A novel and alternative treatment method for moderate diabetic foot ulcer: tibial periosteal distraction

Abstract

Objective

Researchers have proposed a novel surgical treatment for moderate diabetic foot ulcer: tibial periosteal distraction (TPD) which could improve affected limb microcirculation. We aimed to describe the method and therapeutic effects of this technique.

Methods

We provided a technical guide to perform TPD surgery for the treatment of moderate diabetic foot ulcer of who had been treated in our department. The demographic information had been collected at the time of their admission. The patients were followed up at 3, 6, and 12 months after the operation with the ulcer area, skin temperature of the medial malleolus, transcutaneous oxygen pressure of the medial malleolus, ankle brachial index, dorsalis pedis artery pulsation, 12 item short form survey quality of life scale score, and visual analogue scale.

Results

A total of 35 patients with type 2 diabetes were included in this study, including 19 males and 16 females, with an average age of 62.49 ± 10.34 years and a maximum age of 87 years. The ulcers of all patients were cured, and the average healing time of ulcers was 8.09 ± 2.28 weeks, with no associated complications. The microcirculation indexes of the affected foot were significantly improved (p < 0.05). Three cases showed new vessels regeneration in the affected limbs according to their computed tomography angiography (CTA) results.

Conclusion

TPD surgery technique is a simple procedure that significantly increases the efficacy and reduces the complications of moderate diabetic foot ulcer patients, which could accelerate the formation of collateral circulation.

Introduction

Diabetic foot was first defined by Okaley in 1956 [1]. In 1972, Catterall further clarified the definition of the diabetic foot, pointing out that the loss of sensation at the end of the limb, due to diabetic neuropathy or the loss of vitality due to local ischaemia combined with infection, is called a diabetic foot [2]. In 1999, the World Health Organization defined diabetic foot as foot infection, ulcer, and/or deep tissue destruction related to distal nerve abnormalities and different degrees of peripheral vascular disease of the lower extremities [3]. A study in 2017 showed that the global prevalence of diabetic foot ulcer (DFU) has reached 6.3% [4]. Approximately 15% of diabetes mellitus (DM) patients will have diabetic foot infection or gangrene at some stage of their lives [5], and amputation caused by diabetic foot has become the main cause of amputation worldwide [1, 6–8].

The treatment of diabetic foot ulcers has become a huge financial burden on the medical system. The global medical cost of diabetes was as high as USD 727 billion, of which China was USD 110 billion [9]. In developed countries, diabetic foot occupies 12–15% of diabetes health resources, while, in developing countries, this is as high as 40% [10].

Due to the high risk of ulcers, the recurrence rate of DFU is high. Jiang et al. [11] reported that the incidence of new ulcers in Chinese diabetic patients within 1 year was 8.1%, and the incidence of recurrent ulcers in healed DFU patients within 1 year was 31.6%. Armstrong et al. found that nearly two-thirds of patients will suffer from relapse ulcers within 3 years [11]. The probability of complete healing of chronic or difficult to heal wounds after 20 weeks of treatment is only about 25–50%, or even lower, especially in cases of venous stasis and DFUs [12]. Active treatment of DFUs will reduce foot infections and reduce tissue damage, thereby reducing the amputation rate of diabetic foot patients, improving the quality of life of patients, and ensuring basic social status [13].

Tibial tubercle transfer (TTT) surgery, developed by Chinese doctors, is based on stress tension proposed by Professor Ilizarov of the former Soviet Union, and has gradually been recognised as an appropriate treatment option by more and more people. This method accelerates the healing of DFU by transferring tibial bone blocks. Imaging evidence shows that microcirculation is enhanced after TTT treatment. However, many patients with DFUs suffer from varying degrees of organ dysfunction, difficult to tolerate surgery, and anaesthesia. On the other hand, TTT also increases the economic burden of patients.

Accordingly, we aimed to determine a simpler procedure—staged distraction of the tibial periosteum—to treat moderate diabetic foot ulcers or adjuvant TTT treatment of moderate diabetic foot ulcers. We describe the surgical procedure in detail and the patient prognosis.

