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ONLINE EXCLUSIVES

Smart Dressings for Wound Healing: A Review

Barros Almeida, Isabella PhD; Garcez Barretto Teixeira, Luciana MS; Oliveira de Carvalho, Fernanda PhD; Ramos Silva, Érika PhD; Santos Nunes, Paula PhD; Viana dos Santos, Márcio Roberto PhD; Antunes de Souza Araújo, Adriano PhD

Author Information
Advances in Skin & Wound Care: February 2021 - Volume 34 - Issue 2 - p 1-8
doi: 10.1097/01.ASW.0000725188.95109.68
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Abstract

INTRODUCTION

Chronic wounds affect many people worldwide and can take a long time to heal. They can negatively affect quality of life, lead to changes in patient functioning, and incur high treatment costs. In developed countries, 2% of the population will experience a chronic wound at some point in their life.1 In the US, 6.5 million people are affected by chronic wounds, and the cost for their treatment is almost $25 billion annually.2,3 Besides increasing expenditure, chronic wounds increase hospitalization rates and have significant social and economic implications.4

Accordingly, decreasing the cost of chronic wounds is a major challenge for the medical and scientific communities.5 Dressings with precise, low-cost sensors can be used in a variety of medical conditions to help achieve this.6 Sensors for monitoring wounds are related to the main physiologic indicators such as temperature,7 moisture and pH,8 pressure,9 oxygen,10 and bacterial load.11 Biocompatibility and flexibility are important features in the development of sensors for chronic wound monitoring to avoid further damaging tissue.12 Biosensors can provide wireless data to inform clinical intervention, avoiding unnecessary wound dressing changes and reducing treatment costs.13

In the future, smart bandages will allow the monitoring of multiple wound parameters based on data acquisition from sensors integrated within the smart bandage, decreasing the time required to examine and monitor the wound.10 Because relatively few studies have reported on the effectiveness of sensors in dressings, investigators decided to perform a review of the literature on the subject to provide an overview of the work in this field.

METHODS

Search Strategy

Four databases (PubMed, Science Direct, Web of Science, and Scopus) were used to search for appropriate publications that met the criteria of this study, using different combinations of the following keywords: wound, bandage, and sensors. The databases were searched for studies published through April 2019 (when this search was conducted). The structured search strategy was designed to identify any published document that evaluated the presence of a device for monitoring wound healing. Additional articles were included after analysis of all references from the selected articles. The authors did not contact individual study investigators nor did they try to identify unpublished data.

Study Selection

All electronic search titles, selected abstracts, and full-text articles were independently reviewed by a minimum of two researchers. Disagreements over inclusion/exclusion criteria were resolved through consensus. A single inclusion criterion was applied: studies that evaluated the presence of a device within a dressing to improve wound management. Exclusion criteria were: studies that did not aim to evaluate performance in relation to wound healing, the use of sensors that were not wearable, review articles, meta-analyses, abstracts, conference proceedings, editorials/letters, and case reports.

Data Extraction

Data were extracted by one reviewer using standardized forms and were checked by a second reviewer. The following information was extracted from all the studies: study design, type of wound used to test the sensors, type of dressing and sensor used, purpose of the sensor, and results and conclusions of the study.

RESULTS

The process followed for article selection is presented in Figure 1. The authors found 501 articles in Science Direct, 40 in SCOPUS, 26 in the Web of Science, and 20 in PubMed (N = 587). After removing duplicates, the authors read 537 titles and abstracts. Forty-six articles were then selected to be read in full. After discarding articles without full text; letters to the editor; case studies; articles that were not in English, Spanish, or Portuguese; or whose theme did not meet the criteria of this study, 16 articles remained (Figure 1). There was a high level of agreement on inclusion/exclusion between the two investigators who screened the retrieved articles. The selected studies were performed in various countries, and the publications were produced between 2008 and 2019 (Table).

