Advertisement

International Orthopaedics

, Volume 42, Issue 7, pp 1575–1583 | Cite as

Investigating clinical failure of core decompression with autologous bone marrow mononuclear cells grafting for the treatment of non-traumatic osteonecrosis of the femoral head

  • Lihua Liu
  • Fuqiang Gao
  • Wei Sun
  • Yunting Wang
  • Qingyu Zhang
  • Bailiang Wang
  • Liming Cheng
  • Zi-rong Li
Original Paper

Abstract

Objective

This study aimed to analyze the clinical factors related to the failure of autologous bone marrow mononuclear cells grafting (BMMCG) following core decompression (CD) in early stage osteonecrosis of the femoral head (ONFH).

Methods

In total, 148 patients (192 hips) underwent CD with autologous BMMCG for treatment of non-traumatic ONFH. The patients were classified by their ARCO staging and China-Japan Friendship Hospital (CJFH) typing system. All patients were clinically and radiographically followed up every three months during the first year and every six months in the following years. The clinical evaluation was conducted by pre- and post-operative Harris hip scores (HHS), while serial anteroposterior (AP) and frog lateral radiographs were used for post-operative radiographic evaluation.

Results

There were 56 hips as clinical failure cases, and 50 hips (89.29%) of failure cases developed between three and ten months after operation. Based on CJFH classification system, type L2 showed more failure rate with 60.0% (9 of15). The Cox risk model showed that disease type was an independent risk factor for post-operative clinical failure (P = 0.042). Multivariate analysis of the Cox proportional-hazards model showed that type L1 had a hazard ratio (HR) of 0.286 (95% CI 0.100–0.816), type L3 with HR of 0.245 (95% CI 0.079–0.759), respectively.

Conclusion

Disease type is an important risk factor for autologous BMMCG combined with CD, and the degree of lateral pillar necrosis is a significant reference index for prognosis evaluation in early stage of ONFH.

Keywords

Osteonecrosis of the femoral head Bone marrow Prognosis Treatment Risk factor 

Introduction

Osteonecrosis of the femoral head (ONFH) is a debilitating disease primarily affecting younger, active populations. The major challenge for the treatment of early stage ONFH is preserving the joint, and defers or avoids arthroplasty. Previous reports have conformed the value of earlier and appropriate interventions, especially surgical treatments having better results [1, 2, 3]. Many surgical methods, including core decompression (CD), vascularized and non-vascularized bone graft, trans-trochanteric rotational osteotomy, and other procedures, have been proposed for preserving the femoral head with reliable results, though disputable.

There is a trend among researchers making CD as the preferred method for pre-collapse ONFH. The rationale of CD [4] is to reduce intramedullary pressure and improve blood flow, which contribute to revascularization and promote bone tissue reformation at the site of necrosis. Compared with traditional technique, multiple percutaneous drillings and small trephine diameters demonstrated similar result and fewer complications [5]. Hernigou et al. first reported the beneficial results of autologous bone marrow mononuclear cell grafting (BMMCG) [6], with increasing local osteoprogenitor cells, to promote incomplete reconstruction and repair. Several studies [7, 8, 9, 10] have showed improved clinical results; however, there are always unsatisfactory outcomes with unsatisfactory clinical function and progression of necrosis. The failed or progression of ONFH reported to be related to patient age, aetiology, stage, and type of the disease [3, 7, 11, 12, 13] and so on. It is difficult to exactly predict the prognosis: repair or progression, and when will show up.

The purpose of the present study is to examine the results and discuss the clinical risk factors for failure of CD in combination with BMMCG for the treatment of non-traumatic ONFH in our hospital.

Materials and methods

This study was approved by the Ethics Committee of China-Japan Friendship Hospital. All participants were required to sign an informed consent and complete a questionnaire of ONFH, and routinely examined by bilateral hip plain radiograph and magnetic resonance imaging (MRI) to evaluate the size, location, and extent of necrotic lesions, if necessary, investigated by computerized tomography (CT) to detect subchondral fractures and status of bone repair before surgery.

