Posterior cruciate ligament injury

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Posterior cruciate ligament injury
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Posterior cruciate ligament (center)
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The function of the posterior cruciate ligament (PCL) is to prevent the femur from sliding off the anterior edge of the tibia and to prevent the tibia from displacing posterior to the femur. Common causes of PCL injuries are direct blows to the flexed knee, such as the knee hitting the dashboard in a car accident or falling hard on the knee, both instances displacing the tibia posterior to the femur. [1]

Contents

Surgery to repair the posterior cruciate ligament is controversial due to its placement and technical difficulty. [2]

The posterior drawer test is one of the tests used by doctors and physiotherapists to detect injury to the PCL. An additional test of posterior cruciate ligament injury is the posterior sag test, where, in contrast to the drawer test, no active force is applied. Rather, the person lies supine with the leg held by another person so that the hip is flexed to 90 degrees and the knee 90 degrees. [3] The main parameter in this test is step-off, which is the shortest distance from the femur to a hypothetical line that tangents the surface of the tibia from the tibial tuberosity and upwards. Normally, the step-off is approximately 1 cm, but is decreased (Grade I) or even absent (Grade II) or inverse (Grade III) in injuries to the posterior cruciate ligament. [4]

Patients who are suspected to have a posterior cruciate ligament injury should always be evaluated for other knee injuries that often occur in combination with an PCL injuries. These include cartilage/meniscus injuries, bone bruises, ACL tears, fractures, posterolateral injuries and collateral ligament injuries.[ citation needed ]

Cause

In this medial view of the flexed knee, the lateral femoral condyle has been removed to reveal the structure of the PCL. Because the anterolateral bundle is stretched and the posteromedial bundle relaxed during flexion, excessive flexion in the form of hyperflexion causes tensile stress, shown in red, on the anterolateral bundle of the PCL that leads to PCL injury. PCL Flexion and Hyperflexion.png
In this medial view of the flexed knee, the lateral femoral condyle has been removed to reveal the structure of the PCL. Because the anterolateral bundle is stretched and the posteromedial bundle relaxed during flexion, excessive flexion in the form of hyperflexion causes tensile stress, shown in red, on the anterolateral bundle of the PCL that leads to PCL injury.

The PCL is located within the knee joint where it stabilizes the articulating bones, particularly the femur and the tibia, during movement. It originates from the lateral edge of the medial femoral condyle and the roof of the intercondyle notch [5] then stretches, at a posterior and lateral angle, toward the posterior of the tibia just below its articular surface. [6] [7] [8] [9]

In this medial view of the extended knee, the lateral femoral condyle has been removed to reveal the structure of the PCL. Because the posteromedial bundle is stretched and the anterolateral bundle relaxed during extension, excessive extension in the form of hyperextension causes tensile stress, shown in red, on the posteromedial bundle of the PCL that leads to PCL injury. PCL Extension and Hyperextension.png
In this medial view of the extended knee, the lateral femoral condyle has been removed to reveal the structure of the PCL. Because the posteromedial bundle is stretched and the anterolateral bundle relaxed during extension, excessive extension in the form of hyperextension causes tensile stress, shown in red, on the posteromedial bundle of the PCL that leads to PCL injury.

Although each PCL is a unified unit, they are described as separate anterolateral and posteromedial sections based on each section's attachment site and function. [10] During knee joint movement, the PCL rotates [9] [11] such that the anterolateral section stretches in knee flexion but not in knee extension and the posteromedial bundle stretches in extension rather than flexion. [7] [12]

The types of mechanisms that lead to PCL injury

In this position, the PCL functions to prevent movement of the tibia in the posterior direction [7] [13] and to prevent the tilting or shifting of the patella. [14] However, the respective laxity of the two sections makes the PCL susceptible to injury during hyperflexion, hyperextension, [15] and in a mechanism known as a dashboard injury. [9] Because ligaments are viscoelastic (p. 50 [16] ) they can handle higher amounts of stress only when the load is increased slowly (p. 30 [16] ). When hyperflexion and hyperextension occur suddenly in combination with this viscoelastic behavior, the PCL deforms or tears. [15] In the third and most common mechanism, the dashboard injury mechanism, the knee experiences impact in a posterior direction during knee flexion toward the space above the tibia. [10] [15] These mechanisms occur in excessive external tibial rotation and during falls that induce a combination of extension and adduction of the tibia, which is referred to as varus-extension stress, [10] or that occur while the knee is flexed. [15]

