Biomechanical study of ACL reconstruction grafts

There are no published studies describing the strength quadrupled gracilis tendon alone and quadrupled semitendinosus tendon alone in the configuration used for anterior cruciate ligament (ACL) reconstruction. The primary objective was to compare the mechanical properties of grafts used for ACL reconstruction during a tensile failure test. The secondary objective was to evaluate the effect of uniform suturing on graft strength. Fifteen pairs of knees were used. The mechanical properties of five types of ACL grafts were evaluated: patellar tendon (PT), sutured patellar tendon (sPT), both hamstring tendons (GST4), quadrupled semitendinosus (ST4), and quadrupled gracilis (G4). Validated methods were used to perform the tensile tests to failure and to record the results. Student's t‐test was used to compare the various samples. The maximum load to failure was 630.8N (± 239.1) for the ST4, 473.5N (± 176.9) for the GST4, 413.3N (± 120.4) for the sPT, and 416.4N (± 187.7) for the G4 construct. Only the ST4 had a significantly higher failure load than the other grafts. The sPT had a higher failure load than the PT. The ST4 construct had the highest maximum load to failure of all the ACL graft types in the testing performed here. Uniform suturing of the grafts improved their ability to withstand tensile loading. © 2015 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 33:1188–1196, 2015.     

Research on strength of the grafts that are used in anterior cruciate ligament reconstruction]

Reconstruction of the anterior cruciate ligament (ACL) using autogenous tissue is a frequently performed procedure used to restore functional stability in ACL--deficient knees. The purpose of this study was to determine the structural mechanical properties of the ACL and the grafts that are used in anterior cruciate ligament reconstruction. We tested specimens of human tissue including: ACL, medial third patellar tendon B-PT-B, central third patellar tendon B-PT-B, gracilis tendon, semitendinosus tendon (single-stranded, double-stranded and quadrupled-stranded), distal iliotibial tract and plantaris tendon (single-stranded and double-stranded). Specimens were obtained at autopsy from 32 young male cadavers. Biomechanical tests were performed using the FPZ-100 machine (produced by VEB Rauenstein). The following grafts have shown higher values than ACL: quadrupled semitendinosus--229% of ACL, doubled semitendinosus--130% of ACL, central third patellar tendon B-PT-B--114% of ACL and medial third patellar tendon B-PT-B--107% of ACL. The following grafts have shown lower values than ACL: semitendinosus tendon--72% of ACL, gracilis tendon--49% of ACL, distal iliotibial tract--47% of ACL, doubled plantaris--18% of ACL and single plantaris--10% of ACL.     

前交叉韧带重建术中等长点确定的临床研究

目的 研究前交叉韧带单束重建中等长点位置寻找的方法 及术后效果.方法 选择25例单纯前交叉韧带断裂病例,使用四股的半腱肌和骨薄肌肌腱关节镜下重建前交叉韧带.术中综合应用解剖定位和透视定位方法 初步确定等长点,检查等长效果(误差控制在2 mm以内).记录股骨隧道内口中央点选点次数及变点方向.术后1年随访,行Lysolm膝关节功能评分.结果 17例选点1次.8例变更了股骨选点位置,5例上移,1例下移,2例后上移动,选点次数为1～4次,平均约1.36次.术后随访19例,Lysolm评分92～100分,平均97.5分.结论 在股骨隧道内口初步选点后行等长效果检查,对保证手术质量有非常重要的意义.无论是解剖定位法还是透视定位法,都不能保证在所有病例中的等长效果.     

Prospective clinical comparisons of semitendinosus versus semitendinosus and gracilis tendon autografts for anatomic double-bundle anterior cruciate ligament reconstruction

Background

The data available from the previously reported clinical studies remains insufficient concerning the hamstring graft preparation in double-bundle anterior cruciate ligament (ACL) reconstruction.

Objective

To test the hypothesis that there are no significant differences between the semitendinosus tendon alone and the semitendinosus and gracilis tendon graft fashioning techniques concerning knee stability and clinical outcome after anatomic double-bundle ACL reconstruction.