Surgical procedure

Bone marrow was harvested from anterior iliac crests with the patient under general or spinal anesthesia, and generally, unilateral necrotic lesion with ipsilateral iliac crest aspirated, bilateral lesion with both sides. After a trocar (6–8 cm in length and 1.5 mm in inner diameter) punctured into the cancellous bone, bone marrow was aspirated into a 10-mL syringe and collected into an aseptic blood bag (containing anticoagulant, sodium citrate, and glucose). The direction of trocar was changed in a cone-shaped area with every successful aspiration. After 50–60 mL of marrow was collected, the site of trocar was changed for as much as bone marrow, and eventually, a total of 180–200 mL was collected as the target volume. Collected bone marrow was concentrated using an automatic blood cell processor (COBE 2991TM Cell Processor GAMBRO BCT. Inc.) at 2500 rpm for five to ten minutes, and 30–50 mL suspension containing BMMCs was gradually concentrated and prepared for transplantation.

Percutaneous approach with the patient in supine position, guide-wire (1.5-mm diameter) was inserted through lateral cortex of the proximal femur and penetrated into the necrotic lesion under image intensifier. A trephine trocar (3.0-mm diameter) was applied to debridement the necrotic lesion, and multiple drilling (1.5-mm diameter wire) were made to strength the decompression. The suspension was injected into necrotic area through the channel of trephine trocar. No complications were observed during the procedure, and there were only mild peri-operative side effects.

Patients were instructed to partial weight bearing with crutches for six weeks, and avoiding from strenuous activities and excessive exercise during the first year after operation.

Patient demographics

A total of 148 patients (192 hips) with ONFH were treated with this technique between February 2012 and December 2013. In this series, 44 patients (29.7%) received bilateral operation, 104 patients (70.3%) with unilateral, respectively, whereas in the unilateral group, 42 patients received contralateral “lightbulb” surgery [14], 29 patients with contralateral total hip arthroplasty (THA), and 33 patients with unilateral ONFH only.

Among the 148 patients, 117 were male and 31 were female, with mean ages of 38.3 (range, 13 to 65) and 38.1 (range, 21 to 78) years, respectively. According to the causes, the disease was corticosteroid induced in 44 patients, alcohol in 59 patients, and idiopathic in 45 patients, respectively. With the Association Research Circulation Osseous (ARCO) classification system, we classified five hips as stage I, 25 as stage IIA, 73 as stage IIB, 68 as stage IIC, and 21 as stage IIIA. Disease type was classified 27 hips as type M + C, 88 as type L1, 16 as type L2, and 61 as type L3, according to the China-Japan Friendship Hospital (CJFH) classification system. Based on mid-coronal section of a femoral head MRI or CT data, CJFH classification system was classified into three types: M, C, and L, and type L was further classified into three subtypes: L1, the lateral pillar partially occupied, L2, simply the lateral pillar, and L3, the lateral pillar totally occupied.

Efficacy evaluation

The duration of follow-up was every three months during the first year and every six months in the following years after surgery. The Harris hip score (HHS) was recorded pre- and post-operatively to evaluate the clinical efficacy. A total score of < 70 was considered as poor, 70–80 as fair, 80–90 as good, and 90–100 as an excellent result. Serial plain radiographs were used for post-operative radiographic evaluation. MRI and CT scan were not routine modalities of follow-up, if necessary, to investigate bone marrow oedema and progression of collapse for any reason. Radiological assessments included the femoral head morphology, change of sclerotic lines, presence and absence of ossification, the reduction in the size of lesion, and appearance of the crescent, to determine repair effect and progression of lesion. We ascertained the main endpoint by HHS score < 70, or if needed to perform further surgeries.

Statistical analysis

We used the SPSS Statistical Software (SPSS for Windows, version 19.0) to complete all statistical analyses. The means, standard deviations, and frequencies were calculated for general demographic and routine clinical data. The possible risk factors affecting survival, included sex, age, cause, pre-operative HHS, the initial ARCO stage, the involvement, and type of lateral pillar. The Cox proportional-hazards model was used to evaluate various factors for multivariate analysis. P values were calculated, and < 0.05 considered statistically significant.

Results

The mean follow-up period for the 148 patients (192 hips) was 34.99 (range, 3 to 60) months, and the average post-operative HHS was 81.71 (± 12.42) points at the last follow-up. All patients were discharged with wound healing normally. One with bleeding and haematoma at puncture point, there were no significant surgical site complications and no clinical evidence of surgical and non-surgical site infections.

There were 56 hips as clinical and radiological failure cases, and 29 hips in group of bilateral operation, 27 hips in unilateral group, respectively, and in the unilateral group, 11(42), 7(29), and 9(33), respectively. THA or “lightbulb” surgery was required for 49 hips; the remaining seven hips were treated with conservative treatments by the end of follow-up.