Diagnosis

Prevention

Knee injury

Knee injuries are very common among athletes as well as regular active people and can always be prevented. Ligament tears account for more than forty percent of knee injuries and the posterior cruciate ligament is considered one of the less common injuries. [17] Although it is less common, there are still important measures that can be taken in order to prevent this type of knee injury. Maintaining proper exercise and sport technique is crucial for injury prevention, which include not exceeding the body or not going over the proper range of motion of the knee, properly warming up and cooling down [18]

Quadriceps and hamstring ratio

Another important aspect of maintaining an injury free knee is having strong quadriceps and hamstring muscles because they help stabilize the knee. A low hamstring to quadriceps ratio is associated with knee injury and should be about eighty percent. [19] Some exercises to strengthen the quadriceps and hamstring muscles include leg curls, leg lifts, prone knee flexion with resistance band and knee extensions. Some stretches to help prevent injury to the posterior cruciate ligament include stretching of the hamstring muscles by extending the legs, toes pointing up, leaning forward until the stretch is felt and holding for a few seconds.

Exercises that strengthen the knee joints and the hamstrings include prone knee flexion. Where the knee flexes all the way back to the rear end, hold for about 10 seconds, then slowly lower to original position and repeat. Prone Knee Flexion.JPG
Exercises that strengthen the knee joints and the hamstrings include prone knee flexion. Where the knee flexes all the way back to the rear end, hold for about 10 seconds, then slowly lower to original position and repeat.

Exercises and stretches

In addition, balancing exercises have also been adopted because it has been proven that people with poor balance have more knee injuries than those with good balance. Wobble boards and Bosu balls are very common pieces of equipment used to balance and help prevent knee injuries as long as they are being used with trained personnel. [20] Another possible preventive measure is wearing knee straps to help stabilize the knee and protect it from injury, especially during demanding sports such as football. [21]

Treatment

It is possible for the PCL to heal on its own. Surgery is usually required in complete tears of the ligament. Surgery usually takes place after a few weeks, in order to allow swelling to decrease and regular motion to return to the knee. A procedure called ligament reconstruction is used to replace the torn PCL with a new ligament, which is usually a graft taken from the hamstring or Achilles tendon from a host cadaver. An arthroscope allows a complete evaluation of the entire knee joint, including the knee cap (patella), the cartilage surfaces, the meniscus, the ligaments (ACL & PCL), and the joint lining. Then, the new ligament is attached to the bone of the thigh and lower leg with screws to hold it in place. [22] PCL repair can also be undertaken. This differs from PCL reconstruction because a graft is not needed and the native PCL is reattached. [23]

Rehabilitation

Grades of injury

The posterior cruciate ligament is located within the knee. Ligaments are sturdy bands of tissues that connect bones. Similar to the anterior cruciate ligament, the PCL connects the femur to the tibia. There are four different grades of classification in which medical doctor's classify a PCL injury: Grade I, the PCL has a slight tear. Grade II, the PCL ligament is minimally torn and becomes loose. Grade III, the PCL is torn completely and the knee can now be categorized as unstable. Grade IV, the ligament is damaged along with another ligament housed in the knee e.g. ACL or posteromedial corner. [24] With these grades of PCL injuries, there are different treatments available for such injuries.

Rehabilitation options

It is possible for the PCL to heal on its own without surgery when it is in Grades I and II. PCL injuries that are diagnosed in these categories can have their recovery times reduced by performing certain rehabilitative exercises. Fernandez and Pugh(2012) found that following a PCL grade II diagnosis, a multimodal treatment that spanned over the course of 8 weeks consisting of chiropractic lumbopelvic manipulation, physiotherapy, and implementing an exercise program that emphasized in eccentric muscle contraction (lunges, 1-leg squats, and trunk stabilization) which proved to be an effective way to recover from the PCL injury. [25] For Grades III and IV, operative surgery is recommended or is usually needed. Grafts is the method when addressing PCL injuries that are in need of operative surgery. With grafts, there are different methods such as the tibial inlay or tunnel method. [26]

This picture shows the rehabilitative exercise called a "lunge" used to treat and strengthen PCL injuries. Lunges-2-2.png
This picture shows the rehabilitative exercise called a "lunge" used to treat and strengthen PCL injuries.

