rate, approxi-
subscribed. No additional parameters of animals recov- mately 10 degrees per second. When the tissue cooled
ery were assessed. down to 60–70 °C, the cooling rate dropped to 10 degrees
per 10 s. Thermography data are presented in Table 1.
Statistical analysis
The obtained data was processed in Statistica 13.3 for
Windows (StatSoft Inc., Tulsa, OK, USA). The results
were presented as mean values and standard deviations
(SD). The Student’s t- test was applied to compare continu-
ous variables. The Mann-Whitney U-test was used to com-
pare nonparametric quantitative data. The normality of
data distribution was analyzed using Kolmogorov–Smirnov
and Shapiro–Wilk tests. Differences were considered sig-
nificant at p < 0.05. A power analysis was not applicable be-
cause of the exploratory nature of the study and because it
was part of a subproject of a larger study.

Results
The appendix size (length and width) was similar in both
groups: 9.44 (1.02) cm and 0.95 (0.13) cm in LP and
10.06 (0.86) cm and 1.02 (0.24) cm in SP, respectively.
Ambient temperature was 20 °C. The total number of
analyzed applications in our experiment was 704; total Fig. 2 A thermogram of the cecum (to the left of the black line)
application time was 203 (39) s in LP and 118 (18) s in during mesoappendix (to the right of the black line) dissection. The
SP (р = 0.008). At low power, the average duration of a temperature is given in degrees Celsius. Inside the red zone, the
temperature is over 45 °C; outside the red zone, it is below 42 °C; at
single application was 2.05 (0.53) s, whereas at standard
the border, the temperature is 42–45 °C
power settings, it took 1.34 (0.22) s to attain satisfactory
Nechay et al. BMC Surgery (2020) 20:116 Page 5 of 12

Table 1 Thermography data

Group Low Power Standard Power
R1 R3 R6 R8 Mean R2 R4 R5 R7 Mean p
(SD) (SD)
Mean application time, s 2.5 1.46 2.5 1.75 2.05 1.2 1.09 1.52 1.53 1.34 0.112
(0.53) (0.22)
Min application time, s 0.3 0.1 0.4 0.5 0.33 0.1 0.4 0.4 0.2 0.28 0.773
(0.17) (0.15)
Max application time, s 11.5 7.9 9.8 9.6 9.7 4.1 3.4 6.8 5.8 5.03 0.03
(1.5) (1.55)
Application duration > 3 s, % n/d* 6, 25% 6,8% 12.7 3% 1,2% 11,8% 10,3% 6.6 0.595
3% (10.7) (5.3)
Cecum T max, °C 58.9 55.3 59.1 48.4 55.4 61.3 57.2 48.8 56.1 55.9 0.885
(4.9) (5.2)
Mesoappendix T max °C 152.4 146 160.4 157.2 154 160.6 156.4 160.8 160.5 159.6 0.112
(6.3) (2.1)
T ≥ 42° duration on cecuma, s 42 n/ 13.4 15.5 23.6 24 14 12 13 15.8 0.377
db (15.9) (5.6)
Lateral thermal spreada, mm 8 n/ 4.6 4.48 5.7 5.6 5.6 6 9.3 6.6 0.372
db (1.9) (1.8)
Lateral thermal spread on 28 24 27.6 20.4 25 33 18.4 20.4 32.4 26.1 0.886
mesoappendixa, mm (3.6) (7.7)
Lateral thermal spread on 1.8 1.6 2.5 3.3 2.3 1.4 1.6 3 6 3 (2.1) 0.886
intestinal loop, mm (0.8)
Complication no no Intestinal wall full Intestinal 2/4 no no Intestinal Intestinal 2/4
thickness necrosis perforation perforation perforation
a
≥42 °C
b
no data