The clinical characteristics of the population involved are shown in Table 1. Among the possible risk factors affecting survival, the Cox risk model showed that disease type was an independent risk factor for post-operative failure (P = 0.042). Age was the approximate risk factor with P values as 0.057 (Tables 1 and 2). In the group of ≥ 40 years, three patients ≥ 65 years, ARCO stage and CJFH type as IIB (L3), IIIA (L1), and IIB (L1), all of them were correlated with rapidly progression disease and re-operation within six months after operation. The univariate analysis result showed that sex, age, cause, pre-operative HHS, and the initial ARCO stage were not risk factors for failure of different groups (all P values > 0.05) (Table 1). Table 2 contains a list of survival rate in six months, ten months, and five years after operation, and the mean survival time at the end of follow-up. Overall, 50 hips (89.29%) of failure cases developed into clinical and radiographic failure between three and ten  months after operation.
Table 1

Patient and clinical characteristics

 

No. of patients (%)

χ 2

P

Clinical success

Clinical failure

Sex

  

0.138

0.710

 Male

106 (70.2)

45 (29.8)

  

 Female

30 (73.2)

11 (26.8)

  

Age

  

3.630

0.057

 ≥ 40

62 (64.6)

34 (35.4)

  

 < 40

74 (77.1)

22 (22.9)

  

ARCO stage

  

1.881

0.758

 I

4 (60.0)

2 (40.0)

  

 IIA

16 (64.0)

9 (36.0)

  

 IIB

56 (75.7)

18 (24.3)

  

 IIC

47 (70.1)

20 (29.9)

  

 III

14 (66.7)

7 (33.3)

  

CJFH type

  

8.202

0.042

 C + M

18 (67.7)

9 (33.3)

  

 L1

67 (74.4)

23 (25.6)

  

 L3

45 (75.0)

15 (25.0)

  

 L2

6 (40.0)

9 (60.0)

  

Pre-operative HHS

  

2.947

0.400

 < 70

16 (59.3)

11 (40.7)

  

 70–80

38 (73.1)

14 (26.9)

  

 80–90

48 (76.2)

15 (23.8)

  

 90–100

34 (68.0)

16 (32.0)

  

Cause

  

0.584

0.747

 Corticosteroid

43 (72.9)

16 (27.1)

  

 Alcohol

55 (67.9)

26 (32.1)

  

 Idiopathic

38 (73.1)

14 (26.9)

  

ARCO Association Research Circulation Osseous, CJFH China-Japan Friendship Hospital, HHS Harris hip score

Table 2

Survival rate and mean survival time

Variable

Survival rate (%)

Mean survival time (month)

95% CI

6 months

10 months

5 years

Lower

Upper

Sex

 Male

84.8

75.5

70.2

44.4

40.5

48.2

 Female

80.5

73.2

73.2

45.5

38.2

52.9

Age

 ≥ 40

80.2

68.8

64.6

41.2

36.1

46.3

 < 40

87.5

81.2

77.1

48.0

43.6

52.5

ARCO stage

 I

60.0

60.0

60.0

38.2

14.8

61.6

 IIA

80.0

68.0

64.0

35.6

27.0

44.2

 IIB

89.2

78.4

75.7

47.2

42.1

52.4

 IIC

82.1

74.6

70.1

39.4

34.4

44.4

 III

81.0

76.2

66.7

38.5

29.1

47.9

CJFH type

 C + M

77.8

66.7

67.7

42.0

32.3

51.6

 L1

86.7

77.8

74.4

46.5

41.7

51.3

 L3

86.7

80.0

75.0

42.6

37.5

47.6

 L2

66.7

53.3

40.0

25.5

14.0

37.0

Pre-operative HHS

 < 70

74.1

66.7

59.3

34.9

26.1

43.6

 70–80

86.5

75.0

73.1

45.6

39.2

52.1

 80–90

85.7

79.4

76.2

47.3

41.6

52.9

 90–100

84.0

74.0

68.0

40.2

34.1

46.2

Cause

 Corticosteroid

84.7

78.0

72.9

45.9

40.0

51.9

 Alcohol

84.0

71.6

67.9

43.0

37.6

48.4

 Idiopathic

82.7

76.9

73.1

41.3

35.6

47.0

CI confidence interval, ARCO Association Research Circulation Osseous, CJFH China-Japan Friendship Hospital, HHS Harris hip score

