The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 93, Issue 16

Scientific Articles | August 17, 2011

Prevalence and Clinical Relevance of Radiographic Signs of Impingement in Metal-on-Metal Hybrid Hip Resurfacing

Thomas A. Gruen, MS¹; Michel J. Le Duff, MA²; Lauren E. Wisk, BS²; Harlan C. Amstutz, MD²

¹ 31153 Shaker Circle, Wesley Chapel, FL 33543
² Joint Replacement Institute at St. Vincent Medical Center, The S. Mark Taper Building, 2200 West Third Street, Suite 400, Los Angeles, CA 90057. E-mail address for H.C. Amstutz: harlanamstutz@dochs.org

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Disclosure: One or more of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of an aspect of this work. In addition, one or more of the authors, or his or her institution, has had a financial relationship, in the thirty-six months prior to submission of this work, with an entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. No author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.

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Investigation performed at the Joint Replacement Institute at St. Vincent Medical Center, Los Angeles, California

J Bone Joint Surg Am, 2011 Aug 17;93(16):1519-1526. doi: 10.2106/JBJS.I.01723

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Abstract

Background:

Implant-related impingement has been reported following metal-on-metal hip resurfacing, and reactive osseous patterns associated with implant-bone impingement have been identified. The purpose of this study was to determine the prevalence and clinical implications of radiographic signs of femoral neck-acetabular cup impingement following metal-on-metal hip resurfacing.

Methods:

Serial anteroposterior and lateral radiographs made five to 12.9 years postoperatively were available for ninety-one of the first 100 metal-on-metal hip resurfacing procedures (in eighty-nine patients) performed by the senior author. These radiographs were reviewed by a single independent observer, who was blinded to the clinical results. Radiographic signs of impingement were assessed and were correlated with clinical outcomes.

Results:

Twenty hips (in eighteen patients) had at least one of two reactive osseous signs: a solitary exostosis (six hips, 7%) and an erosive “divot-type” deformity (twenty hips, 22%). Each radiographic sign occurred predominantly at the superior aspect of the femoral neck just distal to the femoral component. None of the patients with such an impingement sign reported any symptoms or discomfort during examination of the range of hip motion. These patients had a greater mean postoperative University of California Los Angeles activity score and a greater mean range of hip motion than the patients without an impingement sign. Based on the numbers available, there was no association between component size, abduction angle and anteversion angle of the socket, femoral stem-femoral shaft angle, or femoral component-femoral neck ratio and the occurrence of repetitive impingement signs on radiographs.

Conclusions:

The reactive osseous features identified in this study should facilitate the radiographic assessment of impingement in other patients following hip resurfacing arthroplasty. Longer-term follow-up is needed to determine whether radiographic signs of impingement are of prognostic consequence.

Level of Evidence:

Therapeutic Level IV. See Instructions to Authors for a complete description of levels of evidence.

Figures in this Article

Introduction

Since the advent of metal-on-metal bearing surfaces, hip resurfacing has been regaining popularity, particularly in the younger and more active patient^1-9. The use of a large femoral head is assumed to enhance the overall stability of the joint^10,11, but the lower femoral head-neck ratio in hip resurfacing compared with that in conventional stem-type total hip replacement remains controversial because of the potential risk of impingement resulting from restricted hip motion. Recent in vitro range-of-motion studies and finite-element analyses have suggested that repetitive implant-to-bone impingement may become a latent clinical problem^12-14. Ongoing clinical studies have not yet provided corroborative radiographic evidence of osseous impingement, although there have been a few case reports of femoral neck remodeling associated with impingement^15,16.

The purpose of the current study was to determine the radiographically visible morphological features associated with repetitive osseous impingement between the femoral neck and the acetabular cup following metal-on-metal hip resurfacing, and to assess the locations, prevalence, and clinical implications of these impingement signs.

Materials and Methods

The first 100 consecutive primary metal-on-metal hip resurfacing procedures were performed by the senior author (H.C.A.) between November 1996 and December 1998 in eighty-nine patients, and details have been published previously^17,18. The retrospective radiographic review of these hip resurfacings was approved by the hospital institutional review board.

