Clinical Physiology of Circulation

ISSN 1814-6910 (Print)
ISSN 2410-9134 (Online)

 

Chief Editor

Leo A. Bockeria, MD, PhD, DSc, Professor, Academician of Russian Academy of Sciences, President of Bakoulev National Medical Research Center for Cardiovascular Surgery


Issue's catalogue ➤ КФК. 2023; 20 (3): 203-320 ➤ Методы определения и мониторирования биомаркеров состояния кровоснабжения тканей на экспериментальных моделях и при кожно-пластических операциях

Methods for determining and monitoring biomarkers of the state of blood supply to tissue in experimental models and during skin-plastic surgery

Authors: Bagyan A.R., Malinin A.A.

Company:
Bakoulev National Medical Research Center for Cardiovascular Surgery, Moscow, Russian Federation

E-mail: Сведения доступны для зарегистрированных пользователей.

DOI: https://doi.org/10.24022/1814-6910-2023-20-3-242-253

UDC: 612.816.4-092.9

Link: Clinical Physiology of Blood Circulaiton. 2023; 3 (20): 242-253

Quote as: Bagyan A.R., Malinin A.A. Methods for determining and monitoring biomarkers of the state of blood supply to tissue in experimental models and during skin-plastic surgery. Clinical Physiology of Circulation. 2023; 20 (3): 242–53 (in Russ.). DOI: 10.24022/1814-6910-2023-20-3-242-253

Keywords:  skin plastic surgery shave-therapy surgery skin autotransplantation plastic surgery with local tissues determination of tissue blood supply tissue viability

Received / Accepted:  04.08.2023 / 13.09.2023

Full text:
Subscribe 🔒

Abstract

The review is devoted to methods for determining the blood supply to various types of skin flaps that are used in skin plastic surgery. To improve treatment results, methods of constant monitoring of the state of their blood supply are used, as the main factor in their viability. They must have such important characteristics as simplicity, accessibility, reproducibility, reliability and the possibility of monitoring. The review analyzes the main factors of the study and new devices based on nanotechnology, biosensors for determining various biomarkers by wirelessly monitoring the state of blood supply to skin flaps. Modern technological methods for monitoring biomarkers with wearable devices that, based on microsensors, transmit research results in real time are presented. Detection of tissue ischemia of the skin flap allows treatment and avoidance of its death. The information presented in the review gives an idea of the current technological level of tissue viability monitoring devices. This will allow surgeons to choose the most appropriate method of monitoring the state of the autograft blood supply for a specific type of skin flap, which will make it possible to improve the results of the operation by timely changing treatment tactics.