Weight measurements on postoperative day 5 revealed in 2 animals from the LP group, involving the loops of
that the animals had lost 268 (53) g on average, but the the large or small intestines (adhesion severity scored 1
differences between the groups were not statistically sig- point on the Vetere scale).
nificant. During the necropsy, we observed no visible One rabbit from the LP group developed full-thickness
macroscopic changes in the cecal serosa and noticed no necrosis of the intestinal wall (1х1 cm) without any signs
signs of hyperemia, necrosis or perforation of the cecum. of perforation (Fig. 3a, marked by a black arrow). Two
The peritoneal cavity showed no signs of pathological rabbits from the SP group and one rabbit from the LP
fluid buildup. Adhesions had started to form at the site group had perforation of the small intestine wall (Fig. 3b,
of the surgical scar in one animal from the SP group and marked by a white arrow). Close to the perforation site,

Fig. 3 Damage to the intestinal loop caused by thermal energy. a zones of transmural coagulation necrosis without perforation (black arrows).
b perforation of the small intestine wall (a white arrow) and a few areas of thermal damage to the serosa
Nechay et al. BMC Surgery (2020) 20:116 Page 6 of 12

there were a few areas of coagulative necrosis in the Tissue myeloperoxidase

intestinal wall with no signs of perforation (Fig. 3b, The enzyme assay did not detect any significant differ-
marked by black arrows). There was also a soft, loose ences between tissue myeloperoxidase levels in the studied
adhesion between the perforated region and the loop samples and the reference values (Fig. 5). The differences
of the small intestine. Dissection of the adhesion pro- between the groups were not statistically significant.
voked leakage of the intestinal contents into the peri-
toneal cavity. Effects of monopolar coagulation during appendectomy
The thermal images obtained during the surgery were
retrospectively analyzed in-depth and compared to nec-
Histological examination ropsy reports. The following thermal effects were noticed:
Minimal to moderate infiltration with plasma cells, lym-
phocytes, and eosinophils was observed in all layers of a) The heat spread through tubular structures (Fig. 6a,
the cecal wall 1 and 2 cm away from the stump in both marked by a black arrow; Fig. 6b). Passing through
groups on day 5 after appendectomy. The mucosa, sub- the mesenteric vessels, it caused a temperature rise in
mucosa and subserosa were edematous to various de- the small intestine (Fig. 6c), resulting in the
grees (Table 2). perforation of the intestinal wall in three rabbits in
The muscular layer fibers exhibited no signs of both groups (Fig. 3b) and transmural necrosis
swelling or degeneration. No damage to collagen fibers without wall perforation in one more rabbit (Fig. 3a);
or neutrophil infiltration was noticed in the samples b) The mesenteric tissue was cooled by the large
(Fig. 4). One rabbit from the LP group had an exten- vessels passing through its thickness and supplying
sive hemorrhagic lesion in the muscular layer, another blood to the small intestinal loop adjacent to the
one had a small area of subepithelial necrosis 1 cm appendix. (Fig. 6a, marked by a white arrow). The
from the stump. In one rabbit from the SP group, a blood vessels heated up almost instantly and gave
large mucosal erosion was observed 2 cm from the off a considerable amount of heat to the
stump. surrounding tissue; they also cooled down quickly,