The mean age (and standard deviation) of the patients at the time of the hip resurfacing was 49.1 ± 15.5 years (range, fifteen to seventy-one years), and fifty-nine (66%) were men. Four patients had bilateral hip resurfacing performed in a single operative session, and seven patients had sequential bilateral hip resurfacing performed with an interval between procedures that ranged from 2.5 to seventeen months. Fifteen patients had a subsequent primary resurfacing arthroplasty of the contralateral hip, but only the initial metal-on-metal hip resurfacing with the minimum ten-year duration of clinical follow-up was included in the current study. During the follow-up period, eleven resurfaced hips were converted to a total hip arthroplasty, five patients (five hips) died of a cause unrelated to the resurfacing, and two patients (two hips) were lost to follow-up¹⁷. The mean duration of radiographic follow-up was 9.2 ± 2.8 years (range, 2.4 to 12.9 years). Seventy-one hips had at least ten years of radiographic follow-up, and ninety-one hips had at least five years. The analysis of the radiographic findings was based on the ninety-one hips with a minimum of five years of follow-up. The etiology of the hip disease and the patient demographics for these ninety-one hips are shown in Table I and the Appendix.

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TABLE I Preoperative Etiology of the Resurfaced Hips

	Radiographic Signs of Impingement
Etiology	Present (N = 20)	Absent (N = 71)
Osteoarthritis	15	44
Developmental dysplasia	0	6
Osteonecrosis	5	13
Posttraumatic osteoarthritis	0	1
Legg-Calvé-Perthes disease	0	0
Slipped capital femoral epiphysis	0	1
Epiphyseal dysplasia	0	1
Ankylosing spondylitis	0	3
Juvenile rheumatoid arthritis	0	1
Melorheostosis	0	1
Previous surgical procedures
Hemiresurfacing	1	1
Osteotomy	0	2
Pinning	0	1
Coring	1	4

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TABLE I Preoperative Etiology of the Resurfaced Hips

	Radiographic Signs of Impingement
Etiology	Present (N = 20)	Absent (N = 71)
Osteoarthritis	15	44
Developmental dysplasia	0	6
Osteonecrosis	5	13
Posttraumatic osteoarthritis	0	1
Legg-Calvé-Perthes disease	0	0
Slipped capital femoral epiphysis	0	1
Epiphyseal dysplasia	0	1
Ankylosing spondylitis	0	3
Juvenile rheumatoid arthritis	0	1
Melorheostosis	0	1
Previous surgical procedures
Hemiresurfacing	1	1
Osteotomy	0	2
Pinning	0	1
Coring	1	4

All of the metal-on-metal hip resurfacings were performed with use of CONSERVE PLUS implants (Wright Medical Technology, Arlington, Tennessee), which were made of a cast cobalt-chromium-molybdenum alloy (conforming to the ASTM F-75 standard) that was heat-treated and solution-annealed. The head of the CONSERVE PLUS femoral component extends slightly beyond a hemisphere (208° arc)¹⁸.

The postoperative clinical outcome was assessed with use of several outcome measures including the University of California Los Angeles (UCLA) hip score¹⁹, the Short Form-12 (SF-12) health survey score²⁰, and the Harris hip score²¹.

Anteroposterior, modified table-down lateral, and Johnson cross-table lateral radiographs²² were made during each follow-up visit. An independent reviewer (T.A.G.) who was experienced with hip resurfacing evaluated all radiographs retrospectively for the purposes of the current study. The reviewer was blinded to all clinical data until all radiographs had been read^23,24.

Radiographic signs of osseous impingement are associated with repetitive bone-to-bone or implant-to-bone abutment. Comparable signs for other joints such as the ankle^25-30 or the shoulder have been reported previously as “impingement” or “notching.”^31-34 Impingement syndromes resulting from implant-to-bone abutment have been reported following total shoulder arthroplasty^35-39.

Two primary signs of repetitive implant-to-bone impingement were identified in the radiographic evaluation performed in the current study: a reactive, solitary exostosis and an erosive “divot sign.”

