Abstract
OBJECTIVES:
Many authors recommend posterior cruciate ligament-retaining arthroplasty with the intention to maintain the proprioception properties of this ligament. Preservation of the neuroreceptors and nervous fibers may be essential for retaining the proprioception function of the posterior cruciate ligament. The present study was thus developed to evaluate the presence of neural structures in the posterior cruciate ligament resected during posterior stabilized arthroplasty in osteoarthritis patients. In particular, clinical, radiographic and histological parameters were correlated with the presence or absence of neural structures in the posterior cruciate ligament.
METHODS:
In total, 34 posterior cruciate ligament specimens were stained with hematoxylin-eosin and Gomori trichrome. An immunohistochemical analysis using antibodies against the S100 protein and neurofilaments was also performed. The presence of neural structures was correlated with parameters such as tibiofemoral angulation, histological degeneration of the posterior cruciate ligament, Ahlbäck radiological classification, age, gender and the histologic pattern of the synovial neurovascular bundle around the posterior cruciate ligament.
RESULTS:
In total, 67.5% of the cases presented neural structures in the posterior cruciate ligament. In 65% of the cases, the neurovascular bundle was degenerated. Nervous structures were more commonly detected in varus knees than in valgus knees (77% versus 50%). Additionally, severe histologic degeneration of the posterior cruciate ligament was related to neurovascular bundle degeneration.
CONCLUSIONS:
Severe posterior cruciate ligament degeneration was related to neurovascular bundle compromise. Neural structures were more commonly detected in varus knees. Intrinsic neural structures were detected in the majority of the posterior cruciate ligaments of patients submitted to knee arthroplasty for osteoarthritis.
Posterior Cruciate Ligament; Total Knee Arthroplasty; Osteoarthritis; Neuroreceptors; Immunohistochemical Analysis
INTRODUCTION
Total knee arthroplasty has been demonstrated to be extremely efficient in the
treatment of advanced osteoarthrosis of this joint (11 Jacobs WC, Clement DJ, Wymenga AB. Retention versus removal of
the posterior cruciate ligament in total knee replacement: a systematic
literature review within the Cochrane framework. Acta Orthop. 2005;76(6):757-68,
http://dx.doi.org/10.1080/17453670510045345.
http://dx.doi.org/10.1080/17453670510045...
).
Currently, there are two main arthroplasty techniques, which involve either
preservation or replacement of the posterior cruciate ligament (PCL). Both
techniques have yielded consistent functional results (11 Jacobs WC, Clement DJ, Wymenga AB. Retention versus removal of
the posterior cruciate ligament in total knee replacement: a systematic
literature review within the Cochrane framework. Acta Orthop. 2005;76(6):757-68,
http://dx.doi.org/10.1080/17453670510045345.
http://dx.doi.org/10.1080/17453670510045...
).
The choice of the most suitable implant has generated controversy. Advocates of the use of a prosthesis to preserve the PCL allege that this would ensure an increased range of motion, better stair-climbing performance and enhanced proprioception (22 Barrett DS, Cobb AG, Bentley G. Joint proprioception in normal, osteoarthritic and replaced knees. J Bone Joint Surg Br. 1991;73(1):53-6.,33 Andriacchi TP, Galante JO. Retention of the posterior cruciate in total knee arthroplasty. J Arthroplasty. 1988;3[Suppl]:S13-9.).
An innovative study performed by Kennedy et al. (44 Kennedy JC, Alexander IJ, Hayes KC. Nerve supply of the human
knee and its functional importance. Am J Sports Med.
1982;10(6):329-35,
http://dx.doi.org/10.1177/036354658201000601.
http://dx.doi.org/10.1177/03635465820100...
) in 1982 revealed the presence of nerve fibers and mechanoreceptors in
anterior and posterior cruciate ligaments, menisci and capsular structures,
indicating that these structures may be related to proprioception. These authors
also described a nerve bundle in the synovium surrounding the PCL that is supposedly
continuous with the tibial nerve and that carries nerve impulses.
In subsequent studies, Franchi et al. (55 Franchi A, Zaccherotti G, Aglietti P. Neural system of the human
posterior cruciate ligament in osteoarthritis. J Arthroplasty.
