Pathological study on correlation of pain duration and cartilage degeneration degree in femoral head necrosis

doi:10.3877/ cma.j.issn.1674-134X.2025.01.010

Abstract

Abstract:

Objective

To investigate the relationship between differences in pain duration and pathological mechanisms of cartilage degeneration in osteonecrosis of femoral head (ONFH).

Methods

The femoral head specimens were collected from patients who underwent total hip arthroplasty at the First Affiliated Hospital of Guangzhou University of Chinese Medicine between January 2020 and June 2023.The patients who could provided informed consent and met the diagnostic criteria for ONFH, with hip dysplasia complicated by osteoarthritis or femoral neck fractures were enrolled; those with a history of previous hip surgery were excluded.A total of 39 patients (40 hips) were included and categorized into four groups: the short-term pain group(14 hips with ONFH of Association Research Circulation Osseous stage (ARCO) Ⅲ and pain duration≤ six months),the long-term pain group(15 hips with ONFH of ARCO stage Ⅲ and pain duration > six months), the OA group(six hips with hip dysplasia complicated by osteoarthritis) and the normal group(five hips with femoral neck fractures).Gross specimen observations and safranin O-fast green staining were performed.Western blot was used to detect the expression of matrix metalloproteinase 9 (MMP9), hypoxia-inducible factor-1α (HIF-1α), superoxide dismutase 1 (SOD1) and type Ⅱ collagen (Col2).Pairwised comparisons of cartilage stateand modified Mankin scores among the four groups were performed using independent samples t test or Mann-Whitney U test, and the significance level was adjusted for multiple comparisons using the Bonferroni method(adjusted P<0.0083).

Results

Gross observation: the hip OA group predominantly exhibited cartilage wear and integrity destruction, the cartilage damage score was (13.50±0.56).ONFH cartilage showed structural integrity with characteristic surface wrinkles and indentations; cartilage damage scores of the short-term pain and long-term pain groups were (4.07±0.92) and (8.53±0.77), the difference was statistically significant(U=28.00, P<0.001).As pain duration increased, ONFH cartilage exhibited dull color, reduced elasticity,and thinning.Histopathology: the hip OA group showed progressive cartilage matrix degradation and cell death from the superficial to the calcified cartilage layer, with significant cartilage wear and vertical fissures reaching deep cartilage；the Mankin score was (10.94±0.76).The ONFH group presented intact cartilage structure,with longer pain durations correlated with more pronounced matrix degradation and apoptotic-like changes such as pyknotic nuclei and reduced cell numbers.These changes were more severe in the deep radial layer and progressively worsened from the calcified to the superficial layer.Superficial cartilage wear and small fissures were observed in the ONFH group; Mankin scores oftheshort-term pain and long-term pain groups were (2.16±0.43) and (5.28±0.55), the difference was statistically significant (t=-4.489, P<0.001).Western blot: compared to the short-term pain group, the long-term pain group showed reduced expression of HIF-1α, SOD1 and Col2 in the femoral head cartilage, indicating the disruption of the hypoxic environment and exacerbated cartilage degradation.The decreased Col2 protein expression and increased MMP9 levels mirrored the pathological manifestations of chondrocyte death and cartilage matrix degradation.

Conclusions

Unlike the cartilage degeneration seen in OA, ONFH cartilage degeneration progresses from the subchondral layer to the superficial layer.The duration of pain can indirectly reflect the cartilage condition in ONFH, with its degeneration mechanism linked to the disruption of the hypoxic environment in the cartilage layer.

Key words: Femur head necrosis, Pain, Cartilage

Zhangzheng Wang, Liang Mo, Wei He, Chi Zhou, Zhenqiu Chen, Bin Fang, Yuhao Liu. Pathological study on correlation of pain duration and cartilage degeneration degree in femoral head necrosis[J]. Chinese Journal of Joint Surgery(Electronic Edition), 2025, 19(01): 65-75.

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URL: https://zhgjwkzz.cma-cmc.com.cn/EN/10.3877/ cma.j.issn.1674-134X.2025.01.010