References

  1. Sun B.K., Siprashvili Z., Khavari P.A. Advances in skin grafting and treatment of cutaneous wounds. Science. 2014; 346: 941–5. DOI: 10.1126/science.1253836
  2. Tomioka Y., Sekino M., Gu J., Kurita M., Yamashita S., Miyamoto S. et al. Wearable, wireless, multi-sensor device for monitoring tissue circulation after freetissue transplantation: a multicentre clinical trial. Sci. Rep. 2022; 12: 16532. DOI: 10.1038/s41598-022- 21007-8
  3. Fawzy A., Putranti I.O. Perioperative management of the facial wounds with insight of scar prevention. Int. J. Med. Sci. Clin. Res. Studies. 2022; 2 (10): 1028–37. DOI: 10.47191/ijmscrs/v2-i10-01
  4. Малинин А.А., Прядко С.И., Пескова А.С., Чомаева А.А. Тактика лечения трофических венозных язв с хирургическим дебридментом и одномоментной аутодерматопластикой. Флебология. 2022; 16 (2): 130–8. DOI: 10.17116/flebo20221602122
  5. Конради А.О. Биомаркеры, их типы и основы применения в персонализированной медицине. Российский журнал персонализированной медицины. 2022; 2 (3): 6–16. DOI: 10.18705/2782-3806-2022-2-3-6-16
  6. Zai W., Yuan Y., Kang L., Xu J., Hu Y., Kang L., Wu J. Oxygen penetration through full-thickness skin by oxygen-releasing sutures for skin graft transplantation. Engineering. 2023; 29: 83–94. DOI: 10.1016/j.eng.2023.05.006
  7. Özsoylu D., Janus K.A., Achtsnicht S., Wagner T., Keusgen M., Schöning M.J. (Bio-) Sensors for skin grafts and skin flaps monitoring. Sensors Actuators Rep. 2023; 100163. DOI: 10.1016/j.snr.2023.100163
  8. Berthelot M., Henry F.P., Hunter J., Leff D., Wood S., Jallali N. et al. Pervasive wearable device for free tissue transfer monitoring based on advanced data analysis: clinical study report. J. Biomed. Opt. 2019; 24 (6): 1–8. DOI: 10.1117/1.JBO.24.6.067001
  9. Lu Di, Li S., Yang Q., Arafa H.M., Xu Y., Yan Y. et al. Implantable, wireless, self-fixing thermal sensors for continuous measurements of microvascular blood flow in flaps and organ grafts, biosensors. Bioelect. 2022; 206: 114145. DOI: 10.1016/j.bios.2022.114145
  10. Li Z., Roussakis E., Koolen P.G.L., Ibrahim A.M.S., Kim K., Rose L.F. et al. Non-invasive transdermal twodimensional mapping of cutaneous oxygenation with a rapid-drying liquid bandage. Biomed. Opt. Express. 2014; 5: 3748. DOI: 10.1364/BOE.5.003748
  11. Guo H., Bai W., Ouyang W., Liu Y., Wu C., Xu Y. et al. Wireless implantable optical probe for continuous monitoring of oxygen saturation in flaps and organ grafts. Nat. Commun. 2022; 133009. DOI: 10.1038/s41467-022-30594-z
  12. Mehrara B.J., Santoro T.D., Arcilla E., Watson J.P., Shaw W.W., Da Lio A.L. Complications after microvascular breast reconstruction: experience with 1195 flaps. Plast. Reconstr. Surg. 2006; 118: 1100–9. DOI: 10.1097/01.prs.0000236898.87398.d6
  13. Chen K.-T., Mardini S., Chuang D.C.-C., Lin C.-H., Cheng M.-H., Lin Y.-T. et al. Timing of presentation of the first signs of vascular compromise dictates the salvage outcome of free flap transfers. Plast. Reconstr. Surg. 2007; 120: 187–95. DOI: 10.1097/01.prs.0000264077.07779.50
  14. Kohlhauser M., Luze H., Nischwitz S.P., Kamolz L.P. Historical evolution of skin grafting – a journey through time. Medicina (B. Aires). 2021; 5: 7348. DOI: 10.3390/medicina57040348
  15. Mofikoya B.O., Ugburo A.O., Belie O.M. Clinical assessment score for monitoring free flaps in the dark skin. Alban. J. Med. Heal. Sci. 2018; 49: 18–22.
  16. Каторкин С.Е., Сушков С.А., Кушнарчук М.Ю. Современные стандарты хирургического лечения венозных трофических язв нижних конечностей. Новости хирургии. 2021; 29 (1): 75–89. DOI: 10.18484/2305-0047.2021.1.75
  17. Oda T., Kato H., Nakamura M., Morita A. Analysis of biomonitoring data after full-thickness skin grafting. J. Dermatol. 2021; 48: 1035–43. DOI: 10.1111/1346- 8138.15873