Post-operative multivariate analysis showed that disease type was the sole risk factor, which was consistent with the result of univariate analysis. Compared with type L2, the result revealed that type L1 had a hazard ratio (HR) of 0.286 (95% CI 0.100–0.816), type L3 with HR of 0.245 (95% CI 0.079–0.759), respectively. The degree of lateral pillar necrosis was an important reference index for stratification and evaluation of prognosis in early stage of ONFH. There were no significant differences in the survival rates of patients with other possible risk factors (Table 3).
Table 3

Multivariate cox regression analysis results

Variable

β

SE

Wald

P

HR

95% CI

Lower

Upper

Sex

 Female

    

Reference

  

 Male

0.003

0.389

0.000

0.993

1.003

0.468

2.150

Age

 < 40

    

Reference

  

 ≥ 40

− 0.539

0.288

3.504

0.061

0.583

0.332

1.026

ARCO stage

 I

    

Reference

  

 IIA

− 0.033

0.964

0.001

0.973

0.968

0.146

6.402

 IIB

− 0.512

0.586

0.765

0.382

0.599

0.190

1.889

 IIC

− 0.337

0.488

0.476

0.490

0.714

0.274

1.859

 III

0.117

0.500

0.055

0.815

1.124

0.422

2.995

CJFH type

 L2

    

Reference

  

 C + M

− 0.659

0.590

1.245

0.265

0.518

0.163

1.646

 L1

− 1.254

0.536

5.478

0.019

0.286

0.100

0.816

 L3

− 1.408

0.577

5.945

0.015

0.245

0.079

0.759

Pre-operative HHS

 < 70

    

Reference

  

 70–80

0.053

0.489

0.012

0.914

1.054

0.404

2.751

 80–90

− 0.153

0.397

0.148

0.700

0.858

0.394

1.870

 90–100

− 0.338

0.379

0.795

0.373

0.714

0.340

1.498

Cause

 Idiopathic

    

Reference

  

 Corticosteroid

0.141

0.400

0.124

0.725

1.151

0.526

2.519

 Alcohol

0.175

0.353

0.246

0.620

1.191

0.596

2.379

HR hazard ratio, CI confidence interval, ARCO Association Research Circulation Osseous, CJFH China-Japan Friendship Hospital, HHS Harris hip score

The Kaplan–Meier survivorship curves of different possible risk factor showed that the survival rate of type L2 was lower than that of other type, and the survival rate of the group of ≥ 40 years was close to lower than the group of < 40 years Fig. 1.
Fig. 1

Kaplan–Meier survival curve of different possible risk factors

Discussion

ONFH is an intractable disease; studies have shown spontaneous regression or improvement of the necrotic area with many factors involved in the process. Early diagnosis and intervention [3] prior to collapse of the femoral head are keys to a successful outcome of joint-preserving procedures. The choices of surgical interventions are determined by lesion characteristics, patient factors, and preference of doctors. Therefore, the study focuses on possible risk factors affecting clinical failure rates, and which suggests that BMMCG combined with CD is a safe and effective treatment choice in early stage of ONFH, especially disease type’s significance in evaluation of prognosis.

There should be a trend in minimizing the surgical injury and evaluation of treatment from a long-term view to obtain the greatest advantage. We routinely applied CD with multiple percutaneous drillings and small trephine diameters, and autologous BMMCG grafting [15] for treatment of early stage and periocollapse (Fig. 2) of ONFH. This technique is more feasible with no influence of biomechanical structure and retains the structural basis for cell therapy repair.
Fig. 2

Female, 45 years old, idiopathic, left. ①②preoperation X-ray, ③④ 5-year follow-up of X-ray

Cell therapy is a promising method to directly restore local cell populations for repairing [16]. Some previous studies suggested that outcomes were worse for patients with corticosteroid induced ONFH. The result of this study showed that there were no significant differences between different causes. Although decreased cell activity and proliferation ability of mesenchymal stem cells (MSCs) [17] with corticosteroid induced ONFH, MSCs have a better proliferative ability harvested from ilium than femoral head [18]. The effectivity of grafting is positively correlated with not only the quality, but also the quantity of concentrated or culture-expanded cells. Previous studies [7, 19] showed satisfactory results with decreased volume of necrosis, and improved clinical outcome than CD alone.

