http://informahealthcare.com/jmfISSN: 1476-7058 (print), 1476-4954 (electronic)

J Matern Fetal Neonatal Med, Early Online: 1–6! 2014 Informa UK Ltd. DOI: 10.3109/14767058.2013.879114

ORIGINAL ARTICLE

Preliminary evaluation of novel skin closure of Pfannenstiel incisionsusing cold helium plasma and chitosan films

Yael Hants1, Doron Kabiri1, Lior Drukker1, Abrahamyan Razmik2, Grigoryan Vruyr2, Harutyunyan Arusyak2,Gyulkhasyan Vahe2, Gian Carlo Di Renzo3, and Yossef Ezra1*

1Department of Obstetrics and Gynecology, Hadassah-Hebrew University Medical Center, Ein-Kerem, Jerusalem, Israel, 2Department of Obstetrics

and Gynecology, Republic Institute of Reproductive Health, Perinatology, Obstetrics and Gynecology, Yerevan, Armenia, and 3Department of

Gynecology, Obstetrics and Pediatrics, University of Perugia, Perugia, Italy

Abstract

Objective: To assess the safety and performance of a new energy-based skin closure system(BioWeld1TM) for the surgical Pfannenstiel incision in patients scheduled for elective cesareansection.Methods: This prospective, single center, non-randomized study included 20 patients who werescheduled for elective cesarean section. The BioWeld1 system was performed after suturing theinternal layers of the cesarean section incision. A clinical evaluation of safety and efficacy wasperformed for 1, 2, 4–7, 21, and 45 d after the procedure. The Vancouver Scar Scale (VSS) wasused to evaluate scarring.Results: Up to 21 d after the procedure, no safety device-related adverse events were reported.All patients had full closure of the epidermis, a very low total VSS score, and no evidence ofdischarge, redness, edema, or thermal damage. None of the patients exhibited more than amild degree of encrustation.Conclusion: The BioWeld1 System has been shown to be safe and effective for skin closure incesarean section.

Keywords

Chitosan, cold helium plasma, skin closure

History

Received 15 July 2013Revised 30 November 2013Accepted 23 December 2013Published online 3 February 2014

Introduction

Cesarean section is the most common major surgery in many

developed countries and is performed on tens of millions of

women annually worldwide. Therefore, adhering to the safest,

most effective technique with the fewest maternal complica-

tions is extremely important.

A variety of materials and techniques are used for skin

closure after cesarean section, but no conclusive evidence is

currently available regarding how the skin should be closed.

Non-suture methods offer advantages, including good tensile

strength, microbial barrier properties, negligible histotoxicity,

decreased pain, shorter application time, no need for suture

or staple removal, and reduced risk of needle-stick injury to

the surgeon or assistant [1–3].

In the pursuit of non-suture technology for skin closure,

IonMed Ltd. (Yokneam, Israel) has developed the novel

BioWeld1 system. The BioWeld1 system consists of a cold-

plasma ejecting generator and surgical handpiece with a

chitosan film (ChitoPlastTM, Millipore Corporation, Billerica,

MA). The ejection of cold helium plasma on the chitosan

welds the wound. Chitosan is a widely used biomaterial with

known biocompatibility and hemostatic properties. The pearl-

colored, odorless, and non-toxic chitosan is produced com-

mercially by the full or partial deacetylation of chitin, which

is the structural element in the exoskeleton of crustaceans

(e.g. crabs and shrimps) and the cell walls of fungi. Chitin is a

high molecular weight nitrogen-containing polysaccharide in

which monomers occur with the glycosidically linked com-

ponents beta [1,4]. Chitin is a fiber, and it presents

exceptional chemical and biological qualities that can be

used in many industrial and medical applications.

Chitosan has good biocompatibility and biodegradability

and is capable of accelerating the wound healing process.

Therefore, this material has been widely applied for cell

scaffolding, the controlled release of pharmaceuticals, and

wound dressing. Due to its intrinsic hemostatic properties,

chitosan is indicated for moderate to severe hemorrhage and

is currently used for hemostasis in emergency and military

settings [4–7].

The benefit of plasma treatment is the contactless, pain-

free, non-invasive, and pure physical application, which

simultaneously benefits the patient and health care provider.

Non-thermal gas plasma (cold plasma) is a new and rapidly

developing technology that has great potential to change the

face of wound care. In contrast to thermal plasma systems,

*Y. Ezra is a medical consultant for IonMed Ltd.