1995;10(5):679-82,
http://dx.doi.org/10.1016/S0883-5403(05)80215-3.
http://dx.doi.org/10.1016/S0883-5403(05)...
) and
Del Valle et al. (66 Del Valle ME, Harwin SF, Maestro A, Murcia A, Vega JA.
Immunohistochemical analysis of mechanoreceptors in the human posterior cruciate
ligament: a demonstration of its proprioceptive role and clinical relevance.
J Arthroplasty. 1998;13(8):916-22,
http://dx.doi.org/10.1016/S0883-5403(98)90199-1.
http://dx.doi.org/10.1016/S0883-5403(98)...
) recognized Ruffini and
Pacini receptors, Golgi endings and nerve fiber terminals in the PCL of
osteoarthritis patients submitted to prosthetic knee replacement.
To achieve adequate biomechanical performance, a knee prosthesis needs PCL
preservation to ensure sufficient conservation of the anatomical and functional
structures (77 Kleinbart FA, Bryk E, Evangelista J, Scott WN, Vigorita VJ.
Histologic comparison of posterior cruciate ligaments from arthritic and
age-matched knee specimens. J Arthroplasty. 1996;11(6):726-31,
http://dx.doi.org/10.1016/S0883-5403(96)80012-X.
http://dx.doi.org/10.1016/S0883-5403(96)...
,88 Nelissen RG, Hogendoorn PC. Retain or sacrifice the posterior
cruciate ligament in total knee arthroplasty? A histopathological
study of the cruciate ligament in osteoarthritic and rheumatoid disease.
J Clin Pathol. 2001;54(5):381-4,
http://dx.doi.org/10.1136/jcp.54.5.381.
http://dx.doi.org/10.1136/jcp.54.5.381...
). Similarly, it is necessary for the nerve endings and neuroreceptors
to remain present and functional to ensure that the proprioceptive properties of the
retained PCL are maintained (55 Franchi A, Zaccherotti G, Aglietti P. Neural system of the human
posterior cruciate ligament in osteoarthritis. J Arthroplasty.
1995;10(5):679-82,
http://dx.doi.org/10.1016/S0883-5403(05)80215-3.
http://dx.doi.org/10.1016/S0883-5403(05)...
).
An analysis of PCL innervation in patients with advanced arthrosis is likely to be
important in clinical practice, as the presence of neuroreceptors remaining in the
ligament would be a sign that this ligament should be preserved for proprioception
purposes (66 Del Valle ME, Harwin SF, Maestro A, Murcia A, Vega JA.
Immunohistochemical analysis of mechanoreceptors in the human posterior cruciate
ligament: a demonstration of its proprioceptive role and clinical relevance.
J Arthroplasty. 1998;13(8):916-22,
http://dx.doi.org/10.1016/S0883-5403(98)90199-1.
http://dx.doi.org/10.1016/S0883-5403(98)...
). Along the same line of
reasoning, if we can establish a subgroup of patients with particular clinical
and/or radiological parameters in whom PCL innervation is seriously impaired, a
posterior-stabilized prosthesis, which would require the ligament to be sacrificed,
could be considered. These data may provide additional evidence that may be used to
determine the most suitable type of implant for a particular patient.
MATERIALS AND METHODS
A cross-sectional study in which 31 patients (34 ligaments) were evaluated was conducted. Of these patients, 22 were female and 9 were male. The patients' age ranged from 53 to 87 years and they were submitted to arthroplasty with PCL replacement at our service between June 2009 and June 2011.
This research complied with the Declaration of Helsinki and was approved by the Ethics Committee of Universidade de São Paulo (USP).
Only cases of primary osteoarthritis were included in this series; patients with rheumatic diseases and patients who underwent osteosynthesis surgery, osteotomy or previous arthrotomy at the knee level and posttraumatic sequelae were excluded.
The patients who participated in this survey signed an informed consent form declaring their awareness of the methodology and objectives of this study.
The PCL was sectioned at its femoral origin during surgery and its tibial bone insertion was maintained. This ligament was removed after tibial sectioning was performed.
The PCL was preserved in 10% formaldehyde and was subsequently placed in a paraffin mold such that the ligament fibers were oriented along the longitudinal axis. The paraffin blocks were then sectioned and stained with hematoxylin-eosin.
