Volar and Dorsal Blood Supply to the Lunate: A Cadaveric Study .

Orthopaedics

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Kienböck disease was first described by Kienböck1 in 1910 as softening of the lunate bone, occurring mainly in men between the ages of 20 and 40 years.2 Kienböck1 theorized that lunatomalacia resulted from the traumatic disruption of the lunate blood supply and the subsequent disturbance of the bony nutrition.2,3 Although multiple studies have examined the causative factors of this disease, the etiology remains unclear.4 Among the causative factors, various vascular and mechanical factors have been proposed, and it is thought that repetitive stress across the distal radioulnar joint can lead to vascular compromise and the development of this disease.

Theories regarding the mechanism of osteonecrosis of the lunate include compression fracture, repetitive loading, and trauma leading to disruption of the lunate blood supply.5–7 Many radiological and anatomic studies have reported a single dorsal artery in lunate specimens.8–11 However, confusion still exists regarding the arterial supply of the lunate and whether insufficiency of volar or dorsal blood supply is the major contributor to the etiology of Kienböck disease. Furthermore, no anatomic study has examined the nutrient arteries of lunate bone in a large number of skeletal specimens. The aim of this study was to examine and evaluate the nutrient foramina from the dorsal and volar aspects of lunate specimens to determine the extraosseous vascular pattern of blood supply to the lunate and thus the major contributor of blood supply to the lunate.

Materials and Methods

The Hamann-Todd Osteological Collection in Cleveland, Ohio, contains more than 3300 treated and dried human specimens, of which 950 specimens from 1900 wrists were randomly chosen for examination in no particular order. Only specimens in which nutrient artery foramen were clearly visible on the volar and dorsal surfaces of the lunate were included in the study. Specimens with severe degeneration of the lunate or with poor bone quality were excluded. Furthermore, to evaluate for any differences between right and left lunates, only specimens with matching corresponding contralateral lunates were included. Following these criteria, a total of 913 specimens were included in the study.

The specimens in the collection represent individuals who died between 1893 and 1938 in Cleveland, Ohio. This study included 750 men and 163 women, with ages ranging from 17 to 105 years. A total of 366 specimens were of Black race, and the remaining specimens were of White race.

The lunates were grossly examined subjectively twice by two examiners (V.C., N.S.B.). Interrater reliability was determined by comparing the results of 100 specimens randomly selected from within the study group. According to the anatomic location of the nutrient foramen, these were divided into volar and dorsal nutrient arteries (Figures 12). The number of foramen on the volar and dorsal aspects of each lunate was tabulated. Age, sex, and race data were collected. Specimens were divided into 7 age groups according to the decade of life, and the average number of foramen was calculated on the volar and dorsal aspect of the lunate in each group. Specimens also were examined according to the number of nutrient artery foramina.

Anterior view photographs of the nutrient artery foramina of the right and left lunate bones from the volar aspect in 2 randomly selected specimens: HTH 779 (A) and HTH 999 (B).

Figure 1:

Anterior view photographs of the nutrient artery foramina of the right and left lunate bones from the volar aspect in 2 randomly selected specimens: HTH 779 (A) and HTH 999 (B).

Posterior view photographs of the nutrient artery foramina of the right and left lunate bones from the dorsal aspect in 2 randomly selected specimens: HTH 779 (A) and HTH 999 (B).

Figure 2:

Posterior view photographs of the nutrient artery foramina of the right and left lunate bones from the dorsal aspect in 2 randomly selected specimens: HTH 779 (A) and HTH 999 (B).

Results

A total of 913 specimens were examined. Of the 913 specimens, 163 were female and 750 were male; 547 were White and 366 were Black (Table 1). In every age group, there was a greater number of male specimens than female specimens. In the groups younger than 35 years, there was a greater number of Black specimens than White specimens. In the groups older than 35 years, there was a greater number of White specimens than Black specimens (Table 1). There was a high interrater reliability of the reported findings (95%).

Age, Sex, and Racial Breakdown of the Lunate Specimens

Table 1:

Age, Sex, and Racial Breakdown of the Lunate Specimens

In the specimen sample, the average number of nutrient artery foramina was 1.63 and 1.65 on the right and left volar aspects, respectively, and 1.70 and 1.72 on the right and left dorsal aspects, respectively (Table 2). Interestingly, in specimens younger than 35 years, with the exception of left lunates in the 15 to 24 years age group, there was an increased number of nutrient artery foramina on the volar aspect compared with the dorsal side. However, for specimens older than 35 years, there were more nutrient artery foramina on the dorsal side compared with the volar aspect (Table 2). There was no significant difference in the average number of nutrient artery foramina between the right and left volar aspects (P=.59) and the right and left dorsal aspects (P=.61).