Address for correspondence: Yael Hants, M.D., Department of Obstetricsand Gynecology, Hadassah-Hebrew University Medical Center, Ein-Kerem, P.O. Box 12000, Jerusalem 91120, Israel. Tel: +972 50 5172293. Fax: +972 2 6777 541. E-mail: yhants@gmail.com

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which induce temperatures of over 80 �C, the cold plasma

BioWeld1 system does not induce heat or thermal damage to

the surrounding tissue. In addition to its potential to facilitate

tissue welding, cold plasma has been shown to benefit

disinfection, hemostasis, angiogenesis, and wound repair,

and to have anti-cancer effects. For example, the results of

two clinical trials demonstrated the safety and efficacy of

cold atmospheric argon plasma for treating chronic wounds

in patients [8–12].

This preliminary study was designed to evaluate the safety

and performance of the BioWeld1 system as two distinct

endpoints. The novel technique was assessed for surgical

incision closure in women scheduled for elective cesarean

section.

Methods

BioWeld1 system

The BioWeld1 system is a novel technology to ‘‘bio-weld’’

incisions using cold plasma, incorporating the use of a special

chitosan plaster (ChitoPlast). Initially, the incision area

is covered with the ChitoPlast (Figure 1). The BioWeld1

generator uses radiofrequency (RF) energy to ionize the

helium gas flowing from a tank, transforming it into cold

plasma. The plasma flows out of a handheld probe and

interacts with the incision area where the ChitoPlast was

applied. The plasma energy enhances the chitosan-mediated

closure of the wound and promotes the natural healing

processes.

The ChitoPlast is composed of three main parts: two strips

of medical plasters composed of a non-woven commercial

plaster (3M�) coated with hypoallergenic, pressure-sensitive

acrylate adhesive, protected by silicon liners until application

to the skin; narrow strips of medical plaster composed of

a soft polyurethane pad with polyester filaments (3M�) for

reinforcement of the ChitoPlast; and the Chitosan film applied

to the incision itself.

The plasma device (Figure 2) includes a helium tank

that supplies the helium gas to the main unit of the RF

generator, which provides the RF signal and gas to a hand

piece.

Patients

Patient enrollment for this prospective, single center, non-

randomized study began in November 2012 and was

completed in January 2013. Patients were enrolled at the

Republican Institute of Reproductive Health, Perinatology,

Obstetrics, and Gynecology, Yerevan, Armenia. Patient

evaluations included a screening assessment before surgery

and post-operative assessments at 1, 2, 4–7, 21, and 45 d.

The screening process involved the collection of demographic

information, height, weight, medications, and medical

history (Table 1). A physical examination was performed

and the patient’s eligibility for the study checked against the

inclusion and exclusion criteria.

The study population consisted of 20 healthy women

undergoing elective cesarean section. The patients were aged

between 20 and 40 years with a range of BMI 18.6–24.8 prior

to pregnancy. The exclusion criteria were past or present

radiotherapy or chemotherapy, treatment with steroids (or

any other medication that interferes with wound healing),

treatment with Acutan in the last 6 months, bleeding diath-

esis or hypercoagulable state, prior cosmetic or medical

treatment in the incision area (e.g. phosphatidylcholine

injections), or pre-procedure thrombocytopenia (platelet

count 5100 000/mm3). Intra-operative exclusion criteria

were severe or excessive wound bleeding.

The study protocol was reviewed and approved by the

appropriate ethics committee, the institutional review board

of Yerevan State Medical University after the Mkhitar Heratsi

Ethics Committee. Written informed consent was obtained

from all patients.

Surgical procedure

A standard surgical technique was performed through a

Pfannenstiel incision. In patients with previous cesarean

section, the scar was removed. The transverse lower segment

uterine incision was closed with two layers of continuous

0 polyglactin suture (Vicryl, Ethicon, Piscataway, NJ).

The fascia was closed with a continuous 0 polydioxanone

suture (PDS II, Ethicon, Somerville, NJ). The subcutaneous

layer was closed with a 00/000 polyglactin suture. Skin

approximation was performed with the BioWeld1 system. All

operative procedures were performed by the same team of

surgeons. All patients received intravenous oxytocin (10 IU)

and prophylactic antibiotics immediately after the delivery of

the newborns.

Post-surgical analgesic treatment consisted of diclofenac

with or without Analgin and Dimedrol (depending on the

physicians’ preferences).