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Figures/Tables 10

Table 1 Clinical data

组别Groups	例数/髋Number ofcases / hips	年龄［岁，（ $\overset{ˉ}{x}$ ±s）］Age (year)	性别（例）Gender		塌陷程度［mm，（ $\overset{ˉ}{x}$ ±s）］Collapse degree	ARCO分期（髋）ARCO staging（hip）		疼痛时间［个月，（ $\overset{ˉ}{x}$ ±s）］Pain duration (months)
组别Groups	例数/髋Number ofcases / hips	年龄［岁，（ $\overset{ˉ}{x}$ ±s）］Age (year)	男Male	女Female	塌陷程度［mm，（ $\overset{ˉ}{x}$ ±s）］Collapse degree	Ⅲ_a	Ⅲ_b	疼痛时间［个月，（ $\overset{ˉ}{x}$ ±s）］Pain duration (months)
短期疼痛组Short-term pain group	14 /14	45. 8±13. 9	11	3	1. 0±0. 7	12	2	3. 4±2. 0
长期疼痛组Long-term pain group	14/15	43. 3±10. 1	7	7	1. 0±0. 8	12	3	16. 1±8. 0
OA组OA group	6/6	57. 8±10. 7	1	5
正常组Normal group	5/5	59. 4±6. 0	3	2
统计值Statistical values		H=9. 826	χ ²=6. 725		U=96. 5	-		U=0
P值		0. 02	>0. 05		>0. 05	0. 535^*		＜0. 001

Table 1 Clinical data

组别Groups	例数/髋Number ofcases / hips	年龄［岁，（ $\overset{ˉ}{x}$ ±s）］Age (year)	性别（例）Gender		塌陷程度［mm，（ $\overset{ˉ}{x}$ ±s）］Collapse degree	ARCO分期（髋）ARCO staging（hip）		疼痛时间［个月，（ $\overset{ˉ}{x}$ ±s）］Pain duration (months)
组别Groups	例数/髋Number ofcases / hips	年龄［岁，（ $\overset{ˉ}{x}$ ±s）］Age (year)	男Male	女Female	塌陷程度［mm，（ $\overset{ˉ}{x}$ ±s）］Collapse degree	Ⅲ_a	Ⅲ_b	疼痛时间［个月，（ $\overset{ˉ}{x}$ ±s）］Pain duration (months)
短期疼痛组Short-term pain group	14 /14	45. 8±13. 9	11	3	1. 0±0. 7	12	2	3. 4±2. 0
长期疼痛组Long-term pain group	14/15	43. 3±10. 1	7	7	1. 0±0. 8	12	3	16. 1±8. 0
OA组OA group	6/6	57. 8±10. 7	1	5
正常组Normal group	5/5	59. 4±6. 0	3	2
统计值Statistical values		H=9. 826	χ ²=6. 725		U=96. 5	-		U=0
P值		0. 02	>0. 05		>0. 05	0. 535^*		＜0. 001

Figure 1 Gross specimens and cartilage damage scores of femoral head.A is the image of gross appearance and X-ray images of the femoral head in typical patients from each group; B is bar chart of total cartilage damage scores for gross specimens; C is bar chart of cartilage damage scores in each category for gross specimens

Table 2 Gross observation cartilage damage scores

分组Groups	样本数Number ofsamples	色泽Color	表面Surface	形态Morphology	弹性Elasticity	厚度Thickness	总分Total Score
短期疼痛组Short-term pain group	14	0. 71±0. 22	0. 71±0. 24	1. 07±0. 22	1. 00±0. 21	0. 57±0. 23	4. 07±0. 92
长期疼痛组Long-term pain group	15	2. 00±0. 20	1. 47±0. 22	1. 67±0. 21	2. 00±0. 22	1. 40±0. 19	8. 53±0. 77
OA组OA group	6	2. 67±0. 21	2. 33±0. 21	3. 00	2. 83±0. 17	2. 67±0. 21	13. 50±0. 56
正常组Normal group	5	0. 40±0. 25	0. 40±0. 25	0	0. 20±0. 20	0. 20±0. 20	1. 20±0. 76
短期疼痛组vs 长期疼痛组	U值	30. 50	53. 50	62. 50	42. 50	45. 50	28. 00
Short-term pain group vslong-term pain group	P值	0. 001^*	0. 023	0. 063	0. 005^*	0. 008^*	＜0. 001^*
短期疼痛组vs OA组	U值	3. 00	7. 00	3. 00	4. 00	4. 00	3. 50
short-term pain group vsosteoarthritis group	P值	＜0. 001^*	0. 002^*	＜0. 001^*	0. 001^*	0. 001^*	＜0. 001^*
短期疼痛组vs 正常组	U值	28. 50	29. 50	7. 50	13. 50	26. 50	12. 50
short-term pain group vsosteoarthritis group	P值	0. 559	0. 622	0. 007^*	0. 044	0. 444	0. 034
长期疼痛组vs OA组	统计值	U=23. 00	U=18. 00	U=6. 00	U=20. 00	U=8. 00	t=-5. 191
Long-term pain group vsOA group	P值	0. 095	0. 036	0. 001^*	0. 055	0. 002^*	＜0. 001^*
长期疼痛组 vs 正常组	统计值	U=4. 00	U=11. 50	U=2. 50	U=2. 50	U=8. 50	t=6. 872
Long-term pain group vsnormal group	P值	0. 002^*	0. 019^*	0. 001^*	0. 001^*	0. 008^*	＜0. 001^*
OA组 vs 正常组	统计值	U=0	U=0	U=0	U=0	U=0	t=13. 289
OA group vs normal group	P值	0. 004^*	0. 004^*	0. 004^*	0. 004^*	0. 004^*	0. 004^*