Methods

Patient selection

We included patients with DFUs admitted to two hospitals from June 2021 to June 2022. This study was approved by the Ethics Committee of our hospital. We included patients who were diagnosed with DFUs according to the 2019 IWGDF guidelines, with Texas University grade 2B or 2 C, Wagner grade 3, and a popliteal artery patency rate > 50%. We excluded the following patients: those with mental illness who could not cooperate with treatment; patients with other uncontrollable severe diabetic complications diagnosed by endocrinologists; active Charcot foot; cerebral or myocardial infarction in the past 3 months; a history of heart failure, cancer, or renal failure; those undergoing treatment with corticosteroids, immunosuppressive drugs, and/or chemotherapy; and any deaths by unrelated causes before the end of the follow-up.

General treatments

When treating patients, endocrinologists and vascular surgeons would be invited for consultation to monitor the patient’s blood sugar and evaluate the vascular condition of his limbs, adjust blood glucose fluctuations (target blood glucose control standards: rapid blood glucose before meal < 7 mmol/L, rapid blood glucose 2 h after meal < 11 mmol/L). All exudates from foot ulcers will undergo bacterial culture and drug susceptibility testing which results would be the basis for sensitive antibiotics selection for intravenous application.

Anaesthesia

The administered anaesthetic included a mixture of 1% lidocaine hydrochloride injection 10 mL + ropivacaine hydrochloride 10 mL + 0.9% sodium chloride solution 10 ml. A sterile towel with a hole was disinfected and placed over the medial proximal tibial area. Then, the needle was inserted vertically at the midpoint of the tibial crest and the posterior margin of the tibia on the tibial tubercle. The drug was then administered layer-by-layer until reaching the bone surface, so that the anaesthetic fully infiltrated the surrounding periosteum.

TPD surgery

The patient was placed in a supine position. The skin was cut approximately 1 cm along the long axis of the tibia at the midpoint of the medial tibia, tibial crest, and posterior margin of the tibia, 3 cm from the tibial plateau. The periosteum was exposed after soft tissue was peeled off, and approximately 1 cm was cut perpendicular to the long axis of the periosteum. The periosteal strip was bluntly peeled to the distal and proximal ends.

The locking distraction plate was inserted into the distal and proximal periosteum. The hollow locking screw was inserted into the locking hole of the plate, and a Kirschner wire was inserted into the cannulated screw to fix the locking plate and screw. A Kirschner wire was inserted in parallel, into the locking plate hole beside the screw to rotate the locking screw. The plate was reset if we detected that it could move vertically with the screw rotated. The periosteum and subcutaneous tissue were sutured layer-by-layer, and finally bandaged with sterile dressing (Fig. 1).

Fig. 1.

Surgical procedure chart. A: The periosteum is cut; B: blunt stripping of the periosteum; C: subperiosteal drilling; D: subperiosteal implantation of the plate; E–H: screws and anti-rotation parallel Kirschner wires placed

Postoperative management

On the first day after the operation, X-rays were taken to observe the position of the plate relative to the tibia, and to determine the tension. We then stretched the plate at a rate of 1 mm per day (0.5 mm in the morning, and 0.5 mm in the evening).

After 10 days of stretching, X-rays were taken again, and we determined if the traction plate was distracted maximally.

We then reversed the traction plate back to the bone surface, twice a day (1.0 mm in the morning and 1.0 mm in the evening). After 15 days of distraction, the distraction plates, screws, and Kirschner wires were removed. Because there was no osteotomy, the patient did not need to wear a brace or limit weight bearing. During the distraction period, attention was paid to nursing the wound at the distractor, to prevent complications such as nail tract infection and periosteal infection, and we kept the nail tract and surrounding skin tissue under close observation.

Follow-up

The patients were followed up at 3, 6, and 12 months after the operation. The follow-up included the ulcer area (if the ulcer had healed, the healing time was recorded), skin temperature of the medial malleolus, transcutaneous oxygen pressure of the medial malleolus, ankle brachial index, dorsalis pedis artery pulsation, 12 item short form survey (SF-12) quality of life scale score, and visual analogue scale (VAS). When the ulcer surface was completely epithelised without drainage and maintained for at least 2 weeks, the ulcer was considered to have been healed.