Table 2 Pathologic findings at the different sites of the cecum layers on day 5 after appendectomy using monopolar
electrocoagulation
Power 30 W 60 W
Distance from stump 1 cm 2 cm 1 cm 2 cm
Cell infiltration
Severity
Absent 2/4 (50%) 0/4 2/4 (50%) 2/4 (50%)
Moderate 1/4 (25%) 2/4 (50%) 2/4 (50%) 1/4 (25%)
Marked 1/4 (25%) 2/4 (50%) 1/4 (25%)
Minimal: < 10% 0/4 0/4 0/4 1/4 (25%)
Mild: 10–25%; 1/4 (25%) 0/4 1/4 (25%) 1/4 (25%)
Moderate: 26–50% 2/4 (50%) 3/4 (75%) 3/4 (75%) 2/4 (50%)
Marked: > 51% 1/4 (25%) 1/4 (25%) 0/4 0/4
Extent
Mucosal 2/4 (50%) 2/4 (50%) 2/4 (50%) 3/4 (75%)
Mucosal and submucosal 1/4 (25%) 1/4 (25%) 1/4 (25%) 0/4
Mucosal, submucosal and subserosal 1/4 (25%) 1/4 (25%) 1/4 (25%) 1/4 (25%)
Edema
Severity
Absent 2/4 (50%) 0/4 2/4 (50%) 2/4 (50%)
Moderate 1/4 (25%) 2/4 (50%) 2/4 (50%) 1/4 (25%)
Marked 1/4 (25%) 2/4 (50%) 1/4 (25%)
Extent 1/4 (25%) 4/4 (100%) 1/4 (25%) 2/4 (50%)
Submucosal 1/4 (25%) 1/4 (25%)
Mucosal and submucosal
Mucosal, submucosal and subserosal
Nechay et al. BMC Surgery (2020) 20:116 Page 7 of 12

Fig. 4 Representative images of H&E-stained cecum sections illustrate histopathological changes on day 5 following appendectomy aided by
monopolar surgical energy. a (LP group) and c (SP group) - 1 cm from the stump; b (LP group) and d (SP group) - 2 cm from the stump (× 100,
scale bar 500 μm)

Fig. 5 MPO activity in tissue samples. R – animals, high – ME 60 W, low – 30 W

Nechay et al. BMC Surgery (2020) 20:116 Page 8 of 12

Fig. 6 Effects of ME in appendectomy. a Current channeling (a black arrow), the “clamp effect” (a purple arrow), mesenteric vessel cooling by
blood flow (a white arrow). b Current channeling (white arrows). c Lateral thermal spread causes heating of the surrounding tissue (a small
intestine loop – a black arrow). d The “pedicle effect” causes heating of tissues where a smaller tubular structure (a vessel – a white arrow) enters
a larger tubular structure (an intestinal loop – a black arrow). e The “jump over” effect (a white arrow). f Current leakage through the nonactive
instrument (a white arrow)
Nechay et al. BMC Surgery (2020) 20:116 Page 9 of 12