  18. Nsaful K.O., Paintsil A.B., Dakubo J.C.B., Nsaful J., Appiah-Labi K., Nartey E. Evaluation of bacterial infection of split-thickness skin grafts at the Korle Bu teaching hospital. Bali Med. J. 2020; 9: 259–65. DOI: 10.15562/bmj.v9i1.1760
  19. Khan A.Z., Utheim T.P., Byholt M., Fiabema T., Sylvester-Jensen H.C., Tønseth K.A. Skin grafting. Tidsskrift. Den. Norske, Legeforening. 2022; 142: 1–7. DOI: 10.4045/tidsskr.21.0671
  20. Lee J.-H., You H.-J., Lee T.-Y., Kang H.J. Current status of experimental animal skin flap models: Ischemic preconditioning and molecular factors. Int. J. Mol. Sci. 2022; 23 (9): 5234. DOI: 10.3390/ijms23095234
  21. Ogawa A., Nakagawa T., Oda G., Hosoya T., Hayashi K., Yoshino M. et al. Study of the protocol used to evaluate skin-flap perfusion in mastectomy based on the characteristics of indocyanine green. Photodiagn. Photodyn. Ther. 2021; 35: 102401. DOI: 10.1016/j.pdpdt.2021.102401
  22. Marks H., Bucknor A., Roussakis E., Nowell N., Kamali P., Cascales J.P. et al. A paintable phosphorescent bandage for postoperative tissue oxygen assessment in DIEP flap reconstruction. Sci. Adv. 2020; 6 (51): eabd1061.
  23. Gu J., Tomioka Y., Kida K., Xiao Y., Saito I., Okazaki M. et al. Measurement of optical reflection and temperature changes after blood occlusion using a wearable device. Sci. Rep. 2020; 10: 11491. DOI: 10.1038/s41598-020-68152-6
  24. Bian H.Z., Pek C.H., Hwee J. Current evidence on the use of near-infrared spectroscopy for postoperative free flap monitoring: a systematic review. Chinese. J. Plastic Reconstruc. Surg. 2022; 4: 194–202. DOI: 10.1016/j.cjprs.2022.08.008
  25. Bui D.T., Cordeiro P.G., Hu Q.-Y., Disa J.J., Pusic A., Mehrara B.J. Free flap reexploration: indications, treatment, and outcomes in 1193 free flaps. Plast. Reconstr. Surg. 2007; 119: 2092–100. DOI: 10.1097/01.prs.0000260598.24376.e1
  26. Halani S.H., Hembd A.S., Li X., Kirby B., Beard C.C., Haddock N.T., Suszynski T.M. Flap monitoring using transcutaneous oxygen or carbon dioxide measurements. J. Hand. Microsurg. 2022; 14: 10–8. DOI: 10.1055/s0040-1718862
  27. Copelli C., Tewfik K., Cassano L., Pederneschi N., Catanzaro S., Manfuso A., Cocchi R. Gestione del fallimento dei lembi liberi in chirurgia Testa-Collo. Acta Otorhinolaryngol. Italica. 2017; 37: 387–92. DOI: 10.14639/0392-100X-1376
  28. Smith M.K., Mooney D.J. Hypoxia leads to necrotic hepatocyte death. J. Biomed. Mater. Res A. 2007; 80 (3): 520–9. 29. Song Y., Mukasa D., Zhang H., Gao W. Self-powered wearable biosensors. Accounts Mater. Res. 2021; 2: 184–97. DOI: 10.1021/accountsmr.1c00002
  29. Özsoylu D., Wagner T., Schoning M.J. Electrochemical cell-based biosensors for biomedical applications. Curr. Top. Med. Chem. 2022; 22: 22713–733. DOI: 10.2174/1568026622666220304213617
  30. Gil Rosa B., Akingbade O.E., Guo X., Gonzalez-Macia L., Crone M.A., Cameron L.P. et al. Multiplexed immunosensors for point-of-care diagnostic applications. Biosens. Bioelectron. 2022; 203: 114050. DOI: 10.1016/j.bios.2022.114050
  31. Morales-Narváez E., Dincer C. (Eds.) Wearable physical, chemical and biological sensors. Elsevier; 2022.
  32. Rodrigues D., Barbosa A.I., Rebelo R., Kwon I.K., Reis R.L., Correlo V.M. Skin-integrated wearable systems and implantable biosensors: a comprehensive review. Biosensors. 2020; 10: 79. DOI: 10.3390/bios10070079
  33. Ates H.C., Nguyen P.Q., Gonzalez-Macia L., MoralesNarváez E., Güder F., Collins J.J., Dincer C. End-toend design of wearable sensors. Nat. Rev. Mater. 2022; 7: 887–907. DOI: 10.1038/s41578-022-00460-x 35.