Statistical analysis

The data was analysed and plotted using PASW Statistics 18 and Graphpad Prism 9 software. The distribution characteristics of continuous variables were tested by Shapiro–Wilk test. The mean level of data obeying normal distribution was expressed by mean and standard deviation, and the median and quartile were used to represent the mean level of data with non-normal distribution. One-way analysis of variance was used to compare the statistical differences between the groups, and the test level was 0.05. A statistical chart was drawn using the median and quartiles of continuous variables.

Results

A total of 35 patients with type 2 diabetes were included in this study, including 19 males and 16 females, with an average age of 62.49 ± 10.34 years and a maximum age of 87 years (Table 1).

Table 1.

Demographics of patients

Charateristics	Value
Age, y	62.49 ± 10.34
Gender, n
male	19 (54.29%)
female	16 (45.71%)
BMI	23.54 ± 3.17
Diabetes course, m	9 ± 3.33
DFU course, m	5 [4,7]
DFU type (Texas), n
2B	13 (37.14%)
2C	22 (62.86%)
Fasting blood sugar, mmol/L	10.91 ± 1.93
HbA1c, mmol/mol	12.91 ± 2.21
Smoking history, n	9 (25.71%)
Drinking history, n	20 (57.14%)
Comorbidities, n
hypertension	35 (100%)
coronary disease	27 (77.14%)
renal insufficiency	12 (34.29%)
cerebral infarction	1 (2.85%)

Y: years; n: numbers; BMI: body mass index; m:months; DFU: diabetic foot ulcer

The ulcers in all patients were cured. The average healing time was 8.09 ± 2.28 weeks. A classical case could be seen in Fig. 2.

Fig. 2.

Classical case. A 62-year old male patient who suffered from TEXAS 2 C diabetic foot ulcer received TPD treatment. A: The ulcer graphs before surgery. B: The ulcer graphs after debridement and TPD surgery. C: The postoperative X-ray graphs of the tibia. D: The appearance graphs of the affected foot at 3 weeks after operation. E: The appearance graphs of the affected foot at 6 weeks after operation

The pain of the affected foot disappeared, and the skin temperature and ABI at the ankle level were significantly improved compared at three months compared to those before the operation (p < 0.001). With increased follow-up time, the foot skin temperature and ABI of the foot approached normal.

At 3 months after the operation, there was no significant difference in TCPO₂ at ankle level compared with that before the operation (p = 0.192); at 6 and 12 months after the operation, there was a significant increase (p < 0.001).

Among the 17 patients who had an absent pulse in the dorsalis pedis artery, pulsation returned in nine, four, and four patients at 3, 6, and 12 months after surgery, respectively. With the extension of follow-up time, the quality of life of patients also gradually improved. (Table 2; Fig. 3).

Table 2.

Outcomes of patients

Items	Pre-op	Post-op 3 m	Post-op 6 m	Post-op 12 m
Ulcer area, cm2	2.6 [2.2,3.5]	0	0	0
Temperature, ℃	35.34 ± 0.15	35.6 [35.5,35.6]	35.7 [35.6,35.8]	35.9 [35.8,35.9]
TCPO2, mmHg	36 [36,38]	37 [36,38]	38 [37,39]	40 [39,40]
ABI	0.45 ± 0.02	0.65 ± 0.02	0.67 ± 0.01	0.69 [0.68,0.70]
Pulsation of foot dorsal artery, n	18 (51.43%)	27 (77.14%)	31 (88.57%)	35 (100%)
SF-12 score	24.23 ± 2.91	38[36,44]	44.06 ± 4.07	46 [44,50]
VAS	5 [5,6]	0	0	0
Complications	-	0	0	0

Op: operation; TCPO₂: Transcutaneous Oxygen Pressure; ABI: ankle-brachial index; SF-12: 12-item short form survey; VAS: visual analogue scale

Fig. 3.

Postoperative follow-up index box plot. At the end of follow-up, the patients ' Temperature, ABI, TCPO₂ and SF-12 scores were significantly higher than those before surgery (p values were < 0.001, < 0.001, < 0.001, < 0.001, respectively). ^*Compared with preoperative, the indicators were statistically different, p < 0.05; ^#statistically significant compared to last follow-up, p < 0.05

Three patients underwent computed tomography angiography (CTA) examination of the lower extremity artery during the postoperative review. The results showed that TPD could increase the collateral circulation of the affected limb (Fig. 4).