but the mesoappendix tissue stayed heated for a single exposure both in LP and SP groups. In all animals
longer time; with perforation a single exposure of monopolar energy
c) The “clamp effect”: the tissue held with the forceps lasted over 1.5 s thereby causing rising of the temperature
or clamp jaws was heating up as the electrical of the small intestine to a critical threshold through the
current generated by ME was flowing through the entire thickness of the intestinal wall (2 mm).
forceps due to the high current density in the It is difficult to predict and measure thermal spread
grasped tissue (Fig. 6a, marked by a purple arrow). resulting from ME application [10]. Several authors [18]
d) The “pedicle effect”: the heating of tissue (orange have hypothesized or reported that lower power settings
circle) along the tubular structures (the mesenteric would lead to less thermal spread. In fact, surgeons who
vessels) in the area where such structure (artery use ME devices use different power settings, modes and
marked by a white arrow) entered a larger tubular activation times depending on the task [23]. To our
structure (an intestinal loop; marked by a black knowledge, no standardized curriculum for surgeons has
arrow) (Fig. 6d). so far addressed the safe use of ME for the dissection of
e) The “jump over” effect (Fig. 6e, marked by a white the mesoappendix during laparoscopic appendectomy.
arrow). The majority of manuals recommend applying “the low-
f) Leakage of the electrical current through the est possible power setting” [24], others suggest setting
nonactive instrument when it accidentally touched the power to 70 to 90 W in the “pure cutting” mode or
the loop of the small intestine (Fig. 6f, a white to 50 W in the “coagulation” mode [25]. Jones et al.,
arrow). showed in a randomized clinical trial that thermal injury
occurred more frequently in the coagulation mode com-
Analysis of thermograms showed that one to three of pared to the blend mode at the level of the trocar inci-
the above-mentioned effects were detected in each of sion sites [26]. The WSES, EAES and SAGES guidelines
animal with perforation or necrosis. With that, the lat- for diagnosis and treatment of acute appendicitis provide
eral thermal spread on intestinal loop in these animals no recommendations regarding ESU power and voltage
was significantly greater than in animals without compli- for appendectomy [16, 21, 22]. In our study, “coagula-
cations (3.7 (1.6) mm vs.1.6 (0.16) mm, p = 0.029). In an- tion” and “cutting” modes were fixed at 30 and 60 W be-
imals with complications average percent of applications cause general surgeons tend to use such combinations
≥3 s was 13.5 (7.9) vs. 3.5 (2.6) in animals without com- [27] for the mesentery dissection. Besides, we aimed to
plications (p = 0.052). compare results of our in vivo study with main ex vivo
experimental and in vivo clinical studies of lateral ther-
Discussion mal spread [11, 12, 28, 29].
Regarding WSES Jerusalem guidelines for treatment of Previous studies have demonstrated that the area of liv-
acute appendicitis no difference in several methods of ing tissue affected by a thermal burn gradually grows in
mesoappendix dissection was reported. But stating the size after the initial impact, reaching its maximum by days
danger of leaving foreign bodies in the abdominal cavity, 3 to 7, and does not start to shrink until day 14 [18]. Dam-
utilization of energy devices was preferable over clipping age to nearby structures typically occurs on day 4–5 fol-
of appendicular artery. Moreover guidelines suggest en- lowing the surgery due to unrecognized energy transfer
ergy devices in case of inflamed and oedematous mesoap- [25, 30]. Although the cecum had been heated up to 42 °C
pendix consider ME as “the most costeffective method” (“critical temperature”), no clinical manifestations were
among them [16]. According to the study of J R. Robinson noticed on postoperative day 5. At the same time, histo-
et al. [20] surgeons were informed about cost-reducing logical examination revealed signs of moderate inflamma-
opportunities in a real-time while making a decision of tion and reactive edema affecting all tissue layers both at a
taking a preferrable device for mesoappendix dissection. distance of 1 cm and 2 cm from the stump, attesting to
This led monopolar hook to became the most often device thermal exposure. However, at the time of necropsy, the
for mesoappendix dissection (61.3%). Neither SAGES nor inflammation was aseptic in nature: there was no neutro-
EAES guidelines on diagnosis and management of acute phil infiltration and MPO levels in the cecal tissue were
appendicitis provide information about preferable energy low. This could be explained by the design of our experi-
device for appendectomy [21, 22]. ment: appendectomy was performed on the non-inflamed
This study has shown that the duration of ME was the appendix. A study of lateral thermal damage to the
key factor affecting the extent of thermal spread during mesoappendix and the appendiceal base during laparo-
appendectomy, not the power. Regardless of the power scopic appendectomy in children demonstrated that the
settings (30 or 60 W), heat spread more than 2 cm lat- postoperative pain syndrome and the duration of hospital
erally along the mesoappendix when application time stay directly depend on the temperature of the heated tis-
exceeded 3 s. Perforation correlated with long-lasting sue and the size of the thermal lesion [17].
Nechay et al. BMC Surgery (2020) 20:116 Page 10 of 12