For Gomori trichrome staining, the paraffin mold was soaked in this reagent. Gomori trichrome staining is an excellent technique for ligament analysis, as this reagent stains whole or new collagen fibers green, aged collagen fibers red and cell nuclei purplish-blue (hematoxylin) (99 Prophet E, Mills B, Arrington JB, Sobin L. Laboratory methods in histotechnology.Washington: Armed Forces Institute of Pathology; 1994.).
For immunohistochemical analysis, paraffin sections measuring approximately 10 µm were processed in streptavidin-biotin-peroxidase and incubated with anti-S100 protein antibodies. In the axonal neurofilament experiments, the process was similar; however, the processed mold was instead placed in contact with anti-neurofilament antibodies.
The S100 protein is found in the Schwann cells and myelinated fibers present in mechanoreceptors. The anti-neurofilament antibody labels the cytoskeleton (axon).
http://dx.doi.org/10.1016/S0883-5403(96)... ):
- a)
Mild: defined by impairment of fewer than 20% of the collagen fibers based on an examination of 10 fields at 100× magnification. The predominant findings were disorganized collagen bundles in certain areas (fields of the slide) and an increase in slack connective tissue between the bundles.
- b)
Moderate: defined by impairment of at least 20% but less than 50% of the collagen fibers. Based on microscopic examination, the predominant alterations were an inflammatory reaction; hypercellularity; increased vascularization and disorganized, frayed or dense collagen bundles in several places.
- c)
Severe: defined by the involvement of more than 50% of the collagen fibers in the bundles based on the evaluation of 10 fields at 100× magnification. The predominant alterations observed by OM were the presence of cysts, collagen degeneration (fibrinoid/mucoid/myxoid) and intratendon fatty infiltration, with the possibility of total loss of the structure and integrity of the collagen fiber bundles (coalescent fields) (Figure 1).
Gomori trichrome stain (40× magnification). Severe histological degeneration, with loss of collagen fibers and substitution by fibromyxoid tissue (black arrow).
The neural immunomarking of specific corpuscles and of neurofilaments was qualitatively assessed and classified as the presence or absence of marking.
The mechanoreceptors were classified into four types according to the classification established by Freeman and Wyke (1010 Freeman MA, Wyke B. The innervation of the knee joint. An anatomical and histological study in the cat. J Anat. 1967;101(Pt 3):505-32.) (Figure 2):
-
Type I (Ruffini): encapsulated ovoid or globular corpuscles with slow adaptation function.
-
Type II (Pacini): elongated conical corpuscles with fast adaptation function.
-
Type III (Golgi): spindle-shaped corpuscles with fast adaptation function.
-
Type IV: non-corpuscular endings that can be free (pain) or efferent and amyelinic (vasomotricity).
Immunomarking for S100 (200× magnification). Presence of a type II mechanoreceptor (Pacinian corpuscle) in the upper left field (red arrow) and a type IV mechanoreceptor (perivascular terminations) in the center of the image (black arrow).
The Ahlbäck classification was used to classify the radiological pattern of arthrosis into five types (1111 Ahlbäck S. Osteoarthrosis of the knee. A radiographic investigation. Acta Radiol Diagn (Stockh). 1968:Suppl 277:7-72.).
Measurement of the tibiofemoral angulation involved knee radiographs taken with orthostatic support encompassing the distal femoral and proximal tibial diaphysis. A goniometer was used to measure the tibiofemoral angle, which consisted of the intersection of the femoral and tibial anatomical axes. The following angles were considered: varus (less than or equal to 4° of the tibiofemoral valgus), neutral (from 5° to 9° of the valgus) and valgus (above 10°).
The radiological parameters (the Ahlbäck classification and the measurement of the tibiofemoral axis) were evaluated together by two specialist surgeons with more than 10 years of experience in arthroplasty surgery. In case of discordance, a third colleague with the same training assisted in determining the end result.
The patients were divided into two age groups: 70 years and over and under 70 years.
Based on macroscopic analysis at the time of surgery, the anterior cruciate ligament (ACL) was considered either present or absent. No attempt was made to classify the ACL as normal or undergoing macroscopic degeneration, as this would generate a bias in the analysis due to extreme subjectivity.