  34. Cheng S., Gu Z., Zhou L., Hao M., An H., Song K. et al. Recent progress in intelligent wearable sensors for health monitoring and wound healing based on biofluids. Front. Bioeng. Biotechnol. 2021; 9: 1–21. DOI: 10.3389/fbioe.2021.765987
  35. Tang N., Zheng Y., Jiang X., Zhou C., Jin H., Jin K. et al. Wearable sensors and systems for wound healingrelated pH and temperature detection. Micromachines. 2021; 12: 430. DOI: 10.3390/mi12040430
  36. Keller A. A new diagnostic algorithm for early prediction of vascular compromise in 208 microsurgical flaps using tissue oxygen saturation measurements. Ann. Plast. Surg. 2009; 62: 538–43. DOI: 10.1097/SAP.0b 013e3181a47ce8
  37. Desmet C.M., Lafosse A., Vériter S., Porporato P.E., Sonveaux P., Dufrane D. et al. Application of electron paramagnetic resonance (EPR) oximetry to monitor oxygen in wounds in diabetic models. PLoS. ONE. 2015; 10: e0144914. DOI: 10.1371/journal.pone.0144914
  38. Sonmezoglu S., Fineman J.R., Maltepe E., Maharbiz M.M. Monitoring deep-tissue oxygenation with a millimeter-scale ultrasonic implant. Nat. Biotechnol. 2021; 39: 855–64. DOI: 10.1038/s41587-021-00866-y
  39. Wada H., Vargas C.R., Angelo J., Faulkner-Jones B., Paul M.A., Ho O.A. et al. Accurate prediction of tissue viability at postoperative day 7 using only two intraoperative subsecond near-infrared fluorescence images. Plast. Reconstr. Surg. 2017; 139: 354–63. DOI: 10.1097/PRS.0000000000003009
  40. Abe Y., Hashimoto I., Goishi K., Kashiwagi K., Yamano M., Nakanishi H. Transcutaneous pCO2 measurement at low temperature for reliable and continuous free flap monitoring. Plastic Reconstr. Surg. Global Open. 2013; 1: 1–8. DOI: 10.1097/GOX.0b013e3182936cd0
  41. Ashitate Y., Lee B.T., Laurence R.G., Lunsford E., Hutteman M., Oketokoun R. et al. Intraoperative prediction of postoperative flap outcome using the near-infrared fluorophore methylene blue. Ann. Plast. Surg. 2013; 70: 360–5. DOI: 10.1097/SAP.0b013e318236babe
  42. Yoshinobu T., Schöning M.J. Light-addressable potentiometric sensors for cell monitoring and biosensing. Curr. Opinion. Electrochem. 2021; 28: 100727. DOI: 10.1016/j.coelec.2021.100727
  43. Poghossian A., Schöning M.J. Recent progress in silicon-based biologically sensitive field-effect devices. Curr. Opinion. Electrochem. 2021; 29: 1008–11. DOI: 10.1016/j.coelec.2021.100811
  44. Özsoylu D., Isık T., Demir M.M., Schöning M.J., Wagner T. Cryopreservation of a cell-based biosensor chip modified with elastic polymer fibers enabling ready-to-use on-site applications. Biosens. Bioelectr. 2021; 177: 112983. DOI: 10.1016/j.bios.2021.112983
  45. Naresh V., Lee N. A review on biosensors and recent development of nanostructured materials-enabled biosensors. Sensors. 2021; 21 (4): 1109. DOI: 10.3390/s21041109
  46. Daulton E., Wicaksono A., Bechar J., Covington J.A., Hardwicke J. The detection of wound infection by ion mobility chemical analysis. Biosensors. 2020; 10: 19. DOI: 10.3390/bios10030019
  47. Saleh K., Strömdahl A.C., Riesbeck K., Schmidtchen A. Inflammation biomarkers and correlation to wound status after full-thickness skin grafting. Front. Med. (Lausanne). 2019; 6: 159. DOI: 10.3389/fmed.2019.00159
  48. Kollar B., Shubin A., Borges T.J., Tasigiorgos S., Win T.S., Lian C.G. et al. Increased levels of circulating MMP3 correlate with severe rejection in face transplantation. Sci. Rep. 2018; 8: 1–12. DOI: 10.1038/s41598-018-33272-7
  49. Lee W., Jeong S.H., Lim Y.W., Lee H., Kang J., Lee H. et al. Conformable microneedle pH sensors via the integration of two different siloxane polymers for mapping peripheral artery disease. Sci. Adv. 2021; 7: 6290. DOI: 10.1126/sciadv.abI6290/
  50. Schneider L.A., Korber A., Grabbe S., Dissemond J., Influence of pH on wound-healing: a new perspective for wound-therapy? Arch. Dermatol. Res. 2007; 298: 413–20.
