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Hyperbaric oxygen therapy facilitates healing of chronic foot ulcers in patients with diabetes.
Open accessAbstract
OBJECTIVE: Chronic diabetic foot ulcers are a source of major concern for both patients and health care systems. The aim of this study was to evaluate the effect of hyperbaric oxygen therapy (HBOT) in the management of chronic diabetic foot ulcers. RESEARCH DESIGN AND METHODS: The Hyperbaric Oxygen Therapy in Diabetics with Chronic Foot Ulcers (HODFU) study was a randomized, single-center, double-blinded, placebo-controlled clinical trial. The outcomes for the group receiving HBOT were compared with those of the group receiving treatment with hyperbaric air. Treatments were given in a multi-place hyperbaric chamber for 85-min daily (session duration 95 min), five days a week for eight weeks (40 treatment sessions). The study was performed in an ambulatory setting. RESULTS: Ninety-four patients with Wagner grade 2, 3, or 4 ulcers, which had been present for >3 months, were studied. In the intention-to-treat analysis, complete healing of the index ulcer was achieved in 37 patients at 1-year of follow-up: 25/48 (52%) in the HBOT group and 12/42 (29%) in the placebo group (P = 0.03). In a sub-analysis of those patients completing >35 HBOT sessions, healing of the index ulcer occurred in 23/38 (61%) in the HBOT group and 10/37 (27%) in the placebo group (P = 0.009). The frequency of adverse events was low. CONCLUSIONS: The HODFU study showed that adjunctive treatment with HBOT facilitates healing of chronic foot ulcers in selected patients with diabetes.
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“Dressing selection Based on wound characteristics, ie, location, inflammation, and amount of exudate Promote a moist environment conducive to tissue growth and epithelial migration.63,64”
From Diabetic Foot Ulcers: A Review (2023) · cites this paper as [63]
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“diabetic foot ulcers, hyperbaric oxygen as an adjunctive therapy resulted in significantly more complete healing of the index ulcer in patients treated with HBOT compared with placebo at 1 year of follow-up (152).”
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“89,91 Overall, the evidence is conflicting, but the studies with lowest risk of bias suggest that there may be some benefit for its use in improving absolute wound healing and reduction in ulcer area.”
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“For HBO therapy, systematic reviews of largely poor quality randomised controlled trials (RCTs) [153], and a more recent well-done RCT [154], suggest a potential role in wound healing but have provided no evidence for a role in treating soft tissue or bone infection.”
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“Of two early RCTs(38,39) with low risk of bias, the larger demonstrated a significantly improved outcome in the intervention group, whose ulcers were more likely to heal within 12 months.(39) Of note, the intervention”
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“Two randomized placebo-controlled trials of HBOT for the treatment of DFUs have been published (11,12).”
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“Some suggest that hyperbaric oxygen decreases rates of lower extremity amputation in patients with diabetic foot ulcers or postsurgical amputation wounds in persons with diabetes, and facilitates ulcer healing [88].”
BackgroundNew insights in diabetic foot infection
Richard, J.-L. (2011) · World Journal of Diabetes · doi:10.4239/wjd.v2.i2.24 · Cited by 155
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“However, a large retrospective cohort trial in 2013 reported lower probabilities of wound healing and increased risk of amputation following HBOT [49].”
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“Some trials suggest that hyperbaric oxygen decreases the rate of lower extremity amputation in patients with diabetic foot ulcers, and might facilitate ulcer healing.(169) However, there are no direct data on the effect of hyperbaric oxygen therapy for infectious aspects of the diabetic foot.”
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BackgroundInfluentialOxygen therapies and their effects on wound healing
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“Since this publication, two additional groups have reported benefits to use of HBO2; one was a double-blinded randomized trial (36, 96).”