Methods

A prospective study was performed on 120 patients who underwent anatomic double-bundle ACL reconstruction according to the graft fashioning technique. The authors developed the protocol to use hamstring tendon autografts. When the harvested doubled semitendinosus tendon is thicker than 6 mm, each half of the semitendinosus tendon is doubled and used for the anteromedial (AM) and posterolateral (PL) bundle grafts (Group I). On the other hand, when the harvested semitendinosus tendon is under 6 mm in thickness, the gracilis tendon is harvested additionally. The distal half of the semitendinosus and gracilis tendons are doubled and used for the AM bundle graft, and the remaining proximal half of the semitendinosus tendon is doubled and used for the PL bundle grafts (Group II). Sixty-one patients were included in Group I, and 59 patients in Group II. The two groups were compared concerning knee stability and clinical outcome 2 years after surgery.

Results

The postoperative side-to-side anterior laxity averaged 1.3 mm in both groups, showing no statistical difference. There were also no significant differences between the two groups concerning the peak isokinetic torque of the quadriceps and the hamstrings, the Lysholm knee score, and the International Knee Documentation Committee evaluation.

Conclusion

There were no significant differences between the two graft fashioning techniques after anatomic double-bundle ACL reconstruction concerning knee stability and postoperative outcome. The present study provided orthopedic surgeons with important information on double-bundle ACL reconstruction with hamstring tendons.

Level of evidence

Level II; prospective comparative study.     

Biomechanics of anterior cruciate ligament reconstruction using twisted doubled hamstring tendons

We studied the biomechanical properties of a twisted doubled semitendinosus and gracilis graft. We applied an un-axial load in order to reproduce the kinematics of a reconstructed anterior cruciate ligament (ACL). A modified cryo-jaw clamp system was used to minimize soft tissue slippage. The lower grip, after fixation of the free ends of the tendons, was rotated 45 degrees, translated 1 cm, and bent 40 degrees, simulating a knee sprain. The graft was tested to failure using a servohydraulic machine. The specimen from one knee of seven unembalmed cadavers was assigned to the untwisted (parallel) bundles group, while its pair was assigned to the twisted group. For the parallel bundles group, the mean maximum load was 1,709.3+/-581.9 N, for the twisted group 2,428.3+/-475.4 N (P<0.05). The mean stiffness was respectively 213.6+/-72.4 N/mm and 310.3+/-97.3 N/mm (P=0.08). Although caution should be used in extrapolating the results to clinical estimates of the strength of hamstring grafts, the results of the present study could justify the use of twisted semitendinosus and gracilis bundles in ACL reconstruction.     

兔四股半腱肌腱重建前交叉韧带的生物力学研究

目的应用动物模型研究四股半腱肌腱重建兔前交叉韧带（ACL）后的生物力学转归以及是否可以通过将四股半腱肌腱编织改善等张性的方法促进束间融合,改善生物力学性能。方法采用成年健康新西兰大白兔32只,分为两组,每组16只,一组行常规自体四股半腱肌腱重建ACL（常规重建组）,另一组行编织的四股半腱肌腱重建ACL手术（编织组）。每组于术后26周和52周各处死8只进行ACL观察,并每组取6只行生物力学测试对比研究。结果常规重建组26及52周共16例韧带中,5例融合为一束,11例存在分束。编织组16例标本中,13例合为一束,3例呈不同程度的分束状态。生物力学测试显示：常规重建的韧带26和52周的最大载荷分别达到正常韧带的22．63％和35．87％,编织组26和52周的最大载荷达到正常韧带的33．17％和67．20％;编织组26、52周标本的最大载荷和硬度均显著高于常规重建组。结论四股半腱肌腱作为前交叉韧带的移植物,各束之间可以发生融合、部分融合以及分束的状态,原因可能与它们之间的相对运动有关,通过编织减少这种相对运动,可以促进各束融合,提高生物学及生物力学性能。     

ACL reconstruction using bone‐tendon‐bone graft engineered from the semitendinosus tendon by injection of recombinant BMP‐2 in a rabbit model