The neurovascular bundle (NVB) was classified as preserved, degenerated or absent. In the degenerated cases, the following characteristics were observed by microscopy: a thickened tunica intima in the vessels, degeneration in the elastic laminae of the vascular wall and nerve atrophy demonstrated by perineural retraction (Figure 3). In the cases classified as absent, the NVB was not visualized. This absence of visualization can be interpreted in two ways: either the NVB was not included in the histological section, or it was not present. The four absent cases were excluded from the statistical analysis due to these two distinct possibilities.
Gomori trichrome stain (40× magnification). Neurovascular bundle presenting a thickened vascular tunica intima (thin black arrow), duplication of elastic fibers (thick black arrow) and nerve atrophy.
The presence of neural structures in the PCL was evaluated and correlated with the tibiofemoral angulation (varus-valgus), the degree of histological degeneration of the collagen fibers, the macroscopic state of the ACL, Ahlbäck's radiological classification, age, sex and the histological state of the NVB contained in the synovium that surrounds the PCL. The histological pattern of the vascular bundle (preserved or degenerated) was also correlated with previously described parameters.
Statistical analysis
The chi-square test was used for analysis of parametric data and the Kruskal-Wallis test and Mann-Whitney test were used for analysis of non-parametric data. Values of p<0.05 were considered significant. Fisher's exact test was used for analysis of categorical data.
RESULTS
Regarding the grade of histological degeneration, there were 23 severe cases (67.5%), 9 moderate cases (26.5%) and 2 mild cases (6%).
According to Ahlbäck's radiological classification of arthrosis, there were seven grade I (20.5%), five grade II (14.5%), 14 grade III (41%), six grade IV (18%) and two grade V (6%) cases.
There were six cases of genu valgum (17.5%), 2 neutral cases (6%) and 26 cases of genu varum (76.5%).
The ACL was present in 64.7% of cases (22 cases) and absent in 35.3% of cases (12 cases).
The NVB contained in the synovium of the PCL was identified in 30 cases (88.5%), whereas it appeared degenerated in 22 cases (65%) (Figure 3) and preserved in eight cases (23.5%). Additionally, in 4 cases, the NVB could not be identified in the histological sections (11.5%).
Immunomarking for neural structures was positive in 23 of the cases (67.5%). Specific mechanoreceptors were identified in 10 ligaments, with 9 type II cases (Pacini) and six type IV cases predominating. Moreover, neurofilaments were identified in 14 ligaments.
Neural immunomarking was more frequent in the genu varum (77%) than in the genu valgum (50%); this difference was statistically significant, as demonstrated by the chi-square test (p = 0.048) (Table 1).
Correlation between the studied parameters and the immunomarking of the neural structures of the PCL.
Immunomarking positivity was observed even at increasing levels of the Ahlbäck classification (p = 0.277).
A significant correlation was demonstrated between severe histological degeneration of the PCL and degeneration of the NVB (Mann-Whitney test, p = 0.015) (Table 2). Considering the 30 cases in which the NVB was identified, in the event of severe degeneration of the PCL, the NVB was degenerated 85.7% of the time (18/21 cases). In the cases with mild or moderate histological impairment of the PCL, the NVB was degenerated 44% of the time (4/9 cases).
Correlation between the studied parameters and the state of conservation of the PCL's subsynovial NVB.
There was no significant relationship between the immunomarking of the neural structures or the pattern of degeneration of the NVB and the other parameters studied (Tables 1 and 2).
DISCUSSION
The functional integrity of the PCL is essential for the functionality of the knee
prosthesis in which this ligament is preserved. The preservation of this structure,
at least in theory, could benefit proprioception (66 Del Valle ME, Harwin SF, Maestro A, Murcia A, Vega JA.
Immunohistochemical analysis of mechanoreceptors in the human posterior cruciate
ligament: a demonstration of its proprioceptive role and clinical relevance.
J Arthroplasty. 1998;13(8):916-22,
http://dx.doi.org/10.1016/S0883-5403(98)90199-1.
http://dx.doi.org/10.1016/S0883-5403(98)...
).