Due to gaps in scientific data concerning critical level to different temperatures as the current passes through it.
of temperature for creation of intestine damage we set In our experiment, the temperature of the appendix rose
the cut-off value for “critical temperature” for possible only after the heat reached the mesoappendix, and that
cell damage at 42 °C, as it was done by other investiga- rise was not very pronounced. We also observed the so-
tors [6, 31]. Commonly it was based on a known fact called “jump-over” effect indicating that thermal processes
that heated over 42 °C cell suffers from protein denatur- in deeper tissues can only be evaluated indirectly and
ation [32]. However, in fact, there is no consensus as to sometimes can go unnoticed. Infrared camera captures a
what temperature should be considered critical in terms temperature rise in the serosa occurring after the appen-
of cell damage. Experimental studies have found that dix gets heated up through its entire thickness from inside.
cells heated in excess of 20 °C die within 15 s; heated in Probably the mesoappendix-appendix borderline played a
excess of 25 °C, in 4 s, and heated in access of 30 °C, in role in preventing the appendix from heating. This obser-
2 s [33]. We found no differences in the histopatho- vation calls into question the role of the appendix diam-
logical changes to the cecal tissue between the studied eter in thermal spread.
groups. Total ME application times and surgery duration In theory, thermal injury involves two major zones
were longer in the LP group than in the SP group. This during appendectomy with ME: the mesoappendix and
could be explained by the fact that in order to achieve the cecum. Interestingly, however, three animals from
the same effect at low power settings, the duration of a both groups developed perforation of the small intestine,
single application needs to be increased. Longer applica- and another rabbit developed transmural necrosis of the
tion times lead to extensive lateral thermal spread; as a small intestine. Based on the effects registered in our ex-
result, the tissues are exposed to the temperatures that perimental study using thermal imaging, several possible
cause cell damage for longer periods of time. This means underlying mechanisms might be assumed. First, current
that the severity of thermal injury does not change sig- channeling through the mesenteric vessels might provoke
nificantly when low power settings are applied, as com- substantial lateral thermal spread. Diamantis [18] com-
pared to standard settings. The maximum temperature pared the effects of different electrosurgical modalities
was the same at any power settings. In addition, three (mono- and bipolar coagulation, impedance-controlled bi-
rabbits from both groups demonstrated a histological polar vessel sealing and US shears) on the short gastric
picture of thermal lesions in different layers of the cecal vessels (1 mm in diameter) on rabbits. Four of 20 animals
wall following the longest exposure of the cecum to treated with ME developed perforation of the greater
T ≥ 42 °C. Previously, Hefermehl [12] conducted an ex- curvature of the stomach at the coagulation site on post-
periment in order to investigate a relationship between operative day 3. Bipolar coagulation resulted in stomach
thermal spread and power settings/application time. He perforation in two rabbits (10%). Khan et al. [34] studied
discovered that at 60 W the area of thermal spread in- the effect of thermal spread on the prostatic nerve plexus
creased by one-third (in comparison with 30 W). Longer during robotic prostatectomy in vivo. He demonstrated
application times (2 s) led to a multifold increase in the that interposition of the vessels significantly reduced ther-
lesion area from 3.5 to more than 20 mm. The majority mal spread to distal tissues. In our case, the structures in
of recommendations on the use of coagulation devices the proximity to the coagulation site were affected because
were developed based on ex vivo experiments on bovine the appendix and the small intestinal loop share common
and porcine musculofascial strips that had no blood flow blood vessels [35] and because heat travels through tubu-
in them [11, 12]. Results of our in vivo study carried out lar structures rapidly. This effect was observed in all ani-
on organs with physiologically normal blood flow are for mals developed perforation or necrosis of small intestine.
the most part in accordance with these data but demon- Another possible cause of intestinal perforation is the
strate that the key factor leading to injury was duration pedicle effect described by Humes et al. [30]. This occurs
of application. The overall percent of such “long-lasting” when the electrical current goes through a tubular struc-
applications (≥3 s) in ¾ of animals with complications ture to the point where the latter enters another tubular
exceed 10%. This fact should be taken into account structure of a larger diameter. Humes et al. demon-
when elaborating surgical guidelines. strated the pedicle effect in a clinical series of three
The dynamics of thermal spread may be influenced by patients with similar common bile duct perforations
the difference in blood supply to healthy and inflamed tis- discovered during laparoscopic cholecystectomy and oc-
sues or their hydrophilicity. However, Pogorelić reported curred at the junction of the cystic and common bile
no significant differences in lateral thermal spread during duct. A similar effect was observed in our study when
appendectomy in patients with acute appendicitis and in the energy spread along the mesenteric vessels that en-
the absence of inflammation [17]. In patients with appen- tered the small intestinal loop. Our hypothesis would be
dicitis, the diameter of the inflamed appendix changes that more heat was emitted at the vasculo-intestinal
along its course, which means that its regions can heat up junction than along the vessels.
Nechay et al. BMC Surgery (2020) 20:116 Page 11 of 12