We attempted to generate a bone‐tendon‐bone structure by injecting human‐type recombinant human bone morphogenetic protein‐2 (rhBMP‐2) into the semitendinosus tendon, and an anterior cruciate ligament (ACL) defect was reconstructed by grafting the engineered bone‐tendon‐bone graft. Two ossicles with a separation distance of 1 cm were generated within the left semitendinosus tendon of a rabbit 6 weeks after the injection of rhBMP‐2 (15 µg at each site). The engineered bone‐tendon‐bone graft was transplanted in order to reconstruct the ACL by passing the graft through the bone tunnels. In the control group, the ACL was reconstructed with the semitendinosus tendon without BMP‐2 using the same methods as those used in the experimental group. The animals were harvested at 4 or 8 weeks after surgery and examined by radiographic, histological, and biomechanical methods. In the experimental group, ossicles in the bone‐tendon‐bone graft were successfully integrated into the host bone of the femur and tibia. Histological analysis revealed that characteristic features identical to the normal direct insertion morphology had been restored. Biomechanical pull‐out testing showed that the ultimate failure load and stiffness of the reconstructed ACL in the experimental group were significantly higher than those in the control group at both 4 and 8 weeks (p < 0.05). These results indicate the potential of regenerative reconstruction of the ACL, and the reconstruction resulted in the restoration of morphology and function equivalent to those of the normal ACL. © 2011 Orthopaedic Research Society Published by Wiley Periodicals, Inc. J Orthop Res 29:1923–1930, 2011     

Patellar tendon versus quadrupled bone-semitendinosus anterior cruciate ligament reconstruction: a prospective clinical investigation in athletes

Purpose:Patellar tendon and hamstrings are both used in anterior cruciate ligament (ACL) reconstruction, and comparisons have been reported with different results. The purpose of this clinical study was to compare the results of ACL reconstruction in athletes with 2 different graft types, both using bone-to-bone healing: bone-patellar tendon-bone graft and a quadrupled bone-semitendinosus graft.Type of Study:Outcomes study.Methods:From 1994 to 1997, 2 groups of 40 athletes who underwent ACL replacement with patellar tendon and quadrupled bone-semitendinosus grafts were prospectively evaluated. Preinjury activity level, age, and gender were comparable in both groups. All patients were operated on by the same surgeon within 5 months from injury and underwent group-specific rehabilitation programs. An independent examiner performed the final evaluations at 36 months. Review included clinical examination, radiographs, computed analysis, isokinetic and functional strength tests, and subjective and objective evaluation with standard knee scores. Additional procedures were recorded. Statistical analysis was performed with both parametric and nonparametric tests.Results:Average surgical time was longer with the semitendinosus graft, and postoperative pain was higher in the patellar tendon group. Standard knee evaluation scores and subjective assessment revealed no significant differences. Isokinetic testing of flexion-extension and internal-external rotation showed lower quadriceps strength and a mild deficit of external rotation in the patellar tendon group and slightly lower flexor strength in the semitendinosus group at 12 months. Computerized laxity analysis showed no difference between the 2 groups with 90% of patients having less than 3 mm side-to-side difference, with a gender difference in the semitendinosus group. Kneeling pain was higher in patellar tendon group.Conclusions:The bone-patellar tendon-bone and quadrupled bone-semitendinosus autograft provide excellent grafts for ACL reconstruction. Both techniques are comparable regarding final stability, but in patients with extensor mechanism problems or those who engage in sports with a high incidence of patellar tendonitis, the semitendinosus graft should be considered.     

Quadrupled bone-semitendinosus ACL reconstruction: a prospective clinical investigation in 100 patients

Abstract The hypothesis of our study was that a quadrupled bonesemitendinosus tendon graft could combine the advantage of bone-tobone healing with the high cross-sectional area of a quadrupled hamstring graft in ACL reconstruction. ACL reconstruction with a semitendinosus tendon graft was performed on 100 patients with isolated ACL injury from January 1996 to December 1999: femoral fixation was obtained with Endobutton and tibial fixation with Fastlok. Patients were evaluated for standard knee scores and functional strength tests, postoperative pain rating, knee radiographs taken after surgery and at final follow-up, magnetic resonance images at 3 and 6 months, isokinetic flexion-extension and internal-external rotation tests at 3, 6, and 12 months. Computerized laxity analysis was performed at final evaluation. Average surgical time was 85 minutes, including 13 minutes for graft preparation; 90% of the patients were discharged within 24 h. Subjective knee rating was 80%; kneeling test was positive in 7% and Werner score was 44 (range, 30–48). Lachman test was negative in 90% at final evaluation (mean follow-up, 38 months). Sensory changes at the anterior part of the proximal tibia were present in 30% at 3 months and 10% had definite hyposthesia. MRI showed graft incorporation at 3 months. Computerized laxity analysis revealed 90% with less than 3-mm side-to-side differences. Isokinetic testing showed normal hamstring and quadriceps peak torques at 12 months. The functional strength tests were normal by 6 months. Average Noyes score was 87.9, Lysholm score 93, and Tegner activity rating 6.0 (pre-injury, 6.1). IKDC score showed 90 normal or nearly normal knees, 9 abnormal, and one severely abnormal knee. Quadrupled bone-semitendinosus is a viable graft for ACL reconstruction and should be considered, especially in patients with pre-existing extensor mechanism problems.     