Use of Oxygen Therapies in Wound Healing
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A systematic review and meta-analysis of adjunctive therapies in diabetic foot ulcers
Elraiyah, T. A., Τσάπας, Α., Prutsky, G. J., Domecq, J. P., Hasan, R., Firwana, B., Nabhan, M., Prokop, L. J., Hingorani, A., Claus, P. L., et al. (2016) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2015.10.007 · Cited by 100
Peters, E. J. G., Lipsky, B. A., Berendt, A. R., Embil, J. M., Lavery, L. A., Senneville, É., Urbančič‐Rovan, V., Bakker, K., & Jeffcoate, W. J. (2012) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2247 · Cited by 99
“Four single-centre RCTs examining the adjunctive use of G-CSF in DFIs were identified [18–20].”
BackgroundInfluentialWound care: The role of advanced wound healing technologies
Wu, S., Marston, W. A., & Armstrong, D. G. (2010) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2010.06.009 · Cited by 98
Hypoxia in Obesity and Diabetes: Potential Therapeutic Effects of Hyperoxia and Nitrate
Norouzirad, R., González‐Muniesa, P., & Ghasemi, A. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/5350267 · Cited by 97
“Hyperoxia has beneficial effects and can reverse the aforementioned hypoxic status, for example, insulin sensitivity and wound healing [146, 148, 149].”
BackgroundAdjunctive Hyperbaric Oxygen Therapy for Healing of Chronic Diabetic Foot Ulcers
Chen, C., Wu, R., Hsu, M.-C., Hsieh, C., & Chou, M.-C. (2017) · Journal of Wound Ostomy and Continence Nursing · doi:10.1097/won.0000000000000374 · Cited by 96
Zhou, Z., Mei, X., Hu, K., Ma, M., & Zhang, Y. (2023) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.3c00459 · Cited by 90
Critical elements to building an effective wound care center
Kim, P. J., Evans, K. K., Steinberg, J. S., Pollard, M. E., & Attinger, C. E. (2013) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2012.11.112 · Cited by 88
The Diabetic Foot: A Historical Overview and Gaps in Current Treatment
Naves, C. C. L. M. (2014) · Advances in Wound Care · doi:10.1089/wound.2013.0518 · Cited by 87
The Diabetic Foot: The Never-Ending Challenge
Peter-Riesch, B. (2016) · Endocrine development · doi:10.1159/000439409 · Cited by 82
Brouwer, R. J., Lalieu, R. C., Hoencamp, R., van Hulst, R. A., & Ubbink, D. T. (2020) · Journal of Vascular Surgery · doi:10.1016/j.jvs.2019.07.082 · Cited by 82
Zhang, Z., Zhang, W., Xu, Y., & Liu, D. (2021) · Asian Journal of Surgery · doi:10.1016/j.asjsur.2021.07.047 · Cited by 82
Vas, P. R. J., Rayman, G. A., Dhatariya, K., Driver, V. R., Hartemann, A., Löndahl, M., Piaggesi, A., Apelqvist, J., Attinger, C., & Game, F. L. (2020) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3284 · Cited by 87
“double-blind RCT demonstrated significantly improved outcomes in the intervention group, who were more likely to heal within 12 months.(170) Of note, the intervention group included patients”
BackgroundDiabetes: foot ulcers and amputations.
Hunt, D. (2009) · Europe PMC (PubMed Central) · Cited by 80
Topical Wound Oxygen Therapy in the Treatment of Chronic Diabetic Foot Ulcers
Frykberg, R. G. (2021) · Medicina · doi:10.3390/medicina57090917 · Cited by 79
Thom, S. R., Milovanova, T. N., Yang, M., Bhopale, V. M., Sorokina, E. M., Uzun, G., Malay, D. S., Troiano, M. A., Hardy, K. R., Lambert, D. S., et al. (2011) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2010.00660.x · Cited by 79
“Hyperbaric oxygen therapy (HBO2) has been shown to improve wound healing and reduce amputation rates of diabetic patients with lower extremity wounds refractory to standard management (1-3).”