Reactive exostosis is defined as a benign osseous protuberance that grows from the surface of a bone in response to inflammation or repeated trauma⁴⁰; this juxta-articular exostosis should not be confused with the marginal osteophyte, a common feature of osteoarthritis, which arises in the periosteum overlying the bone, at the junction between cartilage and bone^41,42. The so-called “divot sign” was defined radiographically as a localized “wedge-shaped” depression below the curvilinear contour of the surface of the femoral neck, and it is similar to radiographic signs associated with ankle impingement during hyperdorsiflexion^30,43. The wedge-shaped defect was clearly distinguishable from other previously reported osseous changes involving the femoral neck, such as femoral neck notching, neck narrowing, and periprosthetic osteolytic lesions.

The regions of interest included the superior and inferior surfaces of the femoral neck on the anteroposterior radiograph and the anterior and posterior surfaces of the neck on the lateral radiographs. The first appearance of osseous impingement was recorded when a reactive exostosis and/or a divot sign at least 2 mm in height or depth became evident on the radiographs. The presence of any “cortical thickening” at the base of the divot sign was also recorded during the review of the radiographs.

The cup abduction angle and anteversion angle were calculated with use of Einzel-Bild-Roentgen-Analysis cup software (EBRA-CUP Digital, 2003 release; Department of Engineering Mathematics, Geometry and Computer Science, University of Innsbruck, Innsbruck, Austria)⁴⁴.

The prosthetic femoral head-femoral neck ratio was measured by a research associate on the first postoperative anteroposterior radiograph, taken within four months of the resurfacing, on which the patient was able to lie on the x-ray table with the hip in sufficient internal rotation. The possibility of impingement was assessed with use of the EBRA cup software by circumscribing a circle corresponding to the femoral component head on the image and determining the location of potential contact points between the acetabular cup and the femoral neck. ImageJ image processing and analysis software (version 1.41; National Institutes of Health, Bethesda, Maryland) was used to measure the distance between these potential contact points as well as the diameter of the femoral head. The postoperative femoral head-neck ratio was calculated by dividing the diameter of the prosthetic femoral head by the measured distance between the contact points of the cup with the femoral neck. The preoperative femoral head-neck ratio was measured in a similar fashion with use of the EBRA software (Fig. 1).

Fig. 1

Measurement of the femoral head-neck ratio on a radiograph made six weeks postoperatively. The potential points of contact of the cup or the acetabulum with the femoral neck are determined with use of the Einzel-Bild-Roentgen-Analysis cup software, which overlays a circle interpolated from selected points on the periphery of the femoral head. The diameter of the femoral head (blue line) is then measured with use of this circle, and the diameter of the femoral neck (green line) is measured between the points at which the circle intersects the femoral neck.

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The hips were divided into two groups: a study group with observed radiographic evidence of impingement and a “control” group with no evidence of impingement. Descriptive statistics were compared between the two groups in an a posteriori analysis. The Shapiro-Wilk W test was used to determine the parametric nature of the variables studied. The Student t test was then used to compare parametric variables between the study group and the “controls,” and the Mann-Whitney U test was used to compare nonparametric variables between the groups. The Wilcoxon signed-rank test was used to compare preoperative with postoperative nonparametric variables. A p value of <0.05 was considered significant, although a value between 0.01 and 0.05 should be interpreted with caution because of the multiple comparisons that were performed.

Source of Funding

Funding for the study was provided by St. Vincent Medical Center, Los Angeles, and by Wright Medical Technology, Inc.

Results

Twenty resurfaced hips (22%, in eighteen patients) had at least one radiographic sign of impingement at the time of the latest follow-up. The mean duration of radiographic follow-up for the hips with signs of impingement was 123.5 ± 29.5 months (range, forty-two to 154 months). When present, the reactive exostosis typically appeared first, and was followed by the appearance of the divot sign. The first appearance of an impingement sign on the available radiographs occurred at a mean (and standard deviation) of 37.1 ± 20 months but ranged from twelve to eighty months.

All twenty hips with radiographic signs of impingement exhibited a divot sign at the time of the latest follow-up, and six of the twenty (7% of the entire cohort) also exhibited a reactive exostosis.

The height of the reactive exostosis ranged from 2 to 5 mm, and the depth of the divot sign ranged from 2 to 7 mm. The distance between the distal edge of the femoral component and the exostosis was typically slightly greater than the width of the metallic acetabular shell (5 mm), and the divot sign was situated between the reactive exostosis and the distal edge of the femoral component (Figs. 2-A and 2-B). The regions in which the exostotic bone formation and the divot sign occurred are summarized in Figures 3-A and 3-B.