Epidemiology

Percentage of PCL to other knee injuries

According to [27] the posterior cruciate ligament injuries only account for 1.5 percent of all knee injuries (figure 2). If it is a single injury to the posterior cruciate ligament that requires surgery only accounted for 1.1 percent compared to all other cruciate surgeries but when there was multiple injuries to the knee the posterior cruciate ligament accounted for 1.2 percent of injuries.

National statistics

In 2010 national statistics was done by Agency for Healthcare Research and Quality for posterior cruciate ligaments injuries. They found that 463 patients were discharge for having some type of PCL injury. The 18- to 44-year-old age group was found to have the highest injuries reported (figure 1). One reason why this age group consists of the majority of injuries to the PCL is because people are still very active in sports at this age. Men were also reported having more injuries to the PCL (figure 3).[ citation needed ]

Recommendation for surgery

A grade III PCL injury with more than 10mm posterior translation when the posterior drawer examination is performed may be treated surgically. Patients that do not improve stability during physical therapy or develop an increase in pain will be recommended for surgery. [28]

Related Research Articles

<span class="mw-page-title-main">Knee</span> Leg joint in primates

In humans and other primates, the knee joins the thigh with the leg and consists of two joints: one between the femur and tibia, and one between the femur and patella. It is the largest joint in the human body. The knee is a modified hinge joint, which permits flexion and extension as well as slight internal and external rotation. The knee is vulnerable to injury and to the development of osteoarthritis.

<span class="mw-page-title-main">Hamstring</span> Any of the three muscles in the thigh

In human anatomy, a hamstring is any one of the three posterior thigh muscles between the hip and the knee.

<span class="mw-page-title-main">Posterior cruciate ligament</span> One of four major ligaments of the knee

The posterior cruciate ligament (PCL) is a ligament in each knee of humans and various other animals. It works as a counterpart to the anterior cruciate ligament (ACL). It connects the posterior intercondylar area of the tibia to the medial condyle of the femur. This configuration allows the PCL to resist forces pushing the tibia posteriorly relative to the femur.

<span class="mw-page-title-main">Anterior cruciate ligament</span> Type of cruciate ligament in the human knee

The anterior cruciate ligament (ACL) is one of a pair of cruciate ligaments in the human knee. The two ligaments are called "cruciform" ligaments, as they are arranged in a crossed formation. In the quadruped stifle joint, based on its anatomical position, it is also referred to as the cranial cruciate ligament. The term cruciate is Latin for cross. This name is fitting because the ACL crosses the posterior cruciate ligament to form an "X". It is composed of strong, fibrous material and assists in controlling excessive motion by limiting mobility of the joint. The anterior cruciate ligament is one of the four main ligaments of the knee, providing 85% of the restraining force to anterior tibial displacement at 30 and 90° of knee flexion. The ACL is the most frequently injured ligament in the knee.

<span class="mw-page-title-main">Lachman test</span> Clinical test to diagnose injury to ligaments

The Lachman test is a clinical test used to diagnose injury of the anterior cruciate ligament (ACL). It is recognized as reliable, sensitive, and usually superior to the anterior drawer test.

<span class="mw-page-title-main">Segond fracture</span> Avulsion fracture of the lateral tibial condyle of the knee

The Segond fracture is a type of avulsion fracture from the lateral tibial plateau of the knee, immediately below the articular surface of the tibia.

The drawer test is used in the initial clinical assessment of suspected rupture of the cruciate ligaments in the knee.

<span class="mw-page-title-main">Anterior cruciate ligament reconstruction</span> Surgical process

Anterior cruciate ligament reconstruction is a surgical tissue graft replacement of the anterior cruciate ligament, located in the knee, to restore its function after an injury. The torn ligament can either be removed from the knee, or preserved before reconstruction through an arthroscopic procedure. ACL repair is also a surgical option. This involves repairing the ACL by re-attaching it, instead of performing a reconstruction. Theoretical advantages of repair include faster recovery and a lack of donor site morbidity, but randomised controlled trials and long-term data regarding re-rupture rates using contemporary surgical techniques are lacking.