BackgroundMethodThe Evaluation and Treatment of Diabetic Foot Ulcers and Diabetic Foot Infections
Core, M. A. D., Ahn, J., Lewis, R. B., Raspovic, K. M., Lalli, T. A. J., & Wukich, D. K. (2018) · Foot & Ankle Orthopaedics · doi:10.1177/2473011418788864 · Cited by 76
“In comparison, negative-pressure wound therapy has been shown to improve wound healing when compared to advanced moist wound therapy.(7,16,18,31) Current evidence does not support the use of antibiotic therapy in the management of noninfected ulcers (Figures 3 and Figure 5A).”
ResultOmar, M. T. A., Alghadir, A. H., Al-Wahhabi, K. K., & Al-Askar, A. B. (2014) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2014.09.024 · Cited by 75
“However, the results from these studies are inconsistent and reported limited success with no conclusive remark on its effect [7–13].”
BackgroundResultEt, H., Mansouri, J., Murad, M. H., Ws, J., Mb, S., Tettelbach, W. H., & Er, W. (2015) · PubMed · Cited by 74
Leg Ulcers in Sickle Cell Disease: Current Patterns and Practices
Delaney, K., Axelrod, K. C., Buscetta, A. J., Hassell, K. L., Adams-Graves, P. E., Seamon, C. A., Kato, G. J., & Minniti, C. P. (2013) · Hemoglobin · doi:10.3109/03630269.2013.789968 · Cited by 73
“Hyperbaric oxygen facilitates healing in diabetic ulcers, though its use in chronic wounds associated with other pathologies still needs rigorous examination (24,25).”
BackgroundSalama, S. E., El-Deeb, A. E., Elbarbary, A. H., & Elsayed, S. E. (2019) · The International Journal of Lower Extremity Wounds · doi:10.1177/1534734619829939 · Cited by 72
Hyperbaric Oxygen Therapy for Diabetic Foot Wounds
Lipsky, B. A., & Berendt, A. R. (2010) · Diabetes Care · doi:10.2337/dc10-0393 · Cited by 71
“(11) in this issue of Diabetes Care provided the proof that HBOT naysayers are seeking? One new study that addressed this issue by Duzgun et al.”
BackgroundSharma, P. M., Kumar, A., Dey, A. D., Behl, T., & Chadha, S. (2021) · Life Sciences · doi:10.1016/j.lfs.2020.118932 · Cited by 70
Evolving spectrum of diabetic wound: Mechanistic insights and therapeutic targets
Chakraborty, R., Borah, P., Dutta, P. P., & Sen, S. (2022) · World Journal of Diabetes · doi:10.4239/wjd.v13.i9.696 · Cited by 71
The Role of Hydrogen Peroxide and Other Reactive Oxygen Species in Wound Healing
Kanta, J. (2011) · Acta Medica (Hradec Kralove Czech Republic) · doi:10.14712/18059694.2016.28 · Cited by 68
“An improvement in wound healing and reduction in ulcer size in diabetic patients after HBOT was reported (28, 31, 39).”
BackgroundAntibacterial microneedle patch releases oxygen to enhance diabetic wound healing
Sun, M., Zhong, X., Dai, M., Feng, X., Tang, C., Cao, L., & Liu, L. (2024) · Materials Today Bio · doi:10.1016/j.mtbio.2024.100945 · Cited by 70
“…oxygen supply to chronic diabetic wounds include hyperbaric chamber therapy, strategies to accelerate the formation of capillary networks (delivery of pro-angiogenic factors or overexpression of factors by stem cells), and use of hemoglobin-mimicking substances to transport oxygen [9 – 11].”
BackgroundAn Update on the Appropriate Role for Hyperbaric Oxygen: Indications and Evidence
Fife, C. E., Eckert, K. A., & Carter, M. J. (2016) · Plastic & Reconstructive Surgery · doi:10.1097/prs.0000000000002714 · Cited by 67
Löndahl, M., Katzman, P., Hammarlund, C., Nilsson, A., & Landin‐Olsson, M. (2010) · Diabetologia · doi:10.1007/s00125-010-1946-y · Cited by 66
“Patients’ baseline characteristics did not differ between HBOT and placebo [ 6 ].”