Figure 2 Cross-sectional image of the femoral head in ONFH（osteonecrosis of the femoral head）

Figure 3 Histopathological images and modified Mankin scores of femoral head specimens.A is safranin O-fast green staining images of cartilage in the weight-bearing area of femoral head from each group (×5 and ×10), showing matrix degradation in the deep cartilage layer and apoptosis-like changes in chondrocytes in long-term pain group, and vertical fissures extending to the deep cartilage layer with significant surface degeneration in OA group; B is the bar chart of total modified Mankin scores for cartilage pathology of femoral heads in four groups; C is the bar chart of modified Mankin scores for cartilage pathology in different categories of femoral heads in four groups

Figure 4 Pathological differences in cartilage of the femoral head weight-bearing area.A is comparison of safranin O-fast green staining between short-term and long-term pain groups（×10）, showing marked loss of staining in the deep cartilage layer of the long-term pain group, with subchondral bone vascular proliferation; B is bar chart of homologous chondrocyte counts under 20 magnification vision field of four groups; C is bar chart of deep cartilage loss of staining scores in short-term and long-term pain groups; D is destruction ratio at the osteochondral junction in short-term and long-term pain groups; E is comparison of calcified cartilage layer thickness by safranin O-fast green staining（×10） among short-term pain, long-term pain, and OA groups, showing significant calcified cartilage thickening in OA group, and OA-like calcified layer thickening in the long-term pain group compared to the short-term pain group

Table 3 Results of the modified Mankin scoring system

分组Groups	样本数Number of samples	软骨结构Cartilage structure	番红染色Safranin O staining	细胞形态Cellular morphology	潮线完整性Tidemark integrity	总分Total scores
短期疼痛组Short-term pain group	14	0. 52±0. 22	0. 58±0. 17	0. 62±0. 19	0. 31±0. 10	2. 16±0. 43
长期疼痛组Long-term pain group	15	0. 60±0. 14	1. 88±0. 27	2. 11±0. 25	0. 64±0. 12	5. 28±0. 55
OA组OA group	6	4. 06±0. 43	3. 11±0. 28	2. 78±0. 11	1	10. 94±0. 76
正常组Normal group	5	0. 13±0. 08	0. 20±0. 20	0. 67±0. 67	0. 13±0. 08	0. 53±0. 37
短期疼痛组vs 长期疼痛组	统计值	U=87. 50	U=34. 50	U=24. 00	U=63. 00	t=-4. 489
Short-term pain group vslong-term pain group	P值	0. 451	0. 001^*	＜0. 001^*	0. 070	＜0. 001^*
短期疼痛组vs OA组	统计值	U=1. 00	U=0. 50	U=0	U=6. 00	t=-10. 104
Short-term pain group vs OA group	P值	＜0. 001^*	＜0. 001^*	＜0. 001^*	0. 002^*	＜0. 001^*
短期疼痛组vs 正常组	U值	25. 50	18. 50	18. 00	26. 50	8. 00
Short-term pain group vs normal group	P值	0. 391	0. 130	0. 130	0. 444	0. 010
长期疼痛组vs OA组	统计值	t=-7. 694	t=-3. 184	U=29. 00	U=27. 00	t=-6. 061
Long-term pain group vs OA group	P值	＜0. 001^*	0. 007^*	0. 235	0. 178	＜0. 001^*
长期疼痛组 vs 正常组	U值	15. 00	6. 50	3. 00	16. 00	1. 00
Long-term pain group vs normal group	P值	0. 053	0. 004^*	0. 001^*	0. 066	＜0. 001^*
OA组 vs 正常组	U值	0	0	0	0	0
OA group vs normal group	P值	0. 004^*	0. 004^*	0. 004^*	0. 004^*	0. 004^*

Figure 5 Safranin O-fast green staining of cartilage in ONFH, showing characteristic changes: destruction of the osteochondral junction.

Figure 6 Safranin O-fast green staining of cartilage in ONFH（×1，×10）, showing cartilage folding

Figure 7 Expression of cartilage proteins in ONFH with different pain durations.A is electrophoresis image of various proteins; B is column image of Col 2(type Ⅱ collagen) expression in cartilage of two groups, showing decreased expression in the long-term pain group;C is column image of SOD1 (superoxide dismutase 1) expression in cartilage of two groups, showing decreased expression in the longterm pain group; D is column image of HIF-1α (hypoxia-inducible factor 1α) expression in cartilage of two groups, showing decreased expression in the long-term pain group; E is column image of MMP 9 (matrix metalloproteinase 9) expression in cartilage of two groups,showing increased expression in the long-term pain group

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