<span class="mw-page-title-main">Medial collateral ligament</span> Ligament on the inner side of the knee joint

The medial collateral ligament (MCL), also called the superficial medial collateral ligament (sMCL) or tibial collateral ligament (TCL), is one of the major ligaments of the knee. It is on the medial (inner) side of the knee joint and occurs in humans and other primates. Its primary function is to resist valgus forces on the knee.

<span class="mw-page-title-main">Semitendinosus muscle</span> One of the hamstring muscles; posterior part of the thigh

The semitendinosus is a long superficial muscle in the back of the thigh. It is so named because it has a very long tendon of insertion. It lies posteromedially in the thigh, superficial to the semimembranosus.

A meniscus transplant or meniscal transplant is a transplant of the meniscus of the knee, which separates the thigh bone (femur) from the lower leg bone (tibia). The worn or damaged meniscus is removed and is replaced with a new one from a donor. The meniscus to be transplanted is taken from a cadaver, and, as such, is known as an allograft. Meniscal transplantation is technically difficult, as it must be sized accurately for each person, positioned properly and secured to the tibial plateau. Its success also depends on donor compatibility, stability of the transplant, and long-term health of the underlying articular cartilage.

The knee examination, in medicine and physiotherapy, is performed as part of a physical examination, or when a patient presents with knee pain or a history that suggests a pathology of the knee joint.

<span class="mw-page-title-main">Cruciate ligament</span> Type of ligament shaped like an X

Cruciate ligaments are pairs of ligaments arranged like a letter X. They occur in several joints of the body, such as the knee joint, wrist joint and the atlanto-axial joint. In a fashion similar to the cords in a toy Jacob's ladder, the crossed ligaments stabilize the joint while allowing a very large range of motion.

<span class="mw-page-title-main">Anterior cruciate ligament injury</span> Ligament injury near the knee

An anterior cruciate ligament injury occurs when the anterior cruciate ligament (ACL) is either stretched, partially torn, or completely torn. The most common injury is a complete tear. Symptoms include pain, an audible cracking sound during injury, instability of the knee, and joint swelling. Swelling generally appears within a couple of hours. In approximately 50% of cases, other structures of the knee such as surrounding ligaments, cartilage, or meniscus are damaged.

<span class="mw-page-title-main">Patellar tendon</span> Tendon in the human knee

The patellar tendon is the distal portion of the common tendon of the quadriceps femoris, which is continued from the patella to the tibial tuberosity. It is also sometimes called the patellar ligament as it forms a bone to bone connection when the patella is fully ossified.

<span class="mw-page-title-main">Unhappy triad</span> Medical condition of the knee

The unhappy triad, also known as a blown knee among other names, is an injury to the anterior cruciate ligament, medial collateral ligament, and meniscus. Analysis during the 1990s indicated that this 'classic' O'Donoghue triad is actually an unusual clinical entity among athletes with knee injuries. Some authors mistakenly believe that in this type of injury, "combined anterior cruciate and medial collateral ligament disruptions that were incurred during athletic endeavors" always present with concomitant medial meniscus injury. However, the 1990 analysis showed that lateral meniscus tears are more common than medial meniscus tears in conjunction with sprains of the ACL.

<span class="mw-page-title-main">Meniscus tear</span> Rupturing of the fibrocartilage strips in the knee called menisci

A tear of a meniscus is a rupturing of one or more of the fibrocartilage strips in the knee called menisci. When doctors and patients refer to "torn cartilage" in the knee, they actually may be referring to an injury to a meniscus at the top of one of the tibiae. Menisci can be torn during innocuous activities such as walking or squatting. They can also be torn by traumatic force encountered in sports or other forms of physical exertion. The traumatic action is most often a twisting movement at the knee while the leg is bent. In older adults, the meniscus can be damaged following prolonged 'wear and tear'. Especially acute injuries can lead to displaced tears which can cause mechanical symptoms such as clicking, catching, or locking during motion of the joint. The joint will be in pain when in use, but when there is no load, the pain goes away.

Posterolateral corner injuries of the knee are injuries to a complex area formed by the interaction of multiple structures. Injuries to the posterolateral corner can be debilitating to the person and require recognition and treatment to avoid long term consequences. Injuries to the PLC often occur in combination with other ligamentous injuries to the knee; most commonly the anterior cruciate ligament (ACL) and posterior cruciate ligament (PCL). As with any injury, an understanding of the anatomy and functional interactions of the posterolateral corner is important to diagnosing and treating the injury.