Fig. 4.

Comparison of limb blood vessels. A and B are lower extremity angiography results before and 1 year after the operation, respectively. The yellow arrow indicates the new collateral vessels

Discussion

All diabetic foot ulcer patients were cured, with no associated complications. Some CTA scans of the lower limbs of patients showed regeneration of the blood vessels.

Although debridement has proven to be an effective treatment for DFU [14], a variety of debridement methods have been developed, such as surgical, biological, mechanical, autolysis, enzymatic, and others [15]. However, due to the complex pathogenesis of DFU, and that DFU is an end-stage complication of diabetes, only debridement has a limited effect on the healing of DFU [16, 17]. Many adjuvant therapies have, therefore, been proposed, such as negative pressure suction, ultrasound, biological factors, stem cells, tissue engineering, etc.

After debridement of diabetic foot ulcers, negative pressure adjuvant therapy improves wound healing and reduces the risk of amputation, but negative pressure debridement cannot be applied to necrotic eschar wounds, dry gangrene, active bleeding wounds, vascular and nerve exposure, and vascular anastomosis [18]. Some evidence does show that low-frequency ultrasound debridement can improve venous ulcers and diabetic foot ulcers. In related clinical controlled experiments, the bacterial load of diabetic foot ulcers was significantly reduced, and the transcutaneous oxygen pressure was increased, after ultrasound debridement [19].

It has been confirmed that platelet-derived growth factor, vascular endothelial growth factor, transforming growth factor-β (TGF-β), basic fibroblast growth factor (bFGF), epidermal growth factor, insulin-like growth factor, and nerve growth factor can promote wound healing [20]. Kim et al. isolated adipose mesenchymal stem cells from adult stem cells, and used them to treat ischaemic wounds in diabetic nude mice, achieving remarkable experimental results [21]. Due to the lack of definite efficacy comparison reference and unified research methods, the mechanisms and specific efficacy of most adjuvant therapies are still unclear.

Ischaemia is the key factor leading to difficult healing of DFU wounds [22]. Vascular recanalisation surgery has a limited role in improving the long-term prognosis of diabetic foot. With the adoption of active cardiovascular risk management programmes, the current mortality rate has decreased [23]. However, the 1-, 3-, and 5-year overall average survival rates of diabetic foot patients after major amputation were 81%, 69%, and 29%, respectively [24]. Although lower extremity vascular interventional surgery in the early treatment of the distal limb rapidly restores the blood flow, thereby improving the symptoms of limb ischaemia and hypoxia, so that foot ulcers gradually heals; percutaneous transluminal angioplasty and endovascular stent placement are the currently accepted intervention methods for clinicians and patients. However, in patients with lower extremity arterial disease who underwent vascular interventional surgery, the amputation rate within 1 year was 8% [25]. Some studies, where 115 patients with lower extremity arteriosclerosis were followed up for an average of 17 months, found that there was no significant difference in mortality and amputation rate between the interventional treatment group and the conventional treatment group [26].

The follow-up data of this study showed that periosteal distraction could improve the blood supply of the foot, which could not be achieved by simple wound treatment. Foot skin temperature and ABI were significantly improved in DFU patients after TPD. Although there was no difference in TCPO₂ between the first 3 months after surgery and before surgery, the TCPO₂ of the foot increased significantly over time.

The existence of cortical vessels and the periosteal vascular network is the possible anatomical basis for the effective treatment of DFUs. The periosteum contains a variety of micro-vessels and growth factors. When observing the blood supply of the osteogenesis area, it was found that many vascular sinuses were formed around the new bone during fracture healing. These newly formed vascular sinuses were mainly supported by the periosteum. Some bones without neovascularisation are prone to non-union [27]. Choi et al. in a rat tibial traction experiment, found that the periosteum and bone marrow blood vessels were increased, and the amount of blood vessels in the bone marrow was less than the amount of periosteum generated [28].