Average Number of Nutrient Artery Foramina on the Volar and Dorsal Aspects of the Right and Left Lunate Bones in the Sampled Specimens

Table 2:

Average Number of Nutrient Artery Foramina on the Volar and Dorsal Aspects of the Right and Left Lunate Bones in the Sampled Specimens

Forty-five percent to 48% of the specimens had 1 or fewer nutrient artery foramen on either aspect (Table 3), whereas 36% to 44% of the specimens had 2 nutrient artery foramina. Eight percent to 14% of the specimens had 3 nutrient artery foramina, and 5% or fewer of the specimens had 4 or more nutrient artery foramina. Interestingly, approximately 2 to 3 times more specimens had 4 or more nutrient artery foramina on the dorsal aspect of the lunate compared with the volar aspect.

Specimens Divided According to the Number of Nutrient Artery Foramina

Table 3:

Specimens Divided According to the Number of Nutrient Artery Foramina

Discussion

Although the etiology of Kienböck disease is unknown, various hypotheses have stated the etiology may be divided into traumatic and nontraumatic causes.4,5,12 The traumatic theory includes trauma directly to the vascular system, the osseous system (fracture theory), and the vascular nervous system.1–5,8,12,13 The trauma can be an injury to the radiocarpal ligaments, a vascular break, or a disruption of the sympathetic nervous system of the blood vessels.1,2,13 The compressive load to the wrist can result in a transverse fracture, which may interfere with the entrance of the arteries, leaving the proximal half of the lunate ischemic.9

Furthermore, repetitive microtraumas associated with the altered biomechanics in negative ulnar variants also may contribute to the vascular compromise and lunatomalacia that characterize Kienböck disease. Several studies14–16 have suggested that the biomechanical stress on the lunate exerted by the relatively longer radius and the load transmission across the distal radiocarpal joint increase in negative ulnar variants. Joji et al17 suggested that high muscle tone across ulnar negative wrists may account for the increase in abnormal stressors on the lunate. Lunates in negative ulnar variant wrists therefore may consistently be exposed to abnormally elevated strains and thus repetitive microtraumas and vascular trauma.

In addition, the “fault plate hypothesis” postulates that various factors cause rupturing of the trabeculae leading to multiple osseous lamina formation, which has the blocking effect of a wall and interferes with vascularity.18 The nontraumatic vascular theory describes embolus formation of the vessels, vasculitis, and corticosteroids in association with osteonecrosis of the lunate.5,7,12

From these theories, it is evident that traumatic and atraumatic events ultimately affect the blood supply of the lunate, leading to lunatomalacia. Several studies have reported that fewer than one-fourth of specimens have a single volar or dorsal blood supply to the lunate.8–11 It is possible that this single blood supply may lead to lunate necrosis. However, these studies all had small samples, and none of the studies was a cadaveric study. The precarious blood supply to the lunate places this bone at an increased risk of avascular necrosis. The purpose of the current study was to anatomically assess the vascularity of the lunate in a large sample of anatomic specimens and to evaluate the number and distribution of nutrient artery foramina in the lunate to better understand the extraosseous supply of the lunate.

Kienböck1 attributed the progressive nature of this disease to trauma that disrupts the blood supply, thereby affecting the associated ligaments of the wrist.2 Travaglini19 studied the extraosseous vascular anatomy of the carpus using injections of 4 specimens and reported the presence of volar and dorsal arterial arches. Lee9 examined 53 lunates injected with 50% micro-opaque suspension, clarified by the Spalteholz method, and concluded that 26% of the specimens were supplied by a single volar (15%) or dorsal (11%) vessel. Gelberman et al11,20 reported that fewer than one-fourth of specimens had a single volar or dorsal blood supply to the lunate.

Various other studies have examined the intraosseous blood supply of the lunate and reported that although there was a consistent volar supply to the lunate, the dorsal supply was inconsistent.10,11,16 Panagis et al10 demonstrated no dorsal blood supply in 20% of the lunates, whereas Stahl8 found that the blood supply of the lunate in 31 specimens was insufficient from the dorsal aspect with only 1 dorsal artery. This is in contrast to the current study, which found the lunate bone had 2 or more nutrient artery foramina on the dorsal aspect in more than 50% of the specimens.

In a study using latex injection and the Spalteholz method, Lamas et al21 reported that dorsal and volar arteries entered the bone in all of the specimens with a greater foramina number in the volar pole of the lunate than the dorsal pole. Vessels entered the dorsal bone through 1 to 3 foramina, whereas 1 to 5 nutrient vessels entered the volar pole through various ligament insertions. A more recent study by Dubey et al22 examined vascular foramina with arterial roentgenograms and found that greater than 91% specimens had more than 2 nutrient vessels. In the current study, only 15% to 25% of the specimens had more than 2 nutrient vessels.