<span class="mw-page-title-main">Tibial plateau fracture</span> Medical condition

A tibial plateau fracture is a break of the upper part of the tibia (shinbone) that involves the knee joint. This could involve the medial, lateral, central, or bicondylar. Symptoms include pain, swelling, and a decreased ability to move the knee. People are generally unable to walk. Complication may include injury to the artery or nerve, arthritis, and compartment syndrome.

<span class="mw-page-title-main">Medial knee injuries</span> Medical condition

Medial knee injuries are the most common type of knee injury. The medial ligament complex of the knee consists of:

References

  1. MedlinePlus Encyclopedia : Posterior cruciate ligament (PCL) injury
  2. Jonathan Cluett, M.D. (2003-08-05). "Injuries to the posterior cruciate ligament (PCL)". about.com. Retrieved 2006-11-11.
  3. Posterior Sag Test From The University of West Alabama, Athletic Training & Sports Medicine Center. Retrieved Feb 2011
  4. Cole, Brian; Miller, Mark J. (2004). Textbook of arthroscopy . Philadelphia: Saunders. p.  719. ISBN   0-7216-0013-1.
  5. Amis, A. A.; Gupte, C. M.; Bull, A. M. J.; Edwards, A. (2006). "Anatomy of the posterior cruciate ligament and the meniscofemoral ligaments". Knee Surgery, Sports Traumatology, Arthroscopy. 14 (3): 257–63. doi:10.1007/s00167-005-0686-x. PMID   16228178. S2CID   15246937.
  6. Girgis, FG; Marshall, JL; Monajem, A (1975). "The cruciate ligaments of the knee joint. Anatomical, functional and experimental analysis". Clinical Orthopaedics and Related Research. 106 (106): 216–31. doi:10.1097/00003086-197501000-00033. PMID   1126079.
  7. 1 2 3 Chandrasekaran, Sivashankar; Ma, David; Scarvell, Jennifer M.; Woods, Kevin R.; Smith, Paul N. (2012). "A review of the anatomical, biomechanical and kinematic findings of posterior cruciate ligament injury with respect to non-operative management". The Knee. 19 (6): 738–45. doi:10.1016/j.knee.2012.09.005. PMID   23022245.
  8. Edwards, A.; Bull, AM.; Amis, AA. (Mar 2007). "The attachments of the fiber bundles of the posterior cruciate ligament: an anatomic study". Arthroscopy. 23 (3): 284–90. doi:10.1016/j.arthro.2006.11.005. PMID   17349472.
  9. 1 2 3 Voos, J. E.; Mauro, C. S.; Wente, T.; Warren, R. F.; Wickiewicz, T. L. (2012). "Posterior Cruciate Ligament: Anatomy, Biomechanics, and Outcomes". The American Journal of Sports Medicine. 40 (1): 222–31. doi:10.1177/0363546511416316. PMID   21803977. S2CID   3524402.
  10. 1 2 3 Malone, A.A.; Dowd, G.S.E.; Saifuddin, A. (2006). "Injuries of the posterior cruciate ligament and posterolateral corner of the knee". Injury. 37 (6): 485–501. doi:10.1016/j.injury.2005.08.003. PMID   16360655.
  11. DeFrate, L. E. (2004). "In Vivo Function of the Posterior Cruciate Ligament During Weightbearing Knee Flexion". American Journal of Sports Medicine. 32 (8): 1923–8. doi:10.1177/0363546504264896. PMID   15572322. S2CID   42810072.
  12. Race, Amos; Amis, Andrew A. (1994). "The mechanical properties of the two bundles of the human posterior cruciate ligament". Journal of Biomechanics. 27 (1): 13–24. doi:10.1016/0021-9290(94)90028-0. PMID   8106532.
  13. Castle, Thomas H.; Noyes, Frank R.; Grood, Edward S. (1992). "Posterior Tibial Subluxation of the Posterior Cruciate-Deficient Knee". Clinical Orthopaedics and Related Research. 284 (284): 193–202. doi:10.1097/00003086-199211000-00027. PMID   1395293. S2CID   24386922.