  51. Gao Y., Nguyen D.T., Yeo T., Lim S.B., Tan W.X., Madden L.E. et al. A flexible multiplexed immunosensor for point-of-care in situ wound monitoring. Sci. Adv. 2021; 7: eabg9614. DOI: 10.1126/sciadv. abg9614
  52. Sagaidachnyi A.A., Fomin A.V., Usanov D.A., Skripal A.V. Thermography-based blood flow imaging in human skin of the hands and feet: a spectral filtering approach. Physiol. Meas. 2017; 38: 272–88. DOI: 10.1088/1361-6579/aa4eaf
  53. Hummelink S., Kruit A.S., van Vlaenderen A.R., Schreinemachers M.J., Steenbergen W., Ulrich D.J. Postoperative monitoring of free flaps using a low-cost thermal camera: a pilot study. Eur. J. Plast. Surg. 2020; 43: 589–96. DOI: 10.1007/s00238-020-01642-y
  54. Marland J.R., Gray M.E., Dunare C., Blair E.O., Tsiamis A., Sullivan P. et al. Real-time measurement of tumour hypoxia using an implantable microfabricated oxygen sensor. Sensing Bio-sensing Res. 2020; 30: 100375. DOI: 10.1016/j. sbsr.2020.100375
  55. Lim C., Hong Y.J., Jung J., Shin Y., Sunwoo S.H., Baik S. et al. Tissue-like skin-device interface for wearable bioelectronics by using ultrasoft, mass-permeable, and low-impedance hydrogels. Sci. Adv. 2021; 7: eabd3716. DOI: 10.1126/sciadv. abd3716
  56. Deegan A.J., Lu J., Sharma R., Mandell S.P., Wang R.K. Imaging human skin autograft integration with optical coherence tomography. Quant. Imaging. Med. Surg. 2021; 11: 784–96. DOI: 10.21037/qims-20-750
  57. Nakano T., Kudo T., Sano Y., Minehara H., Suzuki M., Aoki K., Matsushita T. Transcutaneous CO2 pressure monitoring increases salvage rates after free tissue transplantation for extremity reconstruction. Plastic Reconstr. Surg. Global Open. 2022; 10: e4467. DOI: 10.1097/GOX. 0000000000004467
****
  1. Sun B.K., Siprashvili Z., Khavari P.A. Advances in skin grafting and treatment of cutaneous wounds. Science. 2014; 346: 941–5. DOI: 10.1126/science.1253836
  2. Tomioka Y., Sekino M., Gu J., Kurita M., Yamashita S., Miyamoto S. et al. Wearable, wireless, multi-sensor device for monitoring tissue circulation after freetissue transplantation: a multicentre clinical trial. Sci. Rep. 2022; 12: 16532. DOI: 10.1038/s41598-022- 21007-8
  3. Fawzy A., Putranti I.O. Perioperative management of the facial wounds with insight of scar prevention. Int. J. Med. Sci. Clin. Res. Studies. 2022; 2 (10): 1028–37. DOI: 10.47191/ijmscrs/v2-i10-01
  4. Malinin A.A., Pryadko S.I., Peskova A.S., Chomaeva A.A. Surgical debridement and simultaneous autologous skin grafting for trophic venous ulcers. Flebologiya. 2022; 16 (2): 130–8 (in Russ.). DOI: 10.17116/flebo 20221602122
  5. Konradi A.O. Biomarkers, types and role in personalized medicine. Russian Journal for Personalized Medicine. 2022; 2 (3): 6–16 (in Russ.). DOI: 10.18705/2782- 3806-2022-2-3-6-16
  6. Zai W., Yuan Y., Kang L., Xu J., Hu Y., Kang L., Wu J. Oxygen penetration through full-thickness skin by oxygen-releasing sutures for skin graft transplantation. Engineering. 2023; 29: 83–94. DOI: 10.1016/j.eng.2023.05.006
  7. Özsoylu D., Janus K.A., Achtsnicht S., Wagner T., Keusgen M., Schöning M.J. (Bio-) Sensors for skin grafts and skin flaps monitoring. Sensors Actuators Rep. 2023; 100163. DOI: 10.1016/j.snr.2023.100163
  8. Berthelot M., Henry F.P., Hunter J., Leff D., Wood S., Jallali N. et al. Pervasive wearable device for free tissue transfer monitoring based on advanced data analysis: clinical study report. J. Biomed. Opt. 2019; 24 (6): 1–8. DOI: 10.1117/1.JBO.24.6.067001
  9. Lu Di, Li S., Yang Q., Arafa H.M., Xu Y., Yan Y. et al. Implantable, wireless, self-fixing thermal sensors for continuous measurements of microvascular blood flow in flaps and organ grafts, biosensors. Bioelect. 2022; 206: 114145. DOI: 10.1016/j.bios.2022.114145