There was wide variability in the findings of these studies because the samples were too small to reliably interpret the results. Furthermore, there was geographical variability in vascular patterns, yet the majority of these studies were conducted in European or Asian populations.22 In the current study, a large sample representative of the North American population was evaluated anatomically, and a greater number of nutrient artery foramina was found on the dorsal aspect than the volar aspect of the lunate bone. However, for specimens younger than 35 years, with the exception of left lunates in the 15- to 24-year group, a greater average number of nutrient artery foramina was found on the volar aspect of the lunate compared with the dorsal aspect.

A variety of factors may account for this finding. For example, the numbers of nutrient artery foramina may be altered with growth, due to age-related changes or changes in body composition. To the authors' knowledge, no other anatomic studies to date have examined changes in the numbers of nutrient arteries of the lunate over time or in association with growth- or age-related changes. Such a study could provide further insight into the discrepancy noted in the specimens from the group younger than 35 years compared with specimens from the group older than 35 years.

Furthermore, in comparing the specimens from the group younger than 35 years with those older than 35 years, the authors found that a greater proportion of the younger cohort was Black. In comparison, the cohort 35 years and older was primarily White. These racial differences may contribute to or account for the greater number of volar vs dorsal nutrient artery foramina in the specimens from the group younger than age 35 years. Studies to evaluate the genetic and ethnic contributing factors to lunate vascularity could further elucidate this question.

The current study found there were 2 to 3 times more specimens with 4 or more nutrient artery foramina on the dorsal side compared with the volar aspect. Finally, the authors evaluated for differences between right and left lunates in terms of average number of nutrient artery foramina, and no significant differences were found between right and left for both the volar and dorsal aspects of the lunates.

The current study had several drawbacks. Because it was a retrospective, cadaveric study, the number of extraosseous nutrient foramina could not be correlated with the intraosseous arterial supply of the lunate bone. Ideally, a prospective cohort study following a large group of patients with serial imaging and arthroscopic studies and fresh autopsy analysis after death would be required. Such a study would provide the most satisfactory answers to the current questions. However, such a study would be logistically difficult and financially prohibitive. Therefore, the current study provides the most reliable answers regarding the extraosseous anatomy of nutrient vessels, although further evidence needs to be corroborated with clinical studies. In addition, genetics and other external factors may predispose an individual to Kienböck disease, and these factors could not be taken into account in the current study.

Conclusion

This cross-sectional cadaveric study morphoanatomically compared a wide representative sample of the US population from adolescents to geriatric individuals. The nutrient artery foramina of the dorsal and volar aspect of lunate bone were quantified and examined. In contrast with previous studies, there seems to be a predominant arterial supply from the dorsal aspect compared with the volar aspect. Thus, from this study, it appears that injury to dorsal intercarpal and radiocarpal ligaments leading to the disruption of the dorsal arterial arches may be a major contributor to vascular insufficiency of lunate bone. Additional clinical, biomechanical, and fresh cadaveric studies are needed to substantiate this finding.