  14. von Eisenhart-Rothe, Ruediger; Lenze, Ulrich; Hinterwimmer, Stefan; Pohlig, Florian; Graichen, Heiko; Stein, Thomas; Welsch, Frederic; Burgkart, Rainer (2012). "Tibiofemoral and patellofemoral joint 3D-kinematics in patients with posterior cruciate ligament deficiency compared to healthy volunteers". BMC Musculoskeletal Disorders. 13: 231. doi: 10.1186/1471-2474-13-231 . PMC   3517747 . PMID   23181354.
  15. 1 2 3 4 Janousek, Andreas T.; Jones, Deryk G.; Clatworthy, Mark; Higgins, Laurence D.; Fu, Freddie H. (1999). "Posterior Cruciate Ligament Injuries of the Knee Joint". Sports Medicine. 28 (6): 429–41. doi:10.2165/00007256-199928060-00005. PMID   10623985. S2CID   23746497.
  16. 1 2 Hamill, Joseph; Knutzen, Kathleen. (2009). Biomechanical basis of human movement. Philadelphia: Wolters Kluwer Health/Lippincott Williams and Wilkins. ISBN   978-0-7817-9128-1.[ page needed ]
  17. Rigby, J.; Porter, K. (2010). "Posterior cruciate ligament injuries". Trauma. 12 (3): 175–81. doi:10.1177/1460408610378792. S2CID   73260965.
  18. Sancheti, P.; Razi, M.; Ramanathan, E. B. S.; Yung, P. (2010). "Injuries around the knee - Symposium". British Journal of Sports Medicine. 44 (Suppl 1): i1. doi: 10.1136/bjsm.2010.078725.1 .
  19. Lucia, Alejandro; Daneshjoo, Abdolhamid; Mokhtar, Abdul Halim; Rahnama, Nader; Yusof, Ashril (2012). "The Effects of Injury Preventive Warm-Up Programs on Knee Strength Ratio in Young Male Professional Soccer Players". PLOS ONE. 7 (12): e50979. Bibcode:2012PLoSO...750979D. doi: 10.1371/journal.pone.0050979 . PMC   3513304 . PMID   23226553.
  20. Hrysomallis, C (2007). "Relationship between balance ability, training and sports injury risk". Sports Medicine. 37 (6): 547–56. doi:10.2165/00007256-200737060-00007. PMID   17503879. S2CID   27442246.
  21. Aaltonen, Sari; Karjalainen, Heli; Heinonen, Ari; Parkkari, Jari; Kujala, Urho M. (2007). "Prevention of sports injuries: systematic review of randomized controlled trials". Archives of Internal Medicine. 167 (15): 1585–92. doi:10.1001/archinte.167.15.1585. PMID   17698680.
  22. http://www.orthspec.com/pdfs/PCL-injuries.pdf%5B%5D
  23. Pisanu, Gabriele; Moura, João Luís; Saithna, Adnan; Sonnery-Cottet, Bertrand (June 2019). "Arthroscopic Repair of Proximal Posterior Cruciate Ligament Injuries in Pediatric Patients". Arthroscopy Techniques. 8 (7): e691–e695. doi:10.1016/j.eats.2019.03.003. PMC   6713858 . PMID   31467838.
  24. Saithna, Adnan; MacDonald, Peter B. (2015), Fanelli, MD, Gregory C. (ed.), "Combined Posterior Cruciate Ligament and Posteromedial Reconstruction", Posterior Cruciate Ligament Injuries, Springer International Publishing, pp. 209–217, doi:10.1007/978-3-319-12072-0_17, ISBN   9783319120713
  25. Fernandez, Matthew; Pugh, David (2012). "Multimodal and interdisciplinary management of an isolated partial tear of the posterior cruciate ligament: a case report". Journal of Chiropractic Medicine. 11 (2): 84–93. doi:10.1016/j.jcm.2011.10.005. PMC   3368977 . PMID   23204951.
  26. Wind, William M.; Bergfeld, John A.; Parker, Richard D. (2004). "Evaluation and Treatment of Posterior Cruciate Ligament Injuries: Revisited". The American Journal of Sports Medicine. 32 (7): 1765–75. doi:10.1177/0363546504270481. PMID   15494347. S2CID   22150465.
  27. Majewski et al.[ full citation needed ]
  28. (Mariani teal., 2002)[ full citation needed ]