Figure 1.
Figure 1.:
SEARCH FLOW DIAGRAM
Table. - SUMMARY OF INCLUDED STUDIES
Authors, Year, Country Study Design Wound Type/Dressing Material Sensor Material and Purpose Results Conclusion
Babikian et al,18 2015, US Development and characterization study Not described/PDMS Flexible aluminum electric traces on thin polyester film, microfluidic channels and PDMS, integrated blue LEDs, and electrodes/biochemical analysis of blood The ITP assay demonstrates the ability to execute low-power rapid analysis of samples. The assay can be performed on the arm. Printed circuit boards and surface mount technologies can create integrated bioflexible electronic devices. The biochemical assay isotachophoretic separation/focusing and excitation of fluorescein molecules were successfully achieved on the bioflexible ITP chip for the first time.
Sharp and Davis,11 2008, UK Development and characterization study Surgical and burn wounds/adhesive plaster backing Laminated carbon fiber and a chloritized silver wire/periodic monitoring of urate directly within fluids typical of wound and monitor urate consumption in the presence of microbes The sensor is specific for pyocyanin oxidation, and the results are not affected by any of the other bacterially derived pigments or metabolites. The electrochemical sensor facilitates the detection of urate in bacterial colonies. The sensor can significantly aid in wound management and smart bandage development.
McColl et al,8 2009, UK Clinical study Venous leg ulcers/nonadhesive coating A pair of silver chloride electrodes/moisture monitoring The meter readings resulted in low impedance corresponding to “wet” (excess wound exudate); moisture band “moist” (moist wound on the front of the right leg) and moisture band “dry” (dry environment at the sensor-to-wound interface) for three patients; 100% did not feel the wound monitor. By identifying varying degrees of moisture, the wound monitor could become a useful tool in assessing the progress of treatment and supplementing clinical judgment of dressing changes.
Kassal et al,13 2015, UK, US, Brazil, and Croatia Development and characterization study Chronic wounds/transparent insulator An Ag/AgCl pseudoreference electrode and lead-carbon/sensitive and specific detection of uric acid Excellent analytical performance in terms of sensitivity, selectivity, operational stability, and robustness Smart bandages could reduce unnecessary wound dressing changes, generating significant cost savings, and reducing patient discomfort and allowing a custom application to monitor data transfer about wound status.
Mostafalu et al,10 2015, US Development and characterization study Chronic wounds/TangoPlus FLX930 and hydrogel Parylene-C, silver and electroplated zinc electrodes, potassium hydroxide gel, PDMS, and agarose hydrogel/oxygen monitoring The transient response of the oxygen sensor (1 h) showed a linear response with a sensitivity of 1.5 μA/% and a response time of 20 s The flexible sensors provide real-time updates on oxygen concentrations at the wound site to a remote computer or smartphone.
Hariz et al,16 2015, US Development and characterization study Chronic wounds/transparent adhesive silicone gel Temperature: LM94021B; moisture: Honeywell HIH4030 piezoelectric and Multicomp’s HCZ-D5; sub-bandage pressure: Interlink Electronics’ FSR406/temperature, moisture, and subbandage pressure The average temperature was 33 ± 1° C. The moisture values increased gradually. The subbandage pressure values were dependent on posture. The pressure readings dropped consistently over time The sensing system was capable of accurately measuring instantaneous changes in subbandage pressure, moisture, and temperature under compression bandages and dressings.
Pasche et al,14 2008, Switzerland Development and characterization study Chronic wounds/not described A portable sensing system consisting of a white LED and a detection spectrometer/real-time monitoring of pH changes and CRP concentration The sensor demonstrated reversible pH measurements between pH 6-8 and detected changes in CRP concentration between 1 and 100 μg/mL The portable sensing device opens up new perspectives for real time in situ sensing in ambulatory care.