Safety assessment

The primary outcome measure was adverse events, such as

burns, wound dehiscence, or the need for additional surgical

procedures for the skin wound during the first 21 d after

the operation. Adverse events were categorized according

to severity, seriousness, expectedness, and relationship

to the device and/or procedure. The assessment was per-

formed by the physician during visits and according to patient

reports.Figure 1. BioWeld1 ChitoPlast.

2 Y. Hants et al. J Matern Fetal Neonatal Med, Early Online: 1–6

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The following blood tests were obtained up to 10 d prior

to the procedure: complete blood count (CBC), liver function

tests, creatinine, coagulation profile (PT, PTT), and fibrino-

gen. CBC was also obtained 4–7 d after the procedure at

a follow-up visit. All results were reported as either normal

or abnormal according to the range given by the lab.

Abnormal results such as burns, wound dehiscence, and the

need for additional surgical procedure were reported as

clinically significant (CS).

Skin swabs were collected from the skin adjacent to the

incision during the procedure and, if required (at the

physician’s discretion), during follow-up visits. The result

was reported as positive (including the type of bacterial

growth) or negative.

Efficacy assessment

The incision parameters were evaluated by the physician

during the follow-up visits according to specific grading

scales. Approximation and alignment of the wound edges

(only on postoperative days 1 and 2), redness and edema,

encrustation, discharge from the incision, and thermal damage

were evaluated as 0 – normal, 1 – mild, 2 – moderate, or 3 –

severe. Epidermal closure (postoperative day 3 or later) was

Figure 2. Schematic of the plasma device.

Table 1. Demographic characteristics.

Baseline data N Mean Std Min Median Max

Age (years) 20 27.9 5.8 19.8 27.1 38.5Height (cm) 20 159.2 6.5 146.0 158.5 175.0Weight (kg) 19 71.2 13.0 51.0 69.0 113.0BMI prior pregnancy 20 22.6 2.4 18.6 24.0 24.8Delivery number N %

First 8 40Second 9 45Third 2 10Sixth 1 5Total 20 100

C-section number N %First 16 80.0Second 4 20.0Total 20 100

DOI: 10.3109/14767058.2013.879114 Evaluation of a novel technique for wound closure 3

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evaluated as 0 – closed, 1 – partially open, and 3 – open. The

incision was photographed during the procedure and at each

of the follow-up visits.

Subjective incision area pain was assessed by a visual

analogue scale (VAS). Each patient was asked to evaluate

the intensity of her pain during all follow-up visits by marking

a vertical line along a 100-mm horizontal line. The VAS score

was determined by measuring (in millimeters) from the left

end of the line to the point the patient marked.

The Vancouver Scar Scale (VSS) was used at the 21 and

45 d follow-up visits to quantify the scar appearance in

response to treatment. The VSS includes an assessment of

four variables, each assessed according to a specific grading

scale (total scores 0–13): vascularity (0 – normal, 1 – pink,

2 – red, and 3 – purple); pigmentation (0 – normal, 1 –

hypopigmentation, and 2 – hyperpigmentation); pliability

(0 – normal, 1 – supple, 2 – yielding, 3 – firm, 4 – ropes,

and 5 – contracture); and height (0 – flat, 1 – less than 2 mm,

2 – 2–5 mm, and 3 – greater than 5 mm). After all the

variables were given scores, the total score was calculated

by adding each of the variable scores for each patient.

The performance endpoint comprised complete epidermal

closure, redness and edema grade51, encrustation grade51,

discharge from wound negative, and photographic evidence

of clean healing at postoperative day 21. The exploratory

endpoint comprised VAS evaluation of pain 4–7 d after

procedure, VSS evaluation of scar formation during the long-

term follow, analgesic use not exceeding usual prescription

practice, antibiotic usage similar to or less than usual closure

procedure at the medical center, closure duration similar to

intradermal sutures based on the investigator evaluation

questionnaire, and device performance.

Statistical analysis

The planned sample size was 16 women based on an expected

success rate of 100% for the primary endpoint (i.e. 0 failures

defined as procedure-related adverse events, with 95%

confidence interval (CI) 21 d after the procedure). When the

sample size is 16, a one-sided 95% CI for a single proportion

using the large sample normal approximation will extend

0.015 from the observed proportion for an expected propor-

tion of 1.0. Due to the fact that four patients withdrew from

the study prior to the 21-d follow-up due to non-safety device-

related reasons, an additional four patients were recruited.