Another phenomenon observed in our study was the groups of rabbits which had the “standard” electro-
clamp effect (the heating of tissues grasped by forceps or a cautery surgical management; there was no true control
clamp through which the electrical current flows). It can be group which had no electrocautery. Therefore we did
explained in terms of the physical fundamentals of electri- not study the effect of tissue handling and dissection on
city. When current passes through a conductor, it heats it the inflammatory process. Either a sham group without
up according to the Joule-Lenz law. As the conductor appendectomy could have been use or appendectomy
diameter decreases, resistance and local heat production in- performed without electrocautery.
crease. The clamp effect can be critical for tubular struc-
tures, such as the ureters or the intestinal wall, leading to Conclusion
their heating at a distance from the site of coagulation. To our knowledge, this study is the first real-time inves-
One to three of the above-mentioned effects were ob- tigation of thermal spread produced by a monopolar
served in each animal with perforation or necrosis of the coagulator during appendectomy. The obtained results
small intestine. All effects were detected during retrospect- suggest that the key factor leading to injury due to lat-
ive analysis of thermograms, so we did not perform histo- eral thermal spread is duration of ME application, and
logical examination of the small intestinal loop in the complications might occur not only when the maximum
proximity to the coagulation site in all animals. It is possible power is applied (which is what the majority of such
that other animals with registered effects had pathological studies focus on) but also under certain conditions when
changes of the intestinal wall, but not so pronounced. a surgeon uses standard ME settings.
Further detailed investigation is necessary to identify The spread of heat generated by ME through tubular
the conditions under which preformation can occur, to anatomic structures can cause thermal injury of the in-
assess its severity and the risk of perforation when per- testinal wall in the regions distant to the surgical site, its
forming coagulation in proximity to tubular structures. necrosis and even perforation. Despite certain limitations
Because of inherent difficulties in retrospectively study- of this study, the observed effects of monopolar coagulation
ing mechanisms of laparoscopic injuries, it is important to can bear clinical relevance and require further investigation.
categorize potential mechanisms of unintended energy
Abbreviations
transfer in order to prevent bowel injuries [7]. ME: Monopolar energy; MPO: Myeloperoxidase; ESU: Electrosurgical unit; LP
Summing up, all of the listed effects may play a signifi- group: Low power; SP group: Standard power; SD: Standard deviations;
cant role in postoperative complications. WSES: World Society of Emergency Surgery; (US) shears: Ultrasound