Mehmood et al, 2013,26 Australia Development and characterization study Chronic wounds/biocompatible and PDMS LM94021B: temperature sensor; FSR406: interdigitated electrically conductive and a polymer with carbon-based ink; HCZ-D5: silver-carbon electrodes and polymer/real-time temperature, subbandage pressure, and moisture level information The sensing system was fabricated on a flexible circuit material, enabling it to adapt to limb contours. The low-power profile can be operated continuously under a compression bandage over a longer time period without disturbing the bandaged wound. Battery life can be enhanced by reducing the frequency of wound data transmission The sensing system is lightweight, reliable, flexible, and noninvasive with low-power consumption and wireless connectivity, which make it a strong candidate for use in continuous wound sensing and monitoring applications.
Mehmood et al,4 2014, Australia Development and characterization study Chronic wounds/biocompatible PDMS FSR406: interdigitated electrically conductive and a polymer with carbon-based ink; HCZ-D5: silver-carbon electrodes and polymer/pressure and moisture level The pressure sensor is flexible, noninvasive, and adaptable to limb morphology. Moisture measurement confirmed the reliability and accuracy of the sensing system in measuring transient changes in moisture level The system has advanced features and improved performance and can monitor pressure and moisture. The system automatically acquired data at a determined interval of 5 s.
Mehmood et al,17 2014, Australia Development and characterization study Chronic wounds/biocompatible silicone LM94021: temperature sensor; moisture sensor: HCZ-D5; FSR406: passive pressure sensor/real-time temperature, moisture, and bandage pressure monitoring The average change in pressure was 17.75% of the original value. The moisture graph indicated a high value (58%) when the sensor touched the skin, but the graph gradually dropped down. Average skin temperature was 35.25° C The technology reliably measures, transmits, and displays real-time information of temperature, moisture, and pressure from within a compression bandage. The capability to log the transmitted data of sensed parameters via a mobile device makes the process of clinical decision-making easier and more efficient.
Guinovart et al,9 2014, US and Spain Development and characterization study Chronic and acute wounds/a commercial adhesive bandage A set of screen-printed silver-silver chloride electrodes on a modified commercial adhesive bandage. The reference electrode is polyvinyl butyral polymer, and the working electrode is electropolymerized polyaniline/pH monitoring Bandage can detect pH fluctuations at a wound site for up to 100 min. The sensor displays good resiliency against mechanical stress. The performance is slightly affected by exposure to the autoclave. Increased sensitivity of the sensor is expected over time This pH-sensitive bandage allows new opportunities to embed sensors in a simple, low-cost, and robust fashion for the electrochemical assessment of wound healing.
Sharp et al,15 2010, UK Development and characterization study Not described/fiber layer and insulating polyester sheath Laminated carbon fiber tow electrodes/detection of pyocyanin production by Pseudomonas aeruginosa The quantification of pyocyanin is presented across the biomedically relevant concentration range. The electrode prototypes are potentially suitable to allow the early detection of P aeruginosa The proposed small and inexpensive sensor assembly is suggested for use in monitoring bacteria growth.
Koetse et al,6 2008, US Development and characterization study Not described/transparent thin film encapsulation Organic light-emitting red and yellow diodes and organic photodiodes/measuring the perfusion of microvascular tissue in the wound area with photoplethysmography The device had a relatively low efficiency and a strong angle-dependent emission. Preliminary noise measurements indicate an order of magnitude higher than reported in literature. The light produced an unacceptable amount of heat The modular approach allows for application in a variety of other fields including chemical sensing. This enables measurement of many physiologic parameters using the same bandage and the basic sensor architecture. Organic optoelectronic devices can also be used for the direct measurement of relative changes in physiologic parameters, such as skin perfusion.
Abbreviations: Ag/AgCl, silver chloride; CRP, C-reactive protein; ITP, isotachophoresis; LED, light-emitting diode; PDMS, polydimethylsiloxane.