BackgroundMethodInfluentialNano-Engineered Biomaterials for Tissue Regeneration: What Has Been Achieved So Far?
McLaughlin, S., Podrebarac, J., Ruel, M., Suuronen, E. J., McNeill, B., & Alarcon, E. I. (2016) · Frontiers in Materials · doi:10.3389/fmats.2016.00027 · Cited by 68
Löndahl, M., Landin‐Olsson, M., & Katzman, P. (2010) · Diabetic Medicine · doi:10.1111/j.1464-5491.2010.03185.x · Cited by 65
Present and new techniques and devices in the treatment of DFU: a critical review of evidence
Gottrup, F., & Apelqvist, J. (2012) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2242 · Cited by 60
“03) improved outcome in the intervention group [32], which were more likely to heal within 12months: 25/48 (52%) versus 12/42 (27%).”
BackgroundHyperbaric oxygen therapy as treatment of diabetic foot ulcers
Löndahl, M. (2012) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2256 · Cited by 60
“Major amputations has been performed in 5% (n=61) of HBOtreated patients and 24% (n=57) of non-HBO-treated patients in the non-RCTs compared with 8% (n=107) and 19% (n=104) in the RCTs [4,5,49,50,56,61].”
BackgroundResultInfluentialYang, J., Jin, X., Liu, W., & Wang, W. (2023) · Advanced Materials · doi:10.1002/adma.202305819 · Cited by 58
Hyperbaric Oxygen Therapy: Solution for Difficult to Heal Acute Wounds? Systematic Review
Eskes, A. M., Ubbink, D. T., Lubbers, M. J., Lucas, C., & Vermeulen, H. (2010) · World Journal of Surgery · doi:10.1007/s00268-010-0923-4 · Cited by 56
“The body of evidence on the usefulness of HBOT is larger for chronic wounds than for acute wounds [6, 8, 21].”
BackgroundEmerging drugs for the treatment of diabetic ulcers
Tecilazich, F., Dinh, T. L., & Veves, A. (2013) · Expert Opinion on Emerging Drugs · doi:10.1517/14728214.2013.802305 · Cited by 56
Metadata
- Authors
- Löndahl, M., Katzman, P., Nilsson, A., & Hammarlund, C.
- Affiliations
- Lund University (SE)
- Department of Internal Medicine, Ängelholm Hospital, Ängelholm, Sweden;
- Helsingborgs lasarett (SE)
- Corresponding author
- Löndahl, Magnus
- ORCID
- Löndahl, Magnus
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2010-05-01
- Volume
- 33
- Issue
- 5
- Pages
- 998-1003
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- PMC
- PMC2858204
- OpenAlex
- W2143723758
- Cited by
- 441
- References
- 28
- Citations by year
- 2026: 22 · 2025: 28 · 2024: 25 · 2023: 20 · 2022: 16 · 2021: 31 · 2020: 33 · 2019: 25 · 2018: 31 · 2017: 26 · 2016: 26 · 2015: 28 · 2014: 22 · 2013: 45 · 2012: 29
- FWCI
- 25.69
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Diabetes Care (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetic Foot Ulcer Assessment and Management
- Health Sciences › Medicine › Surgery › Wound Healing and Treatments
- Health Sciences › Medicine › Dermatology › Skin Diseases and Diabetes
- Keywords
- hyperbaric oxygen therapy, chronic diabetic foot ulcers, wound healing, hyperbaric air, Wagner grade, adjunctive therapy, diabetes mellitus, adverse events
- MeSH terms
- Adult, Aged, Aged, 80 and over, Air, Amputation, Surgical, Chronic Disease, Female, Follow-Up Studies, Humans, Hyperbaric Oxygenation, Male, Middle Aged, Placebos, Wound Healing, Treatment Outcome, Diabetic Foot
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