In most reports, the clinical symptom, extent of necrotic lesion, and stage are reliable factors for prediction of the prognosis of osteonecrosis. Mont et al. [1] noted that asymptomatic osteonecrosis had a high trend of progression to symptomatic and collapse femoral head, especially medium and large-sized, and laterally located lesions. Maus U et al. [20] reported the results of CD in different ARCO stage. The necrotic lesions, located on the medial side, central lesions, and area of less than 30% showed better results, and stage I as reversible, stage II as irreversible, respectively. In this series, three patients of stage I and IIA belong to type L2 lesion and chosen further surgery in early period of post-operation. Except for influence of necrosis site, 77.7% (115 of 148) patient with bilateral lesion, 71 patient received “lightbulb,” or THA surgery for contralateral hip, they prefer to choose further interventions at the same clinical situation. Though there is no significant difference between different age and sex groups, the amount and proliferation ability of MSCs may be affect with the increase of age in adult, and the elders are more prone to the benefit of further surgery.

The location of necrotic lesions is considered as the determining factor affecting the failure rates of treatment. Based on acetabulum weight-bearing area, the Japanese Investigation Committee (JIC) classification system indicated the important role of location of necrosis. Tomaru Y et al. [3] reported that necrotic progression was observed in 6/10 and 5/10 hips with type C1 and C2, respectively. Type C had a significantly higher rate of femoral head collapse than other types. The review of Lieberman et al. [2] emphasized that the involved amount of the weight-bearing surface determined on the clinical failure rates. When the femoral head necrotic area exceeded the inner weight-bearing area by 30 and 60%, 1/22 cases (4.5%) was as clinical failure, 41/91 cases (45%) as clinical failures, respectively; however, when the necrotic area exceeded the outer edge of the acetabulum, 26/43 cases (60.5%) were clinical failures. This observation demonstrates the importance of type L2 as predictive factor, which is associated with the most progression of osteonecrosis, and there is little interaction with other factor.

Based on the results of larger and long-term clinical observations, CJFH classification system was more precise [21] in reflecting the prognosis ONFH. The finite element analysis verified that the cortical part of lateral pillar was the main biomechanical support of femoral head, and this type classification has advantages in situation as followings. In case of anatomical dysplasia, abnormal alignment, and position, radiographs may not be much help to exactly determine the relationship between acetabulum and femoral head. There are two pathological patterns [21] of necrosis evaluated on MRI with different prognosis: confined in the cancellous bone, remaining intact cortical bone (Fig. 3), different invasions of spongy and cortical bone. The survivorship analysis of Bozic KJ et al. [22] showed that the sclerosis was helpful for preserving of femoral head. From onset to diagnosis, more details, spontaneous regression, or progression will be analyzed on MRI or CT imaging directly. In this study, we classified patients into different stages and types according to ARCO and CJFH classification system. Multivariate and univariate analysis showed that disease type was the sole risk factor. Type L2 showed more failure rate with 9(15). Compared with type L2, type L1 had a HR of 0.286 (95% CI 0.100–0.816), L3 with HR of 0.245 (95% CI 0.079–0.759), respectively. The lateral pillar of femoral head is an important reference index for classification and evaluation of treatment with early stage of ONFH.
Fig. 3

Female, 25 years old, rheumatoid arthritis, corticosteroid induced, bilateral. ①② pre-operation MRI, ③④⑤ preoperation CT, ⑥⑦ 7-year follow-up of MRI

Given the retrospective design of this study, there are several limitations. It is difficult to design appropriate control group, and there are great of variations in clinical status, the underlying disease, the amount of steroid and alcohol, the withdrawal steroid, and so on, which all may contribute to the results of analysis. The influence of age was not reported with agreement among researchers. To evaluate the efficacy of CJFH classification system, more prospective, multicenter, randomized clinical trials and improved classification researches should be undertaken in future investigations.

Conclusions

In summary, CD in combination with BMMCG was a safe and effective treatment for patient with early stage of non-traumatic ONFH, disease type was a significant risk factor for this treatment, and CJFH classification system was an important reference index for classification and evaluation of prognosis.