Characteristics of Included Studies

The trials encompassed a variety of sensors incorporated into dressings to identify important markers for skin healing. The characteristics of the items discussed are set out in the Table.

Most studies examined sensor use with chronic wounds (n = 7), followed by acute wounds (n = 3), venous leg ulcers (n = 1), surgical wounds (n = 1), and wound infections (n = 1), but three did not report the injury condition. The moisture present in the wound was the most commonly evaluated indicator (n = 6), followed by temperature and pressure (n = 3), bacterial proliferation (n = 4), pH (n = 2), oxygen concentration (n = 1), tissue perfusion (n = 1), and an evaluation of clinical blood biochemistry (n = 2).

Current efforts aim to monitor the wound using a noninvasive biocompatible sensor (incorporated into a dressing or under a compression bandage).12 In this review, various materials were used for the dressings, primarily silicone, although some were not described in detail. The materials included biocompatible polydimethylsiloxane (n = 3); silicone gel comprising both adhesive and nonadhesive elements (n = 1); biocompatible silicone with a hydrogel coating (n = 1); commercial adhesive tape (n = 1); tape (n = 1); a polyester layer (n = 1); transparent film (n = 1); a nonadhesive coating (n = 1); a transparent insulator (n = 1); fibrous layers (n = 1); hydrogel film with carrageenan, locust bean gum, and cranberry extract (n = 1); fibrous configuration (n = 1); and silicone master (n = 1). Only Pasche et al14 did not report what type of material they used to incorporate the sensor.

An extensive variety of products were used in the preparation of the monitoring devices. Silver electrodes were used in eight studies; among these, six studies allied the silver electrode with carbon fiber. Mostafalu et al10 used galvanized zinc with a silver electrode. However, Sharp et al15 used only laminated carbon fiber electrodes. Three articles combined a light-emitting diode with detection electrodes (Table).

The transmission of information detected by a sensor to a receiving device plays an important role in the search for an ideal smart dressing.16 To this end, a noninvasive wireless method is required.17 Many such technologies are currently available, but in this research, investigators found only six studies using a wireless transmission system. Other sensors use electrochemical detection for receiver data instead of wireless transmission.10,13,16,17

All the dressings that included smart biosensors could perform the function assigned to them in the test. The studies highlighted the importance of the data collected by the equipment, and sensors’ role in changing the paradigms of clinical intervention and reducing treatment costs. Although there are costs associated with the various systems studied, the devices allow wound healing to be monitored without removing the dressing, cutting costs and demands on hospital resources.16

Babikian et al18 found that using a printed circuit board and a thin, flexible, low-power electronic device within a comfortable biocompatible wound dressing allowed numerous functions essential for the biochemical analysis of samples such as blood. Sharp and Davis11 demonstrated that a modified carbon network is sensitive to urate in bacterial colonies, and the sensor’s simple manufacturing offers a clear advantage over conventional urate measurements.

The clinical trial by McColl et al8 showed that their device identified different levels of moisture present in wounds, thus becoming a useful tool for determining the number of required dressing changes. Kassal et al13 demonstrated excellent performance of a wireless smart dressing developed for detecting uric acid in the wound. Yang et al19 showed that a flexible bandage was effective in quickly and visually detecting nucleic acids, which can later be used for online detection of pathogens for wounds, diagnosis of tumor biomarkers, and the detection of molecular lesions of epidermal cells. Flexible oxygen sensors described in the article by Mostafalu et al10 provided real-time updates on oxygen concentrations at the wound site.

The articles by Hariz et al16 and Mehmood et al17 proposed the integration of commercially available sensors in a single bandage. Hariz et al16 obtained an average temperature value of 33 ± 1° C, with humidity gradually increasing and pressure values dependent on posture. Mehmood et al17 tested this pressure sensor for the first time on a mannequin leg, showing that it is flexible, noninvasive, and adaptable to limb morphology. In 2014, Mehmood’s study group published two articles4,17 proposing chronic wound monitoring with a dressing composed of smart wireless sensors. The first17 described a system with enhanced functionality that could perform transient measurement of the humidity level and pressure. The second4 reported the development of technology that reliably measures, transmits, and displays real-time information about temperature, humidity, and pressure, thereby confirming the appropriateness of the detection system for the diagnosis of chronic wounds.