Hamstring tendon anterior cruciate ligament reconstruction: does gracilis tendon harvest matter?

Purpose

Hamstring tendon grafts are a popular choice for anterior cruciate ligament (ACL) reconstruction. Typical morbidity reported after hamstring tendon harvest is muscle weakness in flexion, and whilst still a matter for debate, this morbidity may be greater if the gracilis tendon is harvested in addition to the semitendinosus. This study sought to comprehensively compare the outcome of ACL reconstructions in which the semitendinosus was harvested alone (ST group) or with the gracilis (ST/G group).

Methods

Twenty patients (ten ST, ten ST/G) were assessed with a variety of measures that included subjective scores, function, strength and tibial rotation as measured by gait analysis during a pivoting task.

Results

Results showed that the graft diameter was significantly larger in the ST group, but there were no other differences between the groups for any other outcome measure.

Conclusion

Harvesting the gracilis in addition to semitendinosus does not appear to affect either the outcome or graft-related morbidity after hamstring ACL reconstruction.     

Biomechanical comparisons of anterior cruciate ligament: reconstruction procedures with flexor tendon graft

An experimental study was conducted to compare the biomechanical characteristics of six currently available anterior cruciate ligament (ACL) reconstruction procedures with flexor digitorum profundus tendons. Forty porcine knees were divided into eight groups, of 5 knees each. In groups A, B, C, and D, the flexor tendon graft was fixed with sutures and an Endobutton, with 20-mm-wide polyester tapes and staples, with 10-mm-wide polyester tapes and an Endobutton, and with bone plugs and interference screws, respectively. In group E, the graft was fixed using a combined procedure of those in groups B and D. In group F, the graft was directly fixed with interference screws. In groups G and H, the bone-patellar tendon-bone graft was fixed with interference screws, and sutures, respectively. Each femur-graft-tibia complex specimen was tested with a tensile tester by anteriorly translating the tibia until failure. This study demonstrated that the biomechanical properties of the femur-graft-tibia complex reconstructed with the flexor tendon graft were significantly affected by synthetic fixation devices. Regarding the average maximal load of the groups with the flexor tendon graft, group B had the highest (893 N) and group C had the second highest (770 N). Groups E and A were in the third rank. Group F had the second lowest (312 N), and Group D had the lowest (230 N). The maximal load of group B was significantly greater (P < 0.01) than that of group G (656 N) with the bone-patellar tendon-bone grafts. As to clinical relevance, this study indicated that the flexor tendon graft can be an alternative substitute for the bone-patellar tendon-bone graft for ACL reconstruction, if we understand the biomechanical characteristics of each reconstruction procedure. Received: January 21, 2000 / Accepted: June 8, 2000     

Hamstring regrowth following harvesting for ACL reconstruction: The lizard tail phenomenon

This study evaluated the ability of the native semitendinosus tendon to regenerate after harvest for anterior cruciate ligament (ACL) reconstruction in a rabbit model. The histological and biomechanical properties of the regenerate tendons also were studied. At 16 and 28 weeks post-harvesting of the semitendinosus tendon, the regenerate tissue was evaluated by magnetic resonance imaging, gross and histologic pathologic specimens, and biomechanical evaluation. Ten of 10 specimens at 16 weeks and 10 of 10 specimens at 28 weeks demonstrated regeneration of the semitendinosus tendon, with biomechanical strength 23% of normal tendon at 16 weeks and 62% of normal tendon at 28 weeks. The results of this study support regeneration of the semitendinosus tendon to its osseous insertion on the proximal tibia after harvesting for ACL reconstruction.     