For the primary safety endpoint, a 95% CI was calculated

for the proportion of subjects having adverse events. All

adverse events were coded according to coding dictionaries

(MedDRA version 12.1 or higher, McLean, VA) and

presented in summary tables based on system organ class

(SOC) and preferred term (PT). In addition, a 95% CI was

calculated for the proportion of subjects meeting the

performance endpoint criteria.

Results

A total of 20 Caucasian patients were enrolled in the study;

two of them were lost to follow-up 4–7 d after the procedure

and another two were withdrawn from the study prior to

21 d because they did not arrive to the physician’s evaluation

as scheduled. However, these patients were followed up

at 21 d for the safety analysis. The mean age and BMI

were 27.9 years and 22.6, respectively. Forty percent of the

patients were nulliparous, and for four of the patients, the

evaluated delivery was their second cesarean section delivery.

Figures 3 and 4 provide a representative image of a patient’s

wound (patient #5) on the day of operation and 7 d after. Until

this study, follow-up was completed up to 45 d post-operation.

Adverse events

A total of two adverse events were reported in two

patients (N¼ 2, 10%) up to 21 d: one adverse event (endo-

metritis and infiltration from the deep layers to the cutaneous

layer) was classified as a serious adverse event (SAE),

expected and not related to the study device. A second

adverse event was a big step along the middle section of the

incision, but the incision was completely closed. This

was classified as an adverse event, expected and related to

the study device.

Both adverse events were reported at the 4–7 d post-

operative follow-up visit. Thermal damage from the

BioWeld1 device was not assessable 1 and 2 d after the pro-

cedure due to the presence of the ChitoPlast on the incision.

However, at the 4–7, 21, and 45 d follow-ups, we found

no evidence of thermal damage.

Figure 3. Incision on the day of operation.

Figure 4. Incision on post-operative day 7.

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Blood and skin tests

Blood results in most patients were normal or not clinically

significant at baseline and the 4–7 d follow-up. The patient

with endometritis had significantly elevated white blood

cell and neutrophil levels and decreased hemoglobin levels,

which were all related to the SAE.

A total of 13 patients had negative skin swab results during

the procedure. However, the seven positive results were all

within the normal range in terms of prevalence and bacterial

species.

Secondary endpoints

Efficacy data were available for 16 patients 21 d after the

procedure. At 21 d, the epidermis was fully closed in all

16 patients, presenting a closure success rate of 100% for the

BioWeld1 System for all incisions (N¼ 16, 95% CI 0.79–1.0).

Data available at 45 d for 11 patients also showed that the

epidermis was fully closed in all patients. Out of the eight

subjects in whom the epidermal layer of the incision was

partially separated at 4–7 d after the procedure, it was due

to the infection reported as an SAE in one patient, whereas

the dermis was fully closed in the other patients, but the

epidermal edges were still slightly apart.

At postoperative days 1 and 2, the degree of redness and

edema was difficult to assess due to the presence of the

ChitoPlast on the incision. At postoperative days 4–7, after

the removal of the ChitoPlast, we observed mild redness and

edema (score¼ 1) in three patients (15%). At postoperative

day 21, all patients (N¼ 16) had normal redness and edema,

corresponding with a success rate of a 100% (95% CI 0.79–

1.0). Furthermore, the data from 11 patients available at 45 d

reported normal redness and edema in 100% of the patients

(N¼ 11).

At postoperative days 4–7, 2/20 (10%), 17/20 (85%), and

1/20 (5%) patients exhibited normal, mild, and moderate

encrustation, respectively. At postoperative day 21, 13 of the

16 patients (81.3%) exhibited normal encrustation (95%

CI 0.54–0.96) and three of the 16 patients exhibited mild

encrustation.

At postoperative days 1 and 2, the degree of discharge

from the incision was assessed through the ChitoPlast and the

discharge absorbed in the adhesive film dressing. The number

of patients experiencing discharge and the degree of discharge

gradually decreased with time. At postoperative day 1, most

patients exhibited mild or moderate discharge (11/20, 55%

and 8/20, 40%, respectively). At postoperative day 2, 10 of the

20 patients (50%) experienced discharge; all the cases were

mild. At postoperative days 4–7, mild discharge was observed

for 5 of the 20 of the patients (25%). Only the patient

with endometritis experienced purulent discharge, which

originated from the infection in the deep layers of the incision.

At postoperative day 21, none of the incisions exhibited

discharge, corresponding to a success rate of 100% (95% CI

0.79–1.0). Furthermore, the data from 11 patients available

at 45 d reported no discharge from the incisions in 100% of

the patients (N¼ 11).