Notes

Funding information

This study was supported by the National Natural Science Foundation of China (81672236, 81372013), and Beijing Natural Science Foundation (7182146).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The procedures performed in this study involving human participants were approved by the ethics committee of China-Japan Friendship Hospital. (File 1)

Informed consent

Informed consent was obtained from all individual participants included in the study. (File 2)

References

  1. 1.
    Mont MA, Zywiel MG, Marker DR, McGrath MS, Delanois RE (2010) The natural history of untreated asymptomatic osteonecrosis of the femoral head: a systematic literature review. J Bone Joint Surg Am 92(12):2165–2170.  https://doi.org/10.2106/JBJS.I.00575 CrossRefPubMedGoogle Scholar
  2. 2.
    Lieberman JR, Engstrom SM, Meneghini RM, SooHoo NF (2012) Which factors influence preservation of the osteonecrotic femoral head? Clin Orthop Relat Res 470(2):525–534.  https://doi.org/10.1007/s11999-011-2050-4 CrossRefPubMedGoogle Scholar
  3. 3.
    Tomaru Y, Yoshioka T, Sugaya H, Aoto K, Wada H, Akaogi H et al (2017) Hip preserving surgery with concentrated autologous bone marrow aspirate transplantation for the treatment of asymptomatic osteonecrosis of the femoral head: retrospective review of clinical and radiological outcomes at 6 years postoperatively. BMC Musculoskelet Disord 18(1):292.  https://doi.org/10.1186/s12891-017-1652-8 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Ficat P, Arlet J, Vidal R, Ricci A, Fournial JC (1971) Therapeutic results of drill biopsy in primary osteonecrosis of the femoral head (100 cases). Rev Rhum Mal Osteoartic 38(4):269–276PubMedGoogle Scholar
  5. 5.
    Al OA (2013) Multiple drilling compared with standard core decompression for avascular necrosis of the femoral head in sickle cell disease patients. Arch Orthop Trauma Surg 133(5):609–613.  https://doi.org/10.1007/s00402-013-1714-9 CrossRefGoogle Scholar
  6. 6.
    Hernigou P, Beaujean F (2002) Treatment of osteonecrosis with autologous bone marrow grafting. Clin Orthop Relat Res 405:14–23CrossRefGoogle Scholar
  7. 7.
    Hernigou P, Poignard A, Zilber S, Rouard H (2009) Cell therapy of hip osteonecrosis with autologous bone marrow grafting. Indian J Orthop 43(1):40–45.  https://doi.org/10.4103/0019-5413.45322 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Wang BL, Sun W, Shi ZC, Zhang NF, Yue DB, Guo WS et al (2010) Treatment of nontraumatic osteonecrosis of the femoral head with the implantation of core decompression and concentrated autologous bone marrow containing mononuclear cells. Arch Orthop Trauma Surg 130(7):859–865.  https://doi.org/10.1007/s00402-009-0939-0 CrossRefPubMedGoogle Scholar
  9. 9.
    Sen RK, Tripathy SK, Aggarwal S, Marwaha N, Sharma RR, Khandelwal N (2012) Early results of core decompression and autologous bone marrow mononuclear cells instillation in femoral head osteonecrosis: a randomized control study. J Arthroplasty 27(5):679–686.  https://doi.org/10.1016/j.arth.2011.08.008 CrossRefPubMedGoogle Scholar
  10. 10.
    Beckmann J, Schmidt T, Schaumburger J, Rath B, Luring C, Tingart M et al (2013) Infusion, core decompression, or infusion following core decompression in the treatment of bone edema syndrome and early avascular osteonecrosis of the femoral head. Rheumatol Int 33(6):1561–1565.  https://doi.org/10.1007/s00296-012-2597-8 CrossRefPubMedGoogle Scholar
  11. 11.
    Hernigou P, Trousselier M, Roubineau F, Bouthors C, Chevallier N, Rouard H et al (2016) Stem cell therapy for the treatment of hip osteonecrosis: a 30-year review of progress. Clin Orthop Surg 8(1):1–8.  https://doi.org/10.4055/cios.2016.8.1.1 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Houdek MT, Wyles CC, Packard BD, Terzic A, Behfar A, Sierra RJ (2016) Decreased osteogenic activity of mesenchymal stem cells in patients with corticosteroid-induced osteonecrosis of the femoral head. J Arthroplast 31(4):893–898.  https://doi.org/10.1016/j.arth.2015.08.017 CrossRefGoogle Scholar