Fig. 2-A Fig. 2-B

Fig. 2-A Anteroposterior hip radiograph made immediately after metal-on-metal hip resurfacing for the treatment of osteoarthritis in an active forty-eight year-old man. Fig. 2-B Anteroposterior hip radiograph of the same patient made ten years after the resurfacing. The patient remained active and without symptoms. His University of California Los Angeles (UCLA) subscores were 10 for pain, 10 for walking ability, 10 for function, and 8 for activity. The arrow points to the solitary exostosis. As shown by the overlay generated by the Einzel-Bild-Roentgen-Analysis cup software, the cortical remodeling at the site of the defect almost perfectly matches the predicted path and shape of the impinging acetabular component (red dotted lines). The white dotted line represents the original superior surface of the femoral neck.

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Fig. 3-A Fig. 3-B

Figs. 3-A and 3-B Venn diagrams showing the locations at which each impingement sign was observed (S = superior, P = posterior, and A = anterior). Fig. 3-A An exostosis was observed superiorly in five hips, with four hips displaying only a superior exostosis and one hip displaying both a superior and a posterior exostosis. One additional hip displayed only a posterior exostosis. Fig. 3-B A divot sign was observed superiorly in all twenty hips with impingement signs, with fourteen hips displaying only a superior divot sign, four hips displaying both a superior and a posterior divot sign, one hip displaying both a superior and an anterior divot sign, and one hip displaying a divot sign in all three regions.

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At the time of the latest follow-up, twelve (60%) of the hips with a divot sign had reactive sclerosis along the impingement surface, which was often followed by cortical thickening at the base of the wedge-shaped defect (Figs. 2-B and 4).

Fig. 4

Radiographs made ten years after metal-on-metal hip resurfacing for the treatment of osteoarthritis in a sixty-seven year-old woman. She participated in yoga and had UCLA hip subscores of 9 for pain, 10 for walking ability, 10 for function, and 5 for activity. Note the presence of a divot sign in all three regions—superiorly, anteriorly, and posteriorly—and the presence of cortical thickening at the base of the defect. The arrows indicate the superior divot sign on the anteroposterior view (top) and both the anterior and the posterior divot sign on the lateral view (bottom).

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None of the twenty hips with radiographic signs of impingement were symptomatic or had pain during hip motion testing at the time of the latest follow-up. No postoperative episodes of component subluxation or dislocation, adverse local tissue reaction, component loosening or migration, or femoral neck fractures were noted in these twenty hips.

The patients with radiographic signs of hip impingement did not differ significantly from the patients without signs of impingement with respect to sex, mean age, mean height, or mean weight at the time of the surgery, but the mean body-mass index was lower in the patients with signs of impingement (p = 0.0045) (see Appendix). The mean UCLA subscores for postoperative pain and walking ability did not differ significantly between the two groups. The postoperative SF-12 scores indicated that the quality of life was comparable between the two groups (Table II).

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TABLE II Patient-Related Outcomes at the Latest Follow-up*

	Radiographic Signs of Impingement
	Present (N = 20)†	Absent (N = 71)†	P Value
UCLA pain‡	9.5 (0.6)	9.5 (0.9)	0.4883
UCLA walking ability‡	9.7 (0.8)	9.2 (1.3)	0.0628
UCLA function‡	9.7 (0.9)	8.7 (2.0)	0.0303
UCLA activity	7.8 (1.8)	6.6 (1.8)	0.0133
SF-12 physical health‡	50.8 (8.8)	46.6 (11.8)	0.1533
SF-12 mental health‡	48.8 (10.4)	51.2 (11.0)	0.2068
Hip flexion‡(deg)	133.3 (8.2)	122.6 (11.8)	0.0003
Abduction‡(deg)	51.0 (11.7)	42.8 (7.5)	0.0041
Adduction (deg)	31.3 (5.3)	25.9 (5.6)	0.0003
Internal rotation (deg)	43.2 (15.9)	34.3 (14.6)	0.0264
External rotation (deg)	44.7 (12.3)	37.8 (10.5)	0.0178
Arc of rotation (deg)	87.8 (17.4)	72.1 (17.3)	0.0009

*UCLA = University of California Los Angeles, and SF-12 = Short Form-12.
†Values are expressed as the mean, with the standard deviation in parentheses.
‡The variable was not normally distributed.