In 1982, Kennedy et al. (44 Kennedy JC, Alexander IJ, Hayes KC. Nerve supply of the human
knee and its functional importance. Am J Sports Med.
1982;10(6):329-35,
http://dx.doi.org/10.1177/036354658201000601.
http://dx.doi.org/10.1177/03635465820100...
) performed
experiments that were based on a study by Gardiner (1212 Gardner E. The innervation of the knee joint. Anat Rec.
1948;101(1):109-30, http://dx.doi.org/10.1002/ar.1091010111.
http://dx.doi.org/10.1002/ar.1091010111...
) and demonstrated that the tibial nerve is the source of the nerve
fibers that innervate the synovium that surrounds the cruciate ligaments. Using the
silver nitrate impregnation technique, these authors detected the presence of
superficial axons and Golgi receptors in the PCL synovium.
In 1984, Schultz et al. (1313 Schultz RA, Miller DC, Kerr CS, Micheli L. Mechanoreceptors in human cruciate ligaments. A histological study. J Bone Joint Surg Am. 1984;66(7):1072-6.) used a similar technique and also described the presence of several unmyelinated axons in the peripheral fat (synovium) that coats the cruciate ligaments, in addition to significant degeneration of the collagen fibers of these ligaments. In 22 cruciate ligaments, they observed only 1 mechanoreceptor.
Studies conducted by Franchi et al. (55 Franchi A, Zaccherotti G, Aglietti P. Neural system of the human
posterior cruciate ligament in osteoarthritis. J Arthroplasty.
1995;10(5):679-82,
http://dx.doi.org/10.1016/S0883-5403(05)80215-3.
http://dx.doi.org/10.1016/S0883-5403(05)...
) and
Dell Valle et al. (66 Del Valle ME, Harwin SF, Maestro A, Murcia A, Vega JA.
Immunohistochemical analysis of mechanoreceptors in the human posterior cruciate
ligament: a demonstration of its proprioceptive role and clinical relevance.
J Arthroplasty. 1998;13(8):916-22,
http://dx.doi.org/10.1016/S0883-5403(98)90199-1.
http://dx.doi.org/10.1016/S0883-5403(98)...
) revealed that neural
structures and mechanoreceptors were present in the PCL of patients with arthrosis
submitted to knee arthroplasty, even in the presence of degeneration of the
ligament's collagen fibers. In fact, Franchi et al. (55 Franchi A, Zaccherotti G, Aglietti P. Neural system of the human
posterior cruciate ligament in osteoarthritis. J Arthroplasty.
1995;10(5):679-82,
http://dx.doi.org/10.1016/S0883-5403(05)80215-3.
http://dx.doi.org/10.1016/S0883-5403(05)...
) observed a decrease in the number of mechanoreceptors in the
arthritic knee. Both groups of investigators, however, failed to determine either
the histological grade of PCL degeneration or the radiological grade of the
associated arthrosis.
Proprioception is the ability to detect movement and positioning in the space of a particular joint and is performed by neural receptors located within the joint capsule in the ligaments, muscles and skin (1414 Ejnisman B, Faloppa F, Carrera EF, Andreoli CV, Alves MTS, Odashiro A, et al. Estudo imunohistoquímico dos mecanorrecptores do ligamento glenoumeral inferior em cadáveres humanos. Rev Bras Ortop. 2002;37(7):289-98.).
In studies conducted by Barret et al. (22 Barrett DS, Cobb AG, Bentley G. Joint proprioception in normal, osteoarthritic and replaced knees. J Bone Joint Surg Br. 1991;73(1):53-6.) and Skinner (1515 Skinner HB. Pathokinesiology and total joint arthroplasty. Clin Orthop Relat Res. 1993;(288):78-86.), the authors found that proprioception diminishes with age and that proprioception in cases of knee osteoarthritis differs from that in control individuals of the same age. Disorganization of the collagen fibers of the PCL supposedly leads to greater lassitude of this ligament. This process could raise the threshold of response in the nerve fibers and mechanoreceptors located along the axis of the pathologically slackened ligament. Moreover, the function of the afferent neural structures present in the PCL could be impaired, either due to a decrease in their number or due to their degeneration.