Clean healing was observed in most patients at post-

operative day 21, except for three subjects with minimal

encrustation. Thirteen patients (81.3%) had full epidermal

closure, normal redness and edema, no encrustation, and no

discharge.

Efficacy measures

The average pain level gradually decreased with each follow-

up visit, as expected, with the highest average score on

postoperative day 1 (1.5/10). The average pain evaluation at

4–7 d was significantly lower than the average pain evaluated

at 1 d. At 21 and 45 d, some patients still seemed to be

experiencing some pain, but the average was close to 0

(0.2/10 and 0.06/10, respectively). Pain resulting from the

removal of the ChitoPlast was lower than the general pain

the patients were experiencing at that moment.

Most patients had a VSS total score of 1 (11 patients,

68.8%) 21 d after the operation. Similar score ratios were

reported 45 d after the procedure: six patients with a total

score of 1 and three patients with a total score of 3.

Up to postoperative day 21, none of the patients received

any analgesic treatment in addition to the standard of care,

and only one of the patients received antibiotic treatment

in addition to the standard of care. Patient no. 1 received

additional antibiotics as a part of the SAE treatment.

Discussion

In this preliminary study, the BioWeld1 System was shown

to be safe and effective. The evaluation of the safety of the

BioWeld1 consisted of adverse events, blood tests, and skin

swabs. The wound complication rate following cesarean

section is approximately 2.5–16% [13,14]. Out of the two

adverse events in this study, one adverse event was found to

be related to the BioWeld1 procedure. In the first patient,

wound dehiscence was due to severe endometritis involving

all abdominal wall layers, which was not related to the device.

In the second patient, the wound was opened and re-sutured in

order to shorten the time until full healing. This type of

cosmetic defect is often seen in incisions closed with staples;

when the defects are not significant and the wound mostly

closed (as in this case), they are expected to close by

secondary intention healing [14]. In this case, it was the

surgeon’s decision to re-suture in order to shorten the time

until full healing.

The recent development of effective surgical non-thermal

plasma medical systems enables effective blood coagulation,

disinfection, and other favorable tissue effects of plasma

without the problematic thermal damage. The coagulation

effect is achieved through non-thermal plasma stimulation of

specific natural mechanisms of blood coagulation without any

‘‘cooking’’ or damage of the surrounding tissue. Non-thermal

plasma was confirmed experimentally to significantly hasten

blood coagulation in vitro and in vivo [12]. The results of two

clinical trials demonstrated the safety and efficacy of cold

atmospheric argon plasma for treating chronic wounds [8,9].

Correspondingly, in the present study, we found no evidence

of thermal damage in any of the patients.

Cold atmospheric plasma was shown previously to be

very effective against Gram-negative and Gram-positive

bacteria, spores, biofilm-forming bacteria, viruses, and

fungi [10]. This technique may constitute an effective

alternative to antiseptics and antibiotics for the eradication

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of skin and wound pathogens, including methicillin-resistant

Staphylococcus aureus. Furthermore, chitosan is suitable

for many medical and pharmaceutical applications due to

its numerous biocompatible properties: biodegradable by

enzymes, non-toxic, anti-inflammatory, not rejected in vivo,

bacteriostatic, and fungistatic [4–7]. As the BioWeld1 System

consists of cold helium plasma and chitosan, avoiding

placement of a foreign body within the skin tissue, less

inflammation of the skin is expected, and subsequently fewer

wound complications and better short-term results.

Although three patients had encrustation 21 d after the

procedure, it was mild and localized and expected to resolve

within a short time. Encrustation on the incision has also

been described for other closure methods.

Importantly, some degree of discharge is normal immedi-

ately after the procedure, and it is essential for the closure

method to allow drainage. The ChitoPlast applied on the

incision allows free drainage that is absorbed in the OPSITE,

leaving the skin dry. Closure duration with ChitoPlast seems

to be either longer or similar to intradermal sutures based

on surgeons’ opinions.

Overall, the system functioned properly with only two

mechanical problems that were easily resolved by replacing

the hand piece, without delay or risk to the patient. IonMed

is currently working on improving the ChitoPlast in order to

allow easier application and shorten application time.

In conclusion, the BioWeld1 System is safe and effective

for the closure of skin incisions in cesarean section. Further

studies may be needed in order to allow the implementation

of this technique in routine obstetric care.

Declaration of interest

Y. Ezra is a medical consultant for IonMed Ltd. All other

authors report no conflicts of interest. The authors alone are

responsible for the content and writing of this article.

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