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TABLE II Patient-Related Outcomes at the Latest Follow-up*

	Radiographic Signs of Impingement
	Present (N = 20)†	Absent (N = 71)†	P Value
UCLA pain‡	9.5 (0.6)	9.5 (0.9)	0.4883
UCLA walking ability‡	9.7 (0.8)	9.2 (1.3)	0.0628
UCLA function‡	9.7 (0.9)	8.7 (2.0)	0.0303
UCLA activity	7.8 (1.8)	6.6 (1.8)	0.0133
SF-12 physical health‡	50.8 (8.8)	46.6 (11.8)	0.1533
SF-12 mental health‡	48.8 (10.4)	51.2 (11.0)	0.2068
Hip flexion‡(deg)	133.3 (8.2)	122.6 (11.8)	0.0003
Abduction‡(deg)	51.0 (11.7)	42.8 (7.5)	0.0041
Adduction (deg)	31.3 (5.3)	25.9 (5.6)	0.0003
Internal rotation (deg)	43.2 (15.9)	34.3 (14.6)	0.0264
External rotation (deg)	44.7 (12.3)	37.8 (10.5)	0.0178
Arc of rotation (deg)	87.8 (17.4)	72.1 (17.3)	0.0009

*UCLA = University of California Los Angeles, and SF-12 = Short Form-12.
†Values are expressed as the mean, with the standard deviation in parentheses.
‡The variable was not normally distributed.

The mean postoperative UCLA function and activity subscores and all mean postoperative hip motion measurements were greater in the group with radiographic signs of impingement than in the group without signs of impingement (Table II).

A trend toward a lower mean abduction angle of the acetabular component (p = 0.0870) in the hips with radiographic signs of impingement was observed (see Appendix). In addition, the mean preoperative femoral head-neck ratio of the entire cohort of ninety-one hips (1.29) did not differ significantly from the mean postoperative prosthetic head-femoral neck ratio (1.31, p = 0.6842). The preoperative head-neck ratio could not be computed in three hips because the geometry of the femoral head did not permit the application of our method.

A scatterplot of the acetabular component orientation in the twenty hips in the impingement group demonstrated that fifteen were within the so-called “safe zone” defined by Lewinnek et al.⁴⁵ (Fig. 5). Four of the five acetabular cups positioned outside the Lewinnek safe zone had a divot sign in two or more contiguous regions, including one hip with radiographic signs of impingement in all three regions. The three hips with a posterior impingement sign included one with an excessive acetabular abduction angle of >50° and two with an apparent acetabular component anteversion of >25°; the two hips with anterior impingement included one with excessive anteversion and one with an abduction angle of <30° (Fig. 5). Forty-nine of the seventy-one hips without radiographic signs of impingement were located inside the Lewinnek safe zone, and twenty-two were located outside this zone.

Fig. 5

Lewinnek “safe-zone” chart for the twenty hips with radiographic signs of impingement. The abduction angle is plotted on the horizontal axis, and the version angle is plotted on the vertical axis. A superior impingement sign was present in all twenty hips. Data points are labeled with an “A” if additional anterior impingement was visible and with a “P” if additional posterior impingement was visible.

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Discussion

The most important finding of the current study was the absence of adverse clinical consequences associated with the presence of radiographic signs of impingement. This is in contrast with reports investigating conventional total hip implants, for which impingement has been commonly associated with an increased risk of component subluxation and/or dislocation⁴⁶ and with subsequent loosening of the acetabular component⁴⁷.

To our knowledge, the possibility of impingement following resurfacing arthroplasty was first identified in a study involving canines, in which the bone-to-implant impingement led to three cases of postoperative neck fracture⁴⁸. In contrast with the component used in the canine study, which had a sharp edge, the metallic acetabular socket used in the current study has a chamfered rim, which appears to induce remodeling rather than fracture.

Several recent reports of impingement following metal-on-metal hip resurfacing have been published^15,16,49-51; three of these are case reports that indicated an association between impingement and symptomatic hips^15,50,51, and only one described the prevalence of the so-called impingement sign, although the most common location of the sign was different from the most common location in our study¹⁶.