  13. 13.
    Piuzzi NS, Chahla J, Schrock JB, LaPrade RF, Pascual-Garrido C, Mont MA et al (2017) Evidence for the use of cell-based therapy for the treatment of osteonecrosis of the femoral head: a systematic review of the literature. J Arthroplast 32(5):1698–1708.  https://doi.org/10.1016/j.arth.2016.12.049 CrossRefGoogle Scholar
  14. 14.
    Sun W, Li ZR, Gao FQ, Shi ZC, Wang BL, Guo WS (2014) Porous bioceramic beta-tricalcium phosphate for treatment of osteonecrosis of the femoral head. Zhongguo Zuzhi Gongcheng Yanjiu 16:2474–2479.  https://doi.org/10.3969/j.issn.2095-4344.2014.16.003 CrossRefGoogle Scholar
  15. 15.
    Hernigou P, Flouzat-Lachaniette CH, Delambre J, Poignard A, Allain J, Chevallier N et al (2015) Osteonecrosis repair with bone marrow cell therapies: state of the clinical art. Bone 70:102–109.  https://doi.org/10.1016/j.bone.2014.04.034 CrossRefPubMedGoogle Scholar
  16. 16.
    Piuzzi NS, Chahla J, Jiandong H, Chughtai M, LaPrade RF, Mont MA et al (2017) Analysis of cell therapies used in clinical trials for the treatment of osteonecrosis of the femoral head: a systematic review of the literature. J Arthroplast.  https://doi.org/10.1016/j.arth.2017.02.075
  17. 17.
    Hernigou P, Beaujean F, Lambotte JC (1999) Decrease in the mesenchymal stem-cell pool in the proximal femur in corticosteroid-induced osteonecrosis. J Bone Joint Surg Br 81(2):349–355CrossRefPubMedGoogle Scholar
  18. 18.
    Wang BL, Li TJ, Yue DB, Sun W (2014) Proliferation ability of bone marrow mesenchymal stem cells in corticosteroid-induced osteonecrosis of femoral head. Zhongguo Zuzhi Gongcheng Yanjiu 1:7–13.  https://doi.org/10.3969/j.issn.2095-4344.2014.01.002 CrossRefGoogle Scholar
  19. 19.
    Gangji V, De Maertelaer V, Hauzeur JP (2011) Autologous bone marrow cell implantation in the treatment of non-traumatic osteonecrosis of the femoral head: five year follow-up of a prospective controlled study. Bone 49(5):1005–1009.  https://doi.org/10.1016/j.bone.2011.07.032 CrossRefPubMedGoogle Scholar
  20. 20.
    Maus U, Roth A, Tingart M, Rader C, Jager M, Noth U et al (2015) S3 guideline. Part 3: non-traumatic avascular necrosis in adults—surgical treatment of atraumatic avascular femoral head necrosis in adults. Z Orthop Unfall 153(5):498–507.  https://doi.org/10.1055/s-0035-1545902 CrossRefPubMedGoogle Scholar
  21. 21.
    Sun W, Li ZR, Wang BL, Liu BL, Zhang QD, Guo WS (2014) Relationship between preservation of the lateral pillar and collapse of the femoral head in patients with osteonecrosis. Orthopedics 37(1):e24–e28CrossRefPubMedGoogle Scholar
  22. 22.
    Bozic KJ, Zurakowski D, Thornhill TS (1999) Survivorship analysis of hips treated with core decompression for nontraumatic osteonecrosis of the femoral head. J Bone Joint Surg Am 81(2):200–209CrossRefPubMedGoogle Scholar

Copyright information

© SICOT aisbl 2018

Authors and Affiliations

  • Lihua Liu
    • 1
  • Fuqiang Gao
    • 2
  • Wei Sun
    • 3
  • Yunting Wang
    • 3
  • Qingyu Zhang
    • 1
  • Bailiang Wang
    • 2
  • Liming Cheng
    • 2
  • Zi-rong Li
    • 2
  1. 1.Graduate School of Peking Union Medical CollegeChina-Japan Friendship institute of Clinical MedicineBeijingChina
  2. 2.Centre for Osteonecrosis and Joint-preserving & Reconstruction, Orthopaedic DepartmentChina-Japan Friendship HospitalBeijingChina
  3. 3.Centre for Osteonecrosis and Joint-preserving & Reconstruction, Orthopaedic Department, China-Japan Friendship HospitalGraduate School of Peking Union Medical CollegeBeijingChina

Personalised recommendations