Several studies (1515 Skinner HB. Pathokinesiology and total joint arthroplasty. Clin
Orthop Relat Res. 1993;(288):78-86.
16 Lattanzio PJ, Chess DG, Mac Dermid JC. Effect of the posterior
cruciate ligament in knee-joint proprioception in total knee arthroplasty.
J Arthroplasty. 1998;13(5):580-5,
http://dx.doi.org/10.1016/S0883-5403(98)90059-6.
http://dx.doi.org/10.1016/S0883-5403(98)...
-1717 Jacobs WC, Clement DJ, Wymenga AB. Retention versus removal of
the posterior cruciate ligament in total knee replacement: a systematic
literature review within the Cochrane framework. Acta Orthop. 2005;76(6):757-68,
http://dx.doi.org/10.1080/17453670510045345.
http://dx.doi.org/10.1080/17453670510045...
) have not described proprioception differences between
patients who received a PCL replacement prosthesis and those with preservation of
this ligament.
Regarding mechanoreceptors, Pacinian corpuscles predominated in the present study, in
accordance with studies by Franchi et al. (55 Franchi A, Zaccherotti G, Aglietti P. Neural system of the human
posterior cruciate ligament in osteoarthritis. J Arthroplasty.
1995;10(5):679-82,
http://dx.doi.org/10.1016/S0883-5403(05)80215-3.
http://dx.doi.org/10.1016/S0883-5403(05)...
)
and Katonis et al. (1818 Katonis P, Papoutsidakis A, Aligizakis A, Tzanakakis G, Kontakis
GM, Papagelopoulos PJ. Mechanoreceptors of the posterior cruciate ligament.
J Int Med Res. 2008;36(3):387-93.), whereas no Golgi
receptors were found. These results are consistent with the work of Dell Valle et
al. (66 Del Valle ME, Harwin SF, Maestro A, Murcia A, Vega JA.
Immunohistochemical analysis of mechanoreceptors in the human posterior cruciate
ligament: a demonstration of its proprioceptive role and clinical relevance.
J Arthroplasty. 1998;13(8):916-22,
http://dx.doi.org/10.1016/S0883-5403(98)90199-1.
http://dx.doi.org/10.1016/S0883-5403(98)...
), who did not observe this type of
mechanoreceptor in humans.
In our study, in most cases (67.5%), neural structures were present in the PCL, even
in the presence of severe degeneration. These data are in accordance with the work
of Nelissen and Hogendoorn (88 Nelissen RG, Hogendoorn PC. Retain or sacrifice the posterior
cruciate ligament in total knee arthroplasty? A histopathological
study of the cruciate ligament in osteoarthritic and rheumatoid disease.
J Clin Pathol. 2001;54(5):381-4,
http://dx.doi.org/10.1136/jcp.54.5.381.
http://dx.doi.org/10.1136/jcp.54.5.381...
), who examined
a series of 11 knee arthrosis patients and observed eight cases of severe
degeneration of the PCL. In seven of these cases, neural structures were present in
the ligament.
In the current study, mechanoreceptors and neurofilaments were mostly present in the
individuals with advanced grades of arthrosis, as determined using
Ahlbäck's radiological classification (IV and V). In contrast, in the
study by Nelissen and Hogendoorn (88 Nelissen RG, Hogendoorn PC. Retain or sacrifice the posterior
cruciate ligament in total knee arthroplasty? A histopathological
study of the cruciate ligament in osteoarthritic and rheumatoid disease.
J Clin Pathol. 2001;54(5):381-4,
http://dx.doi.org/10.1136/jcp.54.5.381.
http://dx.doi.org/10.1136/jcp.54.5.381...
), in
which only Ahlbäck type IV and V cases were considered, neural structures were
identified in all but one case.
Positive immunomarking was significantly more likely to be observed in cases of genu
varum (77%) than in cases of genu valgum (50%) in the present study. Although
statistical significance could not be determined due to the small size of the study
group, all six cases of genu valgum presented severe histological degeneration of
the PCL. Such findings support the practice of sacrificing the PCL in cases of genu
valgum, which has been reported by certain authors (1919 Sah AP, Scott RD. How to balance the posterior cruciate ligament
in a cruciate retaining total knee arthroplasty. Tech Knee Surg 2010;9(1):43,
http://dx.doi.org/10.1097/BTK.0b013e3181d16672.
http://dx.doi.org/10.1097/BTK.0b013e3181...
