Analysis of reciprocality of anatomical structures of the posterior surface of humerus during fetal period

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1 Archives of Perinatal Medicine 15(3), , 2009 ORIGINAL PAPER Analysis of reciprocality of anatomical structures of the posterior surface of humerus during fetal period ALICJA KĘDZIA 1, JOWITA WOŹNIAK 2, KRZYSZTOF DUDEK 3, MAREK RYBACZUK 4 Abstract The paper presents analysis of reciprocality of human anatomical structures of the posterior surface of humerus during fetal period. Material and methods: analysis was carried out for 140 preparations of upper extremities of foetuses (including 34 female ones) with age between 15 and 28 week (CR lengths: mm). Applied methods comprised anatomical and preparation methods as well as image acquisition with the help of digital camera, system Scion Image Alpha and statistical tests like Pearson chi square, Shapiro-Wilk and Kruskal-Wallis ones. Paper examines reciprocality for any upper limb and it determines (under the system / the following relations: position of radial nerve in medial head of triceps brachii muscle parameter Tn; position of deep brachial artery in medial head of triceps brachii muscles parameter Tt; overlapping of deep brachial artery onto radial nerve parameter Nt). Results: Types of above vessel-nervous structures were determined. Sex dimorphism and symmetry were examined. There is statistically important dependence of appearance of some morphological types for the same foetuses. The position of radial nerve at medial head of triceps brachii muscle (Tn) correlates with position of deep brachial artery at medial head of triceps brachii muscle (Tt). Moreover the position of deep brachial artery at medial head of triceps (Tt) correlates with overlapping of deep brachial artery onto radial nerve. Conclusions: It has been found that the best anatomical variant is position of radial nerve at medial head of triceps brachii muscle, which takes place in 74.3% of examined cases. This layout is important during fracture of humerus. Key words: fetus, humerus, radial nerve, deep brachial artery, triceps brachii muscle, reciprocality Introduction Reciprocality describes mutual position of separate anatomical structures what was applied for analysis of posterior surface of humerus during fetal period. In the available literature there are no papers describing relations between topography of radial nerve and deep brachial artery as well as its main branch medial collateral artery. Papers devoted to foetuses concern the length of humerus. This problem was examined in: [1, 6, 12, 14, 34]. Analysis of the length of humerus was applied in evaluation of hypotrophy of foetuses in examined populations as the important indicator of exchange of motherfoetus [22]. Development of humerus and its ratio comparing with scapula during early embryonic evolution has been described in [18, 19] examined length of died adults, the material comprised 24 extremities, 11 of them were used in examinations of vessel system whereas remaining ones allowed to determine the architecture of triceps brachii muscles. Examinations concerning tricepses brachii muscles in autopsical material of adults were carried out by [9, 21, 23, 32]. Radial nerve in foetuses was described by [15] who examined 200 humeral plexuses of foetuses. This research is devoted to radial nerve within humeral segment during fetal period. Bono et al. [3] measured length of radial nerve for 50 died adults. [31] described clinical cases of damaged radial nerve during intra muscle injections into back or lateral part of humerus or during fracture of humerus. Authors describe also existence of fibrous, arc like strip of lateral head of triceps brachii muscles pressing radial nerve [4, 10] papers dependence between layout of radial nerve and risk of injury during surgical operation in the posterior surface of humerus examining died adults. There are not many papers indicating examinations of deep brachial artery in died adults, mainly the place of branching from humeral artery: [7, 2, 13, 25, 27, 35, 36]. Observations of [24] carried for 71 foetuses between 12 and 40 week showed good supply with oxygen flowing 1 Department of Anatomy, Wrocław School of Medicine, Wrocław, Poland 2 Department of Anatomy, Wrocław School of Medicine, Wrocław, Poland 3 Institute of Machines Design and Operation, Technical University of Wrocław, Wrocław, Poland 4 Institute of Materials Science and Applied Mechanics, Technical University of Wrocław, Wrocław, Poland