  10. Li Z., Roussakis E., Koolen P.G.L., Ibrahim A.M.S., Kim K., Rose L.F. et al. Non-invasive transdermal twodimensional mapping of cutaneous oxygenation with a rapid-drying liquid bandage. Biomed. Opt. Express. 2014; 5: 3748. DOI: 10.1364/BOE.5.003748
  11. Guo H., Bai W., Ouyang W., Liu Y., Wu C., Xu Y. et al. Wireless implantable optical probe for continuous monitoring of oxygen saturation in flaps and organ grafts. Nat. Commun. 2022; 133009. DOI: 10.1038/s41467-022-30594-z
  12. Mehrara B.J., Santoro T.D., Arcilla E., Watson J.P., Shaw W.W., Da Lio A.L. Complications after microvascular breast reconstruction: experience with 1195 flaps. Plast. Reconstr. Surg. 2006; 118: 1100–9. DOI: 10.1097/01.prs.0000236898.87398.d6
  13. Chen K.-T., Mardini S., Chuang D.C.-C., Lin C.-H., Cheng M.-H., Lin Y.-T. et al. Timing of presentation of the first signs of vascular compromise dictates the salvage outcome of free flap transfers. Plast. Reconstr. Surg. 2007; 120: 187–95. DOI: 10.1097/01.prs.0000264077.07779.50
  14. Kohlhauser M., Luze H., Nischwitz S.P., Kamolz L.P. Historical evolution of skin grafting – a journey through time. Medicina (B. Aires). 2021; 5: 7348. DOI: 10.3390/medicina57040348
  15. Mofikoya B.O., Ugburo A.O., Belie O.M. Clinical assessment score for monitoring free flaps in the dark skin. Alban. J. Med. Heal. Sci. 2018; 49: 18–22.
  16. Katorkin S.E., Sushkov S.A., Kushnarchuk M.Yu. Modern standards of surgical treatment of venous trophic ulcers of the lower extremities. Surgery News. 2021; 29 (1): 75–89 (in Russ.). DOI: 10.18484/2305-0047.2021.1.75
  17. Oda T., Kato H., Nakamura M., Morita A. Analysis of biomonitoring data after full-thickness skin grafting. J. Dermatol. 2021; 48: 1035–43. DOI: 10.1111/1346- 8138.15873
  18. Nsaful K.O., Paintsil A.B., Dakubo J.C.B., Nsaful J., Appiah-Labi K., Nartey E. Evaluation of bacterial infection of split-thickness skin grafts at the Korle Bu teaching hospital. Bali Med. J. 2020; 9: 259–65. DOI: 10.15562/bmj.v9i1.1760
  19. Khan A.Z., Utheim T.P., Byholt M., Fiabema T., Sylvester-Jensen H.C., Tønseth K.A. Skin grafting. Tidsskrift. Den. Norske, Legeforening. 2022; 142: 1–7. DOI: 10.4045/tidsskr.21.0671
  20. Lee J.-H., You H.-J., Lee T.-Y., Kang H.J. Current status of experimental animal skin flap models: Ischemic preconditioning and molecular factors. Int. J. Mol. Sci. 2022; 23 (9): 5234. DOI: 10.3390/ijms23095234
  21. Ogawa A., Nakagawa T., Oda G., Hosoya T., Hayashi K., Yoshino M. et al. Study of the protocol used to evaluate skin-flap perfusion in mastectomy based on the characteristics of indocyanine green. Photodiagn. Photodyn. Ther. 2021; 35: 102401. DOI: 10.1016/j.pdpdt.2021.102401
  22. Marks H., Bucknor A., Roussakis E., Nowell N., Kamali P., Cascales J.P. et al. A paintable phosphorescent bandage for postoperative tissue oxygen assessment in DIEP flap reconstruction. Sci. Adv. 2020; 6 (51): eabd1061.
  23. Gu J., Tomioka Y., Kida K., Xiao Y., Saito I., Okazaki M. et al. Measurement of optical reflection and temperature changes after blood occlusion using a wearable device. Sci. Rep. 2020; 10: 11491. DOI: 10.1038/s41598-020-68152-6
  24. Bian H.Z., Pek C.H., Hwee J. Current evidence on the use of near-infrared spectroscopy for postoperative free flap monitoring: a systematic review. Chinese. J. Plastic Reconstruc. Surg. 2022; 4: 194–202. DOI: 10.1016/j.cjprs.2022.08.008
  25. Bui D.T., Cordeiro P.G., Hu Q.-Y., Disa J.J., Pusic A., Mehrara B.J. Free flap reexploration: indications, treatment, and outcomes in 1193 free flaps. Plast. Reconstr. Surg. 2007; 119: 2092–100. DOI: 10.1097/01.prs.0000260598.24376.e1