Guinovart et al9 developed a bandage that could identify pH variations in the wound at relatively long intervals (100 minutes). The research conducted by Sharp et al15 promoted the use of their biosensor for monitoring the growth of Pseudomonas aeruginosa by means of electrochemical measurements for pyocyanin. One other in vitro study20 of Staphylococcus aureus and P aeruginosa demonstrated that color changes in the study sensor could be observed by the naked eye, confirming its use as a visual system for monitoring bacterial wound infections. Bazbouz and Tronci21 developed a sensor that was intended for controlled exudate management capability and visual infection responsivity. This sensor could activate functionalities induced by critical structures for the management and monitoring of chronic wounds. Finally, Koetse et al6 applied an optical detection unit capable of measuring physiologic parameters such as skin perfusion.

DISCUSSION

There is growing interest in research on wounds, but studies on sensors that monitor important markers of wounds are still scarce. In this review, investigators found only one clinical study with 15 patients where a sensor and a dressing were applied to monitor wound moisture.8 The application of sensors in humans is important for developing a better assessment of the wound and improving the reliability of new products. Chronic wounds were the most studied wound type in this review. Chronic wounds are those characterized by nonhealing, and are more susceptible to infection, making their treatment more difficult and time consuming.5

The costs of treating chronic wounds are high, both for the patient and for the public health system. Sensors can help reduce these costs by properly monitoring the chronic wound, avoiding unnecessary dressing changes, and improving patient quality of life13 because changing a dressing often causes pain and stress to the patient.22

The ideal dressing must fulfill numerous, often competing requirements (prevents contamination; neutralizes odor; maintains adequate moisture; requires infrequent changes; promotes autolytic debridement; and is absorbent, conformable, antimicrobial, painless, and cheap) and as such is impossible given clinical realities; nothing currently available comes close to that ideal.23 The biosensors that were developed for the studies in this review can act in conjunction with wound dressings and may help to reduce treatment time, but require further study—clinical trials in particular.

For example, the biosensors included in this review have been studied for application in clinical practice, to aid health professionals, and to hinder the progression of injuries with surface monitoring. However, it is not yet known whether these sensors actually help to reduce the costs of dressing changes. Despite the likelihood that in the future these sensors could reduce the costs of wound treatment, it is premature to talk about specific numbers, because this factor is rarely addressed in available data.

Further, given the range of dressings on the market, it would be extremely interesting to develop comparative studies with the biosensors that are being developed and the most common dressings currently in practice.

Some dressing sensors can stay in place on a wound for days and wirelessly transmit data to a computer, tablet, or smartphone. This is an ideal route to fully exploit the advantages of radio, wireless, or Bluetooth technology.9 This allows the health professional and the patient to receive frequent updates on the state of the wound, alleviating patient anxiety, avoiding unnecessary hospital visits, and reducing medical device bulk. In addition, wireless technology could considerably reduce healthcare spending.4,10,13,16,17

Mostafalu et al10 created a simulated wound environment using hydrogel, and their device allowed for continuous oxygen measurement for 1 hour. The output was linear, with 1.5 μA/% oxygen concentration and a response time of 20 seconds. All of the studies sought to monitor wound status over time, with the sensor remaining at the site of the injury for hours or days. More research is still needed about the use of these sensors in humans to establish the duration of their possible effectiveness on the skin.

In some studies, important parameters for controlling the progression of a wound such as pressure, humidity, temperature, and pH were evaluated,4,8,9,16,24 and one group of researchers studied all four using a single dressing.16 Controlling these parameters can potentially decrease the cost of wound care, particularly in chronic diabetic wounds (Figure 2).25

Figure 2.
Figure 2.:
SCHEMA OF WOUND PARAMETERS MONITORED BY THE AUTHORSImages reprinted with permission.