). Cases of genu valgum are usually more technically demanding than
those of genu varum (1919 Sah AP, Scott RD. How to balance the posterior cruciate ligament
in a cruciate retaining total knee arthroplasty. Tech Knee Surg 2010;9(1):43,
http://dx.doi.org/10.1097/BTK.0b013e3181d16672.
http://dx.doi.org/10.1097/BTK.0b013e3181...
). In particular,
ligament release is more complex and sacrificing the PCL facilitates better ligament
balance in the knee. Moreover, if the proprioceptive capacity of this ligament is
more severely impaired in cases of valgus, a posterior-stabilized prosthesis in
which the PCL ligament is discarded would be more suitable based on this
hypothesis.
In our study, 30/34 of PCL specimens (88%), it was possible to identify the
subsynovial NVB described previously by Kennedy et al. (44 Kennedy JC, Alexander IJ, Hayes KC. Nerve supply of the human
knee and its functional importance. Am J Sports Med.
1982;10(6):329-35,
http://dx.doi.org/10.1177/036354658201000601.
http://dx.doi.org/10.1177/03635465820100...
) and Schultz et al. (1313 Schultz RA, Miller DC, Kerr CS, Micheli L. Mechanoreceptors in
human cruciate ligaments. A histological study. J Bone Joint Surg Am.
1984;66(7):1072-6.). In 22 cases (64.7%), degeneration of this bundle could be observed
by microscopy. Our data are consistent with those of Stubbs et al. (2020 Stubbs G, Dahlstrom J, Papantoniou P, Cherian M. Correlation
between macroscopic changes of arthrosis and the posterior cruciate ligament
histology in the osteoarthritic knee. ANZ J Surg.
2005;75(12):1036-40.), who examined 50 PCLs from arthrosis
patients submitted to arthroplasty and found arteriosclerosis and perineural
fibrosis in 78% and 50% of the ligaments studied, respectively, after histological
analysis.
Degenerative alterations of the NVB could lead to impaired function and decreased transmission of impulses captured in the knee. This degeneration of the subsynovial NVB should be studied in more depth, as it could be, at least in theory, one of the factors responsible for the proprioception deficit of arthritic patients.
A significant statistical correlation (p = 0.015) was identified between the grade of PCL degeneration and the state of the NVB in the current study. The cases of severe histological degeneration of the PCL were related to degenerated NVBs 80% of the time and to impaired bundles 44% of the time in cases of mild or moderate degeneration. These data are important because if we can identify patients with severe PCL degeneration, aside from altered biomechanical properties, this may be an indicator of deficient proprioception in the ligament. Under this potential set of circumstances, PCL replacement arthroplasty would, in theory, be an indication to consider.
The good results obtained with prostheses with preservation of the PCL, despite advanced degeneration in many cases, could be due to the design of the implants; the ligament plays a secondary role when applying an axial load to the prosthesis (2020 Stubbs G, Dahlstrom J, Papantoniou P, Cherian M. Correlation between macroscopic changes of arthrosis and the posterior cruciate ligament histology in the osteoarthritic knee. ANZ J Surg. 2005;75(12):1036-40.). In addition, after arthroplasty, the collateral ligaments and the capsule are responsible for knee proprioception, which helps to explain the similar results obtained using prostheses with and without sacrifice of the PCL (2020 Stubbs G, Dahlstrom J, Papantoniou P, Cherian M. Correlation between macroscopic changes of arthrosis and the posterior cruciate ligament histology in the osteoarthritic knee. ANZ J Surg. 2005;75(12):1036-40.).
This study has certain limitations. The first is that the immunomarking analysis was
merely qualitative; thus, the density of the ligament innervation was not
quantified. Another weak point is the use of Ahlbäck's radiological
classification, which has limited reproducibility (2121 Galli M, De Santis V, Tafuro L. Reliability of the Ahlbäck
classification of knee osteoarthritis. Osteoarthritis Cartilage.