  26. Halani S.H., Hembd A.S., Li X., Kirby B., Beard C.C., Haddock N.T., Suszynski T.M. Flap monitoring using transcutaneous oxygen or carbon dioxide measurements. J. Hand. Microsurg. 2022; 14: 10–8. DOI: 10.1055/s0040-1718862
  27. Copelli C., Tewfik K., Cassano L., Pederneschi N., Catanzaro S., Manfuso A., Cocchi R. Gestione del fallimento dei lembi liberi in chirurgia Testa-Collo. Acta Otorhinolaryngol. Italica. 2017; 37: 387–92. DOI: 10.14639/0392-100X-1376
  28. Smith M.K., Mooney D.J. Hypoxia leads to necrotic hepatocyte death. J. Biomed. Mater. Res A. 2007; 80 (3): 520–9. 29. Song Y., Mukasa D., Zhang H., Gao W. Self-powered wearable biosensors. Accounts Mater. Res. 2021; 2: 184–97. DOI: 10.1021/accountsmr.1c00002
  29. Özsoylu D., Wagner T., Schoning M.J. Electrochemical cell-based biosensors for biomedical applications. Curr. Top. Med. Chem. 2022; 22: 22713–733. DOI: 10.2174/1568026622666220304213617 31. Gil Rosa B., Akingbade O.E., Guo X., Gonzalez-Macia L., Crone M.A., Cameron L.P. et al. Multiplexed immunosensors for point-of-care diagnostic applications. Biosens. Bioelectron. 2022; 203: 114050. DOI: 10.1016/j.bios.2022.114050
  30. Morales-Narváez E., Dincer C. (Eds.) Wearable physical, chemical and biological sensors. Elsevier; 2022.
  31. Rodrigues D., Barbosa A.I., Rebelo R., Kwon I.K., Reis R.L., Correlo V.M. Skin-integrated wearable systems and implantable biosensors: a comprehensive review. Biosensors. 2020; 10: 79. DOI: 10.3390/bios10070079
  32. Ates H.C., Nguyen P.Q., Gonzalez-Macia L., MoralesNarváez E., Güder F., Collins J.J., Dincer C. End-toend design of wearable sensors. Nat. Rev. Mater. 2022; 7: 887–907. DOI: 10.1038/s41578-022-00460-x 35.
  33. Cheng S., Gu Z., Zhou L., Hao M., An H., Song K. et al. Recent progress in intelligent wearable sensors for health monitoring and wound healing based on biofluids. Front. Bioeng. Biotechnol. 2021; 9: 1–21. DOI: 10.3389/fbioe.2021.765987
  34. Tang N., Zheng Y., Jiang X., Zhou C., Jin H., Jin K. et al. Wearable sensors and systems for wound healingrelated pH and temperature detection. Micromachines. 2021; 12: 430. DOI: 10.3390/mi12040430
  35. Keller A. A new diagnostic algorithm for early prediction of vascular compromise in 208 microsurgical flaps using tissue oxygen saturation measurements. Ann. Plast. Surg. 2009; 62: 538–43. DOI: 10.1097/SAP.0b 013e3181a47ce8
  36. Desmet C.M., Lafosse A., Vériter S., Porporato P.E., Sonveaux P., Dufrane D. et al. Application of electron paramagnetic resonance (EPR) oximetry to monitor oxygen in wounds in diabetic models. PLoS. ONE. 2015; 10: e0144914. DOI: 10.1371/journal.pone.0144914
  37. Sonmezoglu S., Fineman J.R., Maltepe E., Maharbiz M.M. Monitoring deep-tissue oxygenation with a millimeter-scale ultrasonic implant. Nat. Biotechnol. 2021; 39: 855–64. DOI: 10.1038/s41587-021-00866-y
  38. Wada H., Vargas C.R., Angelo J., Faulkner-Jones B., Paul M.A., Ho O.A. et al. Accurate prediction of tissue viability at postoperative day 7 using only two intraoperative subsecond near-infrared fluorescence images. Plast. Reconstr. Surg. 2017; 139: 354–63. DOI: 10.1097/PRS.0000000000003009
  39. Abe Y., Hashimoto I., Goishi K., Kashiwagi K., Yamano M., Nakanishi H. Transcutaneous pCO2 measurement at low temperature for reliable and continuous free flap monitoring. Plastic Reconstr. Surg. Global Open. 2013; 1: 1–8. DOI: 10.1097/GOX.0b013e3182936cd0
  40. Ashitate Y., Lee B.T., Laurence R.G., Lunsford E., Hutteman M., Oketokoun R. et al. Intraoperative prediction of postoperative flap outcome using the near-infrared fluorophore methylene blue. Ann. Plast. Surg. 2013; 70: 360–5. DOI: 10.1097/SAP.0b013e318236babe