Pressure sensors could help in the correct application of dressings, minimizing pain to the patient. Further, those monitoring moisture in real time could indicate the correct time to change the dressing, optimizing resource allocation. Wound bed pH monitoring could detect infections and provide warnings about the proliferation of bacteria.26,27

Rahimi et al28 proved that it is possible to develop a low-cost flexible pH sensor for monitoring wounds, using available material to allow for large-scale production. The sensor achieved target sensitivity, repeatability, stability, and biocompatibility, making it suitable for integration with low-cost dressings.

The growing population of older adults has increased the incidence and prevalence of diabetes, raising the costs of diabetic foot ulcers. Monitoring skin temperature values can help prevent diabetic foot ulcer recurrence and assist in intervention selection and the clinical enhancement of the wound; sensors could assist in this manner.27

One point made by all of the studies was the importance of constructing a sensor on a flexible platform so that it can be placed directly on the skin without causing pain and without limiting patient mobility, and an accompanying ability to remain at the wound site for a few days to enable continuous monitoring. Flexible substrates such as some polymers, including Parylene, can help to maintain freedom of movement.12

The electrochemical detection of wound biomarkers is also an option with the construction of new types of sensors using modified electrodes capable of recognizing some biologic markers such as enzymes that generate an electrochemical signal.29 Some studies opted to manufacture sensors that can investigate the periwound electrochemical environment and showed them to be effective in periodic wound monitoring. For example, Sharpe et al27 and Sharp and Davis11 developed an electrochemical sensor for bacterial detection; however, other uses for this type of sensor are also possible. Babikian et al18 developed an intelligent dressing that can perform many types of biochemical blood analysis using three types of technology (electronic, microfluidic, and optic).

Mostafalu et al10 created a localized, three-dimensional printed smart wound dressing incorporating an oxygen sensor and a wireless transmission system using off-the-shelf components capable of accurate, controlled real-time topical drug delivery with the goal of accelerating healing. The dressing has a microparticulate N-isopropylacrylamide base that can be thermally stimulated to release the desired treatment.

Existing dressings can provide good results when used correctly.23 These authors believe that biosensors may provide better results in the clinic but may not reduce costs, because the actual treatment of the lesion is always more important for the patient than monitoring. In this sense, treating the cause of the wound is always the best option to reduce the need for more expensive dressings and enhance recovery for the patient. However, this does not devalue the potential of biosensors as an adjunct in clinical practice.

It is expected that in the future smart dressings will have an interface capable of integrating several electrodes that can read different parameters from the wound in addition to having drug reservoirs with various distribution channels.10 The challenge of producing this kind of dressing involves integrating optical and biochemical systems in a single flexible bandage that can be manufactured on a large scale and at low cost (Figure 3).18

Figure 3.
Figure 3.:
INTEGRATED BIOFLEXIBLE ELECTRONIC DEVICEA, Can be worn comfortably for the electrochemical analysis of blood.17 B, Oxygen sensor on a flexible bandage placed on the arm.10 C, Wireless sensing system measuring temperature, moisture, and pressure.16Images reprinted with permission

CONCLUSIONS

This review shows that there are still gaps in the development of wound sensors. Although all of the sensors in the selected studies were biocompatible and flexible and could be in direct contact with the wound without inhibiting healing, most have not yet been tested in humans and are not commercially available. Chronic wounds were the main focus of the studies because they are difficult to treat, and sensors that can transmit data in real time offer the possibility of better treatment with reduced costs. Future studies involving the evaluation of different parameters and with sensors incorporating the distribution of drugs into a single dressing may further help in wound monitoring and treatment.

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Keywords:

bandage; chronic wounds; monitoring; sensors; smart dressings; wound care

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