TPD using periosteal infiltration of local anaesthesia reduces the complications of anaesthesia in patients with diabetes and reduces the surgical anaesthesia requirements, greatly reducing the burden upon important organs in patients with diabetic foot. Intraoperative anaesthesia has an important influence on the overall completion rate of surgery. Diabetic patients are prone to adverse reactions caused by internal environment disorders such as hypoglycaemia, heart rate, electrolyte, and lipid disorders after surgery. Local anaesthesia, relative to general anaesthesia, maintains self-ventilation without losing airway patency. This greatly reduces the risk of ventilation failure [29], is convenient for postoperative pain management [30], facilitates an early return to normal diet [31], reduces the risk of postoperative nausea and vomiting [32], reduces the stress response to surgery [33], improves patient satisfaction; and reduces the incidence of deep vein thrombosis [34]. In China, 20–40% of diabetic patients have diabetic nephropathy. Local anaesthesia can reduce the use of general anaesthesia and the metabolic burden of diabetic patients.

TPD is a new surgery protocol for the treatment of DFUs. The incision is small and can reduce the complications associated with skin incisions to some extent. Furthermore, during the operation, the tibia will be drilled to stimulate the bone marrow and inner and outer periosteum cells, while reducing the pressure in the medullary cavity, to relieve the pain caused by high medullary cavity vasospasm. The traction device required for the final periosteal distraction is only a screw and an ordinary locking plate, which has a small economic burden for patients, and can be used as a supplement to TTT surgery to further enhance the surgical effect and promote ulcer healing.

Limitations

The limitation of this study is that there is a lack of CTA images as direct evidence for the improvement of lower extremity circulation in each patient. On the one hand, DFU is a terminal complication of diabetic patients, and many patients often have different organ injuries. In this study, 34.29% of patients had renal insufficiency and had difficulty tolerating the nephrotoxicity of the contrast drugs, so this examination was not performed on all patients. On the other hand, the skin temperature, PTCO2, and ABI at the ankle level are all indirect indicators of foot blood supply, which can explain the recovery of foot blood supply after the operation. As an invasive treatment, TPD has the potential to cause osteomyelitis and wound complications. In order to reduce the possibility of wound complications, we chose the proximal tibia with abundant arterial communicating branches as the surgical site, and only a 1 cm wound was cut. This technique chose the part which could provide a relatively sufficient supply of nutrients to the wound and minimized the damage to the soft tissue. This risk of osteomyelitis could be avoided to the greatest extent through standardized aseptic operation and dressing change. In this study, the incidence of the complications of TPD was 0. The osteomyelitis and wound complications are indeed the possible risks of this method, so an experienced orthopedic surgeon was needed as the main surgeon.

Conclusions

In this technical report we provide a step-by-step visual guide on how to perform TPD surgery, which is a new technique for moderate DFUs. The use of a purposefully designed periosteal spatula, screw, and plate are the key factors for a reproducible and successful TPD surgery. Of course, the current protocol is still subject to further refinement and improvement, with continuous endeavour and enthusiasm from colleagues in the field, to promote TPD surgery for the benefit of diabetic and other patients worldwide.

The TPD technique can quickly and effectively promote wound healing for patients with a Texas 2B/2 C DFU. Compared with the bone distraction technique, it has the characteristics of less trauma, a shorter operation time, faster recovery, and less economic burden. It is a treatment worthy of promotion.

Author contributions

HLX and YC designed, supervised this study, and were involved in the enrollment and randomization of all participants. YSY and XFD participated in the study design and wrote this manuscript. YSY and HL participated in the exercise instruction, follow-up and outcomes measurements. All authors were involved in the data collection, statistics analysis.NA and DA were involved in the revision of this manuscript. All authors read and approved the final manuscript.

Funding

This study was supported by Elite Medical Professionals Project of China-Japan Friendship Hospital, No. ZRJY2023-QM29; Capital`s Funds for Health Improvement and Research, No. 2020-2-4086; Beijing Health Science and Technology Achievements and Appropriate Technology Promotion Project, No. BHTPP2022015; National Key R&D Program of China, No. 2022YFC2504302; Beijing Natural Science Foundation, No. L234015.

Data availability

No datasets were generated or analysed during the current study.

Declarations

Ethical approval

This study was approved by the Beijing Longfu Hospital Ethic Committee (resolution no. LFYYLL-2021-26).

Competing interests

The authors declare no competing interests.