  41. Yoshinobu T., Schöning M.J. Light-addressable potentiometric sensors for cell monitoring and biosensing. Curr. Opinion. Electrochem. 2021; 28: 100727. DOI: 10.1016/j.coelec.2021.100727
  42. Poghossian A., Schöning M.J. Recent progress in silicon-based biologically sensitive field-effect devices. Curr. Opinion. Electrochem. 2021; 29: 1008–11. DOI: 10.1016/j.coelec.2021.100811
  43. Özsoylu D., Isık T., Demir M.M., Schöning M.J., Wagner T. Cryopreservation of a cell-based biosensor chip modified with elastic polymer fibers enabling ready-to-use on-site applications. Biosens. Bioelectr. 2021; 177: 112983. DOI: 10.1016/j.bios.2021.112983
  44. Naresh V., Lee N. A review on biosensors and recent development of nanostructured materials-enabled biosensors. Sensors. 2021; 21 (4): 1109. DOI: 10.3390/s21041109
  45. Daulton E., Wicaksono A., Bechar J., Covington J.A., Hardwicke J. The detection of wound infection by ion mobility chemical analysis. Biosensors. 2020; 10: 19. DOI: 10.3390/bios10030019
  46. Saleh K., Strömdahl A.C., Riesbeck K., Schmidtchen A. Inflammation biomarkers and correlation to wound status after full-thickness skin grafting. Front. Med. (Lausanne). 2019; 6: 159. DOI: 10.3389/fmed.2019.00159
  47. Kollar B., Shubin A., Borges T.J., Tasigiorgos S., Win T.S., Lian C.G. et al. Increased levels of circulating MMP3 correlate with severe rejection in face transplantation. Sci. Rep. 2018; 8: 1–12. DOI: 10.1038/s41598-018-33272-7
  48. Lee W., Jeong S.H., Lim Y.W., Lee H., Kang J., Lee H. et al. Conformable microneedle pH sensors via the integration of two different siloxane polymers for mapping peripheral artery disease. Sci. Adv. 2021; 7: 6290. DOI: 10.1126/sciadv.abI6290/
  49. Schneider L.A., Korber A., Grabbe S., Dissemond J., Influence of pH on wound-healing: a new perspective for wound-therapy? Arch. Dermatol. Res. 2007; 298: 413–20.
  50. Gao Y., Nguyen D.T., Yeo T., Lim S.B., Tan W.X., Madden L.E. et al. A flexible multiplexed immunosensor for point-of-care in situ wound monitoring. Sci. Adv. 2021; 7: eabg9614. DOI: 10.1126/sciadv. abg9614
  51. Sagaidachnyi A.A., Fomin A.V., Usanov D.A., Skripal A.V. Thermography-based blood flow imaging in human skin of the hands and feet: a spectral filtering approach. Physiol. Meas. 2017; 38: 272–88. DOI: 10.1088/1361-6579/aa4eaf
  52. Hummelink S., Kruit A.S., van Vlaenderen A.R., Schreinemachers M.J., Steenbergen W., Ulrich D.J. Postoperative monitoring of free flaps using a low-cost thermal camera: a pilot study. Eur. J. Plast. Surg. 2020; 43: 589–96. DOI: 10.1007/s00238-020-01642-y
  53. Marland J.R., Gray M.E., Dunare C., Blair E.O., Tsiamis A., Sullivan P. et al. Real-time measurement of tumour hypoxia using an implantable microfabricated oxygen sensor. Sensing Bio-sensing Res. 2020; 30: 100375. DOI: 10.1016/j. sbsr.2020.100375
  54. Lim C., Hong Y.J., Jung J., Shin Y., Sunwoo S.H., Baik S. et al. Tissue-like skin-device interface for wearable bioelectronics by using ultrasoft, mass-permeable, and low-impedance hydrogels. Sci. Adv. 2021; 7: eabd3716. DOI: 10.1126/sciadv. abd3716
  55. Deegan A.J., Lu J., Sharma R., Mandell S.P., Wang R.K. Imaging human skin autograft integration with optical coherence tomography. Quant. Imaging. Med. Surg. 2021; 11: 784–96. DOI: 10.21037/qims-20-750
  56. Nakano T., Kudo T., Sano Y., Minehara H., Suzuki M., Aoki K., Matsushita T. Transcutaneous CO2 pressure monitoring increases salvage rates after free tissue transplantation for extremity reconstruction. Plastic Reconstr. Surg. Global Open. 2022; 10: e4467. DOI: 10.1097/GOX. 0000000000004467

About Authors

  • Arut R. Bagyan, Postgraduate; ORCID
  • Aleksandr A. Malinin, Dr. Med. Sci., Chief Researcher; ORCID

 If you found mistakes, select text and press Alt+A