References

  1. Kienböck R. Über traumatische malazie des mondbeins und ihre folgezustände: entartungsformen und kompressionsfrakturen. Fortschr Geb Rontgenstr. 1910;16:77–103.
  2. Peltier LF. The classic. Concerning traumatic malacia of the lunate and its consequences: degeneration and compression fractures. Privatdozent Dr. Robert Kienböck. Clin Orthop Relat Res. 1980;(149):4–8. PMID:6996884
  3. Preiser G. Zur frage der typischen trauma-tischen ernabrungsstorungender kaurzen hand-und-fuss-wurzelknochen. Fortschr Geb Rontgenstr. 1911;17:360–362.
  4. Irisarri C. Aetiology of Kienböck's disease. J Hand Surg Br. 2004;29(3):281–287. doi:10.1016/J.JHSB.2004.01.006 [CrossRef] PMID:15142701
  5. Lamas C. Kienböck's Disease. Bosch; 2005:1–181.
  6. Lamas C. Osteotomía de sustracción lateral del radio en casos Zero Variant en la enfermedad de Kienböck [Doctoral thesis]. Autonomous University of Barcelona; 1998.
  7. Axhausen G. Nicht Malacie sondern Nek-rose des os lunatum. Capri. Arch Klin Chir. 1924;129:26.
  8. Stahl F. On lunatomalacia (Kienböck's disease): a clinical and roentgenological study, especially on its pathogenesis and the late results of immobilization treatment. Acta Chir Scand. 1947;95:126.
  9. Lee MLH. The intraosseus arterial pattern of the carpal lunate bone and its relation to avascular necrosis. Acta Orthop Scand. 1963;33(1–4):43–55. doi:10.3109/17453676308999833 [CrossRef] PMID:13929121
  10. Panagis JS, Gelberman RH, Taleisnik J, Baumgaertner M. The arterial anatomy of the human carpus: Part II. The intraosseous vascularity. J Hand Surg Am. 1983;8(4):375–382. doi:10.1016/S0363-5023(83)80195-6 [CrossRef] PMID:6886331
  11. Gelberman RH, Panagis JS, Taleisnik J, Baumgaertner M. The arterial anatomy of the human carpus: Part I. The extraosseous vascularity. J Hand Surg Am. 1983;8(4):367–375. doi:10.1016/S0363-5023(83)80194-4 [CrossRef] PMID:6886330
  12. Antuña-Zapico JM. Malacia del semilunar [Doctoral thesis]. University of Valladolid; 1966.
  13. Leriche R, Fontaine R. Contribution a l'etude de la maladie de Kienböck; son traitment par la sympathectomie périhumerale. Strasb Med. 1929;89:581.
  14. Bonzar M, Firrell JC, Hainer M, Mah ET, McCabe SJ. Kienböck disease and negative ulnar variance. J Bone Joint Surg Am. 1998;80(8):1154–1157. doi:10.2106/00004623-199808000-00008 [CrossRef] PMID:9730124
  15. Chen WS. Kienböck disease and negative ulnar variance. J Bone Joint Surg Am. 2000;82(1):143–144. doi:10.2106/00004623-200001000-00019 [CrossRef] PMID:10653093
  16. Afshar A, Aminzadeh-Gohari A, Yekta Z. The association of Kienbock's disease and ulnar variance in the Iranian population. J Hand Surg Eur Vol. 2013;38(5):496–499. doi:10.1177/1753193412469173 [CrossRef] PMID:23221184
  17. Joji S, Mizuseki T, Katayama S, Tsuge K, Ikuta Y. Aetiology of Kienböck's disease based on a study of the condition among patients with cerebral palsy. J Hand Surg Br. 1993;18(3):294–298. doi:10.1016/0266-7681(93)90044-G [CrossRef] PMID:8345252
  18. Watson HK, Guidera PM. Aetiology of Kienböck's disease. J Hand Surg Br. 1997;22(1):5–7. doi:10.1016/S0266-7681(97)80004-6 [CrossRef] PMID:9061513
  19. Travaglini F. Arterial circulation of the carpal bones. Bull Hosp Joint Dis. 1959;20:19–36. PMID:13839218
  20. Gelberman RH, Bauman TD, Menon J, Akeson WH. The vascularity of the lunate bone and Kienböck's disease. J Hand Surg Am. 1980;5(3):272–278. doi:10.1016/S0363-5023(80)80013-X [CrossRef] PMID:7400565
  21. Lamas C, Carrera A, Proubasta I, Llusà M, Majó J, Mir X. The anatomy and vascularity of the lunate: considerations applied to Kienböck's disease. Chir Main. 2007;26(1):13–20. doi:10.1016/j.main.2007.01.001 [CrossRef] PMID:17418764
  22. Dubey PP, Chauhan NK, Siddiqui MS, Verma AK. Study of vascular supply of lunate and consideration applied to Kienböck disease. Hand Surg. 2011;16(1):9–13. doi:10.1142/S021881041100500X [CrossRef] PMID:21348025

Age, Sex, and Racial Breakdown of the Lunate Specimens

Age group, yNo. of specimensNo.

SexRace

FemaleMaleWhiteBlack
15–24541737747
25–3411937824277
35–442003816210595
45–542122518713181
55–641511114011338
65–7410717909017
≥757018525911
Total913163750547366

Average Number of Nutrient Artery Foramina on the Volar and Dorsal Aspects of the Right and Left Lunate Bones in the Sampled Specimens

Age group, yNo. of specimensAverage no. of nutrient artery foramina

Right lunateLeft lunate


Volar aspectDorsal aspectVolar aspectDorsal aspect
15–24541.981.591.741.81
25–341191.731.711.801.68
35–442001.701.791.671.80
45–542121.551.751.651.64
55–641511.551.661.461.74
65–741071.551.611.661.60
≥75701.591.601.671.83
Total9131.63 (P=.59)1.70 (P=.61)1.65 (P=.59)1.72 (P=.61)

Specimens Divided According to the Number of Nutrient Artery Foramina

No. of foraminaNo. of right lunatesaNo. of left lunatesa


Volar aspectDorsal aspectVolar aspectDorsal aspect
0–1435 (48)407 (45)424 (46)421 (46)
2405 (44)376 (41)386 (42)328 (36)
373 (8)114 (12)98 (11)129 (14)
≥418 (2)34 (4)15 (2)45 (5)