Acknowledgements
The authors thank Pergam-Engineering JSC and personally Ivan Skobov for
Limitations of this study the equipment provided.
We recognize that all laparoscopic appendectomies are Authors’ contributions
not performed with ME, but this practice might be more TN, ST, MA and AS conceived and planned the experiments. TN, ST, MA, EI
prevalent than admitted. The major limitation of our and KM carried out the experiments. ST, MA, EI and TN performed the
measurements. AS was involved in planning and supervised the work. ST
study was that we used healthy animals with non- processed the experimental data, performed the analysis. TN, AT and ST
inflamed appendix, and therefore the potential enhance- drafted the manuscript and designed the Figs. EM performed the MPO assay
ment of inflammation was not studied. No antimicrobial and calculations. KM and EI manufactured the samples and characterized
them histological examination. AS, AT and TN supervised the project. AF
prophylaxis was administered to the animals in our aided in interpreting the results and worked on the manuscript. All authors
study, so we do not know the effects of antibiotic on provided critical feedback and helped shape the research, analysis and
thermal spread. As heavy postoperative complications manuscript. All authors discussed the results and commented on the
manuscript. All authors read and approved the final manuscript.
were not expected we didn’t plan to investigate the influ-
ence of antibiotics on their developing because it didn’t Funding
correlate with the purpose of the study. Another limita- This research did not receive any grant from funding agencies in the public,
commercial, or not-for-profit sectors. Research was performed as part of the
tion of this study is the small sample size. Moreover we employment of the authors in Pirogov Russian National Research Medical
did not compare the effects of other hemostatic devices University and Research and Clinical Center for Physical-Chemical Medicine.
(bipolar, LigaSure, EnSeal, ultrasound etc). We recognize
Availability of data and materials
that while monopolar equipment is less expensive than The experimental surgery videos, thermography visualization, histology and
the other modalities, there are ample data that show that MPO data used to support the findings of this study are available from the
ME might be more dangerous. corresponding author upon request.
In addition, because of anatomical differences between Ethics approval and consent to participate
species, the results obtained in this study might not be The present study was approved by the Institutional Animal Care and Use
directly extrapolated to humans. Moreover, the duration Committee at Pirogov Russian National Research Medical University
(Moscow, Russian Federation, approval number 24/2017). All animal
of application of ME in these animals may not be the experiments were performed in compliance with the NIH Guide for the Care
same that is required in humans. Last, we examined two and Use of Laboratory Animals.
Nechay et al. BMC Surgery (2020) 20:116 Page 12 of 12

Consent for publication 16. Di Saverio S, Birindelli A, Kelly MD, Catena F, Weber DG, Sartelli M, et al.
Not Applicable. WSES Jerusalem guidelines for diagnosis and treatment of acute
appendicitis. World J Emerg Surg. 2016;11:1–25. https://doi.org/10.1186/
Competing interests s13017-016-0090-5.
Authors Taras Nechay, Svetlana Titkova, Mikhail Anurov, Elena Mikhalchik, 17. Pogorelić Z, Katić J, Mrklić I, Jerončić A, Šušnjar T, Jukić M, et al. Lateral thermal
Ekaterina Ivanova, Kirill Melnikov-Makarchyk, Alexander Tyagunov, Abe damage of mesoappendix and appendiceal base during laparoscopic
Fingerhut and Alexander Sazhin have no conflicts of interest or financial ties appendectomy in children: comparison of the harmonic scalpel (Ultracision),
to disclose. bipolar coagulation (LigaSure), and thermal fusion technology (MiSeal). J Surg
Res. 2017;212:101–7. https://doi.org/10.1016/j.jss.2017.01.014.
Author details 18. Diamantis T, Kontos M, Arvelakis A, Syroukis S, Koronarchis D, Papalois A,
1
Pirogov Russian National Research Medical University, Ostrovitianov str. 1, et al. Comparison of monopolar electrocoagulation, bipolar
Moscow 117997, Russia. 2Research and Clinical Center for Physical-Chemical electrocoagulation, ultracision, and ligasure. Surg Today. 2006;36:908–13.
Medicine, Malaya Pirogovskaya 1a, Moscow 119435, Russia. 3Section for 19. Vetere PF, Lazarou G, Apostol R, Khullar P, Okonkwo L, Nezhat F.
Surgical Research, Department of Surgery, Medical University of Graz, 8036 Postoperative adhesion formation in a rabbit model: Monopolar
Graz, Austria. 4Department of Gastrointestinal Surgery, Ruijin Hospital, Electrosurgery versus ultrasonic scalpel. JSLS J Soc Laparoendosc Surg. 2015;
Shanghai Jiao Tong University School of Medicine, Shanghai 20025, China. 19:e2015.00018. https://doi.org/10.4293/JSLS.2015.00018.
20. Robinson JR, Carter NH, Gibson C, Brinkman AS, Van Arendonk K, Speck KE,
Received: 3 January 2020 Accepted: 5 April 2020 et al. Improving the value of care for appendectomy through an individual
surgeon-specific approach. J Pediatr Surg. 2018;53:1181–6.
21. Korndorffer JR, Fellinger E, Reed W. SAGES guideline for laparoscopic
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