Lavigne et al.¹⁵ emphasized the need for care in resecting the femoral neck osteophytes associated with femoroacetabular impingement, in accordance with the suggestion of a study in which it was concluded that no more than 30% of the diameter of the femoral neck could be removed without leading to a fracture of the femoral neck⁵².

Only one of the twenty hips in our study that had radiographic signs of impingement had concurrent evidence of femoral neck narrowing. This implies that radiographic signs of impingement and femoral neck narrowing are two distinctly separate phenomena of reactive osseous changes following metal-on-metal hip resurfacing. The two radiographic signs of impingement reported in the current study, a solitary exostosis and the juxta-articular “divot sign,” have unique features and complement the list of radiographic findings commonly observed after hip resurfacing. The recognition of these two radiographic signs of impingement is dependent on a critical review of serial radiographs, particularly the preoperative and immediate postoperative radiographs, made with use of standardized radiographic projections.

The time between the arthroplasty and the first observation of radiographic signs of impingement averaged 37.1 ± 20 months but ranged from twelve to eighty months. Some of this variation may have resulted from the preference of some patients for resuming a high preoperative activity level; the absence of serial radiographs made prior to five years postoperatively in four patients may also have contributed to the variation. The observation of sclerosis and cortical thickening at the base of the concavity suggested that vascular viability of the superior surface of the femoral neck was preserved.

A divot sign could be seen in two or more contiguous regions, on both the anteroposterior and lateral radiographs, in six hips. The appearance of the divot sign in more than one view suggests that this sign may not represent a localized defect. Instead, it may represent a groove in the femoral neck associated with a combination of supraphysiological hip motions, similar to the ridges and grooves on subchondral, eburnated osseous surfaces of osteoarthritic joints⁵³. Computed tomography, magnetic resonance imaging, or ultrasonography may better delineate the morphological characteristics associated with the impingement signs, as may three-dimensional, subject-specific computer modeling studies similar to those that have been used in studies of conventional stem-type total hip replacements^54-56 to provide a detailed assessment of the role of component orientation and positioning in bone-to-implant impingement. Radiographs represent planar projections; consequently, they often underestimate geometric parameters⁵⁷, and many of the standard radiographic parameters used to diagnose hips with musculoskeletal disorders were found to not be reproducible in a recent study of observer agreement⁵⁸.

The data from the current study did not establish a relationship between component positioning and the presence of radiographic signs of impingement. For instance, signs of impingement in several hips were associated with an apparent lack of osseous coverage of the acetabular component⁵⁹, but this lack of coverage was not necessarily associated with a high abduction angle or a high anteversion angle of the acetabular cup. In contrast, patient-related variables, particularly hip motion and physical activity, were significantly associated with the presence of impingement and appear to be stronger predictors of impingement between the femoral neck and the acetabular socket. Patients with radiographic signs of impingement were typically more active than patients without signs of impingement, and they typically had greater hip motion associated with the practice of activities requiring more flexibility.

Despite the lack of symptoms or other adverse consequences, continued clinical and radiographic follow-up is important to determine whether radiographic signs of impingement are of prognostic consequence. The reactive osseous features identified in this study should facilitate the radiographic assessment of impingement in other patients following hip resurfacing arthroplasty. We now recommend increasing the ratio between the prosthetic femoral head diameter and the femoral neck width, and we also recommend practicing a more careful orientation of the components during the arthroplasty procedure in order to optimize the range of hip motion for the activities that the patient is anticipated to participate in.

Appendix

Tables showing demographic and implant-related characteristics of the groups with and without radiographic signs of impingement are available with the online version of this article as a data supplement at jbjs.org.

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Topics

acetabulum ; neck of femur ; hip joint ; osteochondroma ; radiographic signs ; femoral acetabular impingement ; hip bearing surface, metal-on-metal ; total hip replacement, metal-on-metal

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Thomas A. Gruen, Michel J. Le Duff, Lauren E. Wisk, Harlan C. Amstutz; Prevalence and Clinical Relevance of Radiographic Signs of Impingement in Metal-on-Metal Hybrid Hip Resurfacing. The Journal of Bone & Joint Surgery. 2011 Aug;93(16):1519-1526.

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