Revision anterior cruciate ligament reconstruction using the regenerated semitendinosus tendon: Analysis of ultrastructure of the regenerated tendon

In this report, we present a case of a college skier who sustained a rerupture of the reconstructed anterior cruciate ligament (ACL) 8 months after surgery in which an autogenous semitendinosus tendon graft was used. At the revision surgery, the harvested semitendinosus tendon appeared to be regrown. Thus the regenerated tendon was reharvested, and in combination with the gracilis tendon, was used as a graft. The electron microscopic examination revealed a difference in fibril diameter between the regenerated tissue and the normal tendon. Although the regenerated semitendinosus tendon could be reharvested, the feasibility of its use for revision surgery is still to be determined.     

Tendon-to-bone healing of a semitendinosus tendon autograft used for ACL reconstruction in a sheep model

Anterior cruciate ligament (ACL) reconstruction was performed in a single hind limb of 30 sheep using a doubled semitendinosus tendon graft. Three additional animals were used as controls. Histologic and biomechanical analysis was performed from 4-52 weeks postoperatively. Perpendicular collagen fibers were found connecting the tendon graft to the bone tunnels at 8 weeks. These fibers were seen circumferentially at 12 weeks. By 24 weeks, the bone tunnel was well-defined, and no further changes were observed at 52 weeks. Tendon incorporation within the femoral and tibial tunnels was similar at each interval. Although the small sample size did not permit statistical testing, the reconstruction strength was similar up to 12 weeks (15%-19% of controls). This increased at 24 (28%) and 52 (40%) weeks. The stiffness primarily increased from 4-8 weeks (18%-39%) and 24-52 weeks (52%-82%). Up to 12 weeks, failures occurred by graft pull-out from the bone tunnel. All 24- and 52-week specimens ruptured through the intra-articular portion of the graft, further indicating sufficient graft incorporation within the bone tunnels.     

Double-bundle anatomic anterior cruciate ligament reconstruction using bone-hamstring-bone composite graft

The bone-hamstring-bone (BHB) composite graft is a hybrid ligament reconstruction methodology that combines the advantages but eliminates the disadvantages of the bone-patellar tendon-bone (BPTB) and tendon of semitendinosus and gracilis muscle (STG) methods. We have developed an innovative modified BHB method involving anatomic anterior cruciate ligament (ACL) reconstruction. It takes into account the 2 bundles of the ACL: the anteromedial bundle and the posterolateral bundle. The composite graft was prepared by folding the gracilis and the semitendinosus tendons twice and flanking the ends by bone blocks obtained from the tibia. One tunnel of 11-mm diameter was made in the tibia and the femur, and the top of the graft was introduced into the femoral socket; the distal end of the graft was rotated 90° in the counterclockwise direction for a right knee and 90° in the clockwise direction for a left knee to apply a twist to the graft, giving rise to an anteromedial bundle and a posterolateral bundle. The bone blocks attached to the graft were fixed with 2 interference screws. Modified BHB technique allows free selection of the location of the bone plug, minimizes the intra-articular length of the graft, and maintains the double-bundle structure of the original ACL.Arthroscopy: The Journal of Arthroscopic and Related Surgery, Vol 18, No 5 (May-June), 2002: pp 550–555     

Double-stranded hamstring tendons for anterior cruciate ligament reconstruction.

Bone-patellar tendon-bone autograft is the most commonly used tissue for ACL reconstruction; however, the harvesting of patellar tendon as a free graft can lead to significant morbidity. Alternate grafts may lower morbidity, yet the most commonly used alternate grafts including the double-stranded semi-tendinosus or gracilis have not been studied biomechanically. This study investigated the morphometric and biomechanical properties of double-stranded semi-tendinosus and gracilis tendons separately along with the patellar and quadriceps tendons obtained bilaterally from six fresh, 77-year-old cadaveric specimens. The quadriceps tendon was the thickest and therefore had the largest cross-sectional area, whereas double-stranded semitendinosus had the highest mean peak load to failure (1029+/-158.4 N), 11.5% and 10.3% stronger than patellar tendon and quadriceps tendons, respectively. Midsubstance rupture occurred in the hamstring tendons, whereas the patellar and quadriceps tendons failed at the bone-tendon junctions. Semitendinosus tendons with higher cross-sectional area had higher peak loads to failure. This linear relationship between cross-sectional area and the peak load to rupture also was observed in the other tendon groups (except gracilis). These results indicate that despite a lower cross-sectional area of the double-stranded semitendinosus, this tendon demonstrated a comparable mean peak load to rupture and stress compared with patellar and quadriceps tendons. It also was demonstrated that combined double-stranded semitendinosus and gracilis tendons produce a stronger graft with initial strength twice that of the patellar tendon, but requires further testing.     