2 160 A. Kędzia, J. Woźniak, K. Dudek, M. Rybaczuk through brachial artery and subsequent branching, these vessel have high index of flow resistance. The paper aimed at analysis of reciprocality of vessels nerves and muscles between deep brachial artery close laying radial nerve and medial head of triceps brachii muscles during fetal period, determination of sex dimorphism and symmetry of above structures. Reciprocality has practical influence by a broken humerus this causes the possibility to damage the radial nerve and vessels. Material and methods Material consisted of 140 preparations of foetus humeruses with the age week (34 female ones), with crown-rump lengths (CRL): mm. The morphological age of foetuses was determined according to the dependence described by Carlson [5]. Applied methods comprised anatomical and preparational ones as well as image acquisition with the help of digital camera. Measurements were carried under system Scion Image Alpha [8, 11, 16]. Photos were prepared with the help of programs Gimp 2.2 and Bimp Statistical analysis like Pearson chi square, Shapiro-Wilk and Kruskal-Wallis ones was performed under packages of Statistica [17, 20, 33]. Results The description of somatic features is shown in Table1, the structure of the age of the examinated material is presented on histogram (Fig. 1). Symmetry, sex dimorphism and mutual topographical relations between radial nerve, deep brachial artery and medial head of triceps brachii muscle were examined. For every limb the following relations (Tab. 2) were examined under the / system: position of radial nerve in medial head of triceps brachii muscle (parameter Tn), position of deep brachial artery in medial head of triceps brachii muscle (parameter Tt), overlapping of profunda brachii artery onto radial nerve (Nt). Topographical relations were determined. Three types of vessel-nerve were found. The key criterion was the position of nerve and vessel, distances between these structures were examined in variants (Fig. 2). Table 1. Somatic characteristics of examined foetuses and results of comparison. Examined feature of foetus p value Examined feature of foetus Length CRL [mm]: Mean x Standard deviation SD Median x med Minimal value x min Maximal value x max Mass [g]: Mean x Standard deviation SD Median x med Minimal value x min Maximal value x max p value I a I b II a II b III a III b Table 2. Number (ratios) of foetus humerus versus morphological types, places and sex Type Tn Tt Nt Total Number of foetuses 21 (20%) 15 (10.7%) 10 (7.1%) 51 (36.4%) 37 (26.4%) 6 (4.3%) 140 (100%) Left position 8 (5.7%) 9 (6.4%) 5 (3.6%) 26 (18.6%) 19 (13.6%) 3 (2.1%) 70 (50.0%) Right position 13 (9.3%) 6 (4.3%) 5 (3.6%) 25 (17.9%) 18 (12.9%) 3 (2.1%) 70 (50.0%) Male 7 (5.0%) 7 (5.0%) 10 (7.1%) 34 (24.3%) 14 (10.0%) 2 (1.4%) 74 (52.9%) Female 14 (10% 8 (5.7%) 0 (0%) 17 (12.1%) 23 (16.4%) 4 (2.9%) 66 (47.1%)

3 Analysis of reciprocality of anatomical structures of the posterior surface of humerus during fetal period 161 Fig. 1. Histogram of the examinated fetus against a background of normal distribution (GA gestational age) Fig. 2. Morphological types: radial nerve (A), deep brachial artery (B) and medial head of triceps brachii muscle (C) Fig. 3. Comparison of numbers of appearance of reciprocality Tn (position of radial nerve at medial head of triceps brachii muscle), depending on body side, sex of foetus and results of chi-square test

4 . of observations. of observations 162 A. Kędzia, J. Woźniak, K. Dudek, M. Rybaczuk Fig. 4. Comparison of numbers of appearance of reciprocality Tn (position of radial nerve at medial head of triceps brachii muscle), depending on foetus age and results of chi-square test chi 2 v = 1 = 0.33; p = chi 2 v = 1 = 16.12; p = Fig. 5. Comparison of numbers of appearance of reciprocality Tt (position of deep humeral vessel at medial head of triceps brachii muscle), depending on body side, sex of foetus, foetus age and results of chi-square test

5 Analysis of reciprocality of anatomical structures of the posterior surface of humerus during fetal period 163 Table 3. Matrix of Spearman correlation coefficients Tn Tt Nt Tn Tt Nt Important coefficients are indicated at the level p < 0.05 Tn position of radial nerve in medial head of triceps brachii muscles Tt position of deep brachial artery in medial head of triceps brachii muscles Nt overlapping of deep brachial artery onto radial nerve Fig. 6. Comparison of distance between radial nerve and deep brachial artery of humerus in the half length of humerus ant in shoulders with various morphological types and results of Kruskal-Wallis test A type I a (15.0% foetuses) refers to layout of radial nerve and deep brachial artery outside of medial head of triceps brachii muscle, brachii vessels and nerve were separated. In the type I b (10.7%) vessel touches nerve also behind of muscle head. In the type II a (7.1%) vessel and nerve are situated at muscle but at great distance. The type II b (36.4%) is the most frequent one. Then vessel close to nerve lays outside of humerus and they are situated at medial head triceps brachii muscle. In the type IIIa (26.4%) the observed vessel is situated close to nerve at bone, in turn nerve laid at medial head of triceps brachii muscle. The type IIIb was found in 4.3% of foetuses. Then radial nerve and deep brachial artery were separated, however nerve was situated at muscle but artery laid in the groove for radial nerve. Analysis of dichotomous parameters in the examined material, the radial nerve was situated at the medial head of triceps brachii muscle in