2003;11(8):580-4,
http://dx.doi.org/10.1016/S1063-4584(03)00095-5.
http://dx.doi.org/10.1016/S1063-4584(03)...
); however, it is the most widely used classification system among
orthopedic surgeons. The method by which the grade of histological PCL degeneration
was evaluated was also subjective, although this method was based on previous
studies (77 Kleinbart FA, Bryk E, Evangelista J, Scott WN, Vigorita VJ.
Histologic comparison of posterior cruciate ligaments from arthritic and
age-matched knee specimens. J Arthroplasty. 1996;11(6):726-31,
http://dx.doi.org/10.1016/S0883-5403(96)80012-X.
http://dx.doi.org/10.1016/S0883-5403(96)...
,2020 Stubbs G, Dahlstrom J, Papantoniou P, Cherian M. Correlation
between macroscopic changes of arthrosis and the posterior cruciate ligament
histology in the osteoarthritic knee. ANZ J Surg.
2005;75(12):1036-40.,2222 Allain J, Goutallier D, Voisin MC. Macroscopic and histological
assessments of the cruciate ligaments in arthrosis of the knee. Acta Orthop
Scand. 2001;72(3):266-9,
http://dx.doi.org/10.1080/00016470152846592.
http://dx.doi.org/10.1080/00016470152846...
) and conducted by a
histologist with extensive experience in scientific studies. One strong point of the
study is that it was performed in patients submitted to surgery in whom neural
structures were identified using one of the most widely accepted current techniques:
immunomarking for S100 and neurofilaments. Furthermore, we demonstrated the
relationship between severe degeneration of the PCL and impairment of the NVB. We
also established that neural structures are more commonly present in cases of varus
deformity than in cases of valgus deformity. These original results pave the way for
the development of new questions. Additionally, the results should inspire surveys
geared toward the identification of epidemiological, clinical and radiological
parameters that may be related to the histological and functional states of the PCL
and its applications in surgical practice.
The topic of articular mechanoreceptors is far from being merely academic, as it has
served as one of the foundations of prestigious authors (11 Jacobs WC, Clement DJ, Wymenga AB. Retention versus removal of
the posterior cruciate ligament in total knee replacement: a systematic
literature review within the Cochrane framework. Acta Orthop. 2005;76(6):757-68,
http://dx.doi.org/10.1080/17453670510045345.
http://dx.doi.org/10.1080/17453670510045...
,66 Del Valle ME, Harwin SF, Maestro A, Murcia A, Vega JA.
Immunohistochemical analysis of mechanoreceptors in the human posterior cruciate
ligament: a demonstration of its proprioceptive role and clinical relevance.
J Arthroplasty. 1998;13(8):916-22,
http://dx.doi.org/10.1016/S0883-5403(98)90199-1.
http://dx.doi.org/10.1016/S0883-5403(98)...
) recommendation of
PCL preservation in knee arthroplasty. Additionally, articular mechanoreceptors have
been the subject of recent surveys on other joints, such as the shoulder (1515 Skinner HB. Pathokinesiology and total joint arthroplasty. Clin
Orthop Relat Res. 1993;(288):78-86.) and intervertebral disc (2323 Oliveira VM, Puertas EB, Alves MTS, Yamashita HK. Estudo
comparativo dos mecanorreceptores dos discos intervertebrais normais e
degenerados da coluna lombar de humanos pela radiografia, ressonância
magnética e estudo anatomopatológico. Acta Ortop Bras.
2007;15(1):35-9,
http://dx.doi.org/10.1590/S1413-78522007000100007.
http://dx.doi.org/10.1590/S1413-78522007...
).
CONCLUSION
1) Intrinsic neural structures were detected in the majority of the PCLs of patients submitted to knee arthroplasty for osteoarthritis, even in the presence of severe structural degeneration of the ligament's collagen fibers. 2) There was an association between severe PCL degeneration and NVB compromise. 3) Neural structures were more frequently observed in varus knees than in valgus knees.
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» http://dx.doi.org/10.1590/S1413-78522007000100007
-
No potential conflict of interest was reported.
Publication Dates
-
Publication in this collection
Feb 2015
History
-
Received
12 Sept 2014 -
Reviewed
14 Oct 2014 -
Accepted
19 Nov 2014