无内固定物腘绳肌腱重建前交叉韧带临床探讨

目的探讨用无内固定物的绳肌腱重建前交叉韧带的临床运用和效果。方法自2002年12月～2004年6月对33例前交叉韧带损伤进行了无内固定物的绳肌腱重建前交叉韧带术,其中13例移植肌腱采用二股半腱肌腱和二股股薄肌腱,另20例仅为二股半腱肌腱,术前和术后进行Lachman试验评估膝关节的稳定性,用Lysholm评分方法评定膝关节功能。结果术前Lachman试验均为阳性,术后29例为阴性,4例为阳性。术前Lysholm评分为36～57分,术后Lysholm评分为71～96分。结论无内固定物的绳肌腱重建前交叉韧带为生物固定,固定可靠、费用少、短期效果好,中长期效果有待观察。     

关节镜下自体半腱肌、股薄肌肌腱保留残端重建前交叉韧带的疗效

目的探讨关节镜下自体半腱肌、股薄肌肌腱保留残端重建前交叉韧带(ACL)的疗效。方法在关节镜下取自体半腱肌、股薄肌肌腱保留残端重建38例ACL断裂患者。记录术后并发症、膝关节屈曲活动度,采用Lysholm评分评定临床疗效。结果患者均获得随访,时间12~20个月。术后患者均未出现切口感染、腘动脉血管损伤、下肢深静脉血栓、韧带二次断裂、关节失稳等严重合并症。术后1例下肢皮肤痛觉减退,给予营养神经等治疗5 d后逐渐恢复,考虑为术中使用止血带引起的神经损伤。Lysholm评分:术后6个月、1年明显高于术前,差异均有统计学意义(P<0.05),术后1年明显高于术后6个月,差异有统计学意义(P<0.05)。膝关节屈曲活动度末次随访时较术前明显改善,差异有统计学意义(P<0.05)。结论关节镜下自体半腱肌、股薄肌肌腱保留残端重建ACL手术破坏性小,术后可以早期愈合,功能恢复良好。     

Rotational muscle strength of the limb after anterior cruciate ligament reconstruction using semitendinosus and gracilis tendon

Purpose: To investigate the influence of harvesting semitendinosus and gracilis tendons on the rotational muscle strength of the limb after anterior cruciate ligament (ACL) reconstruction. Type of Study: Prospective study. Methods: We performed a prospective study of 62 consecutive (34 male, 28 female) patients with ACL reconstructions using the semitendinosus and gracilis tendons. The mean age at surgery was 20.8 years. The semitendinosus tendon was harvested in 32 patients (ST group), and semitendinosus and gracilis tendons in 30 patients (STG group). The peak isokinetic torques for extension, flexion, internal rotation, and external rotation were measured before and 12 months after ACL reconstruction using the Cybex 6000B system (Cybex Division of Lumex, Ronkonkoma, NY). The rotational torque was measured at 30°/sec and 120°/sec. Results: Before reconstruction, the mean isokinetic peak torque of the involved limb was decreased in extension and internal rotation. The mean isokinetic peak torque of the involved limb in extension recovered 12 months after ACL reconstruction; however, the weakness in internal rotation persisted. The preoperative weakness of the involved limb in extension and internal rotation recovered in the male patients, but not in the female patients after postoperative rehabilitation. The peak torque of the involved limb in internal rotation was decreased in the STG group, but not in the ST group. Conclusions: The internal rotational torque was influenced by harvesting the semitendinosus and gracilis tendons after ACL reconstruction, especially in female patients and patients from whom the gracilis tendon was harvested. Semitendinosus and gracilis tendons are important for the internal rotation of the limb and it was difficult to compensate for this function. Thus, we recommend harvesting the semitendinosus tendon only if tendon quality is sufficient to further minimize harvesting morbidity.Arthroscopy: The Journal of Arthroscopic and Related Surgery, Vol 18, No 2 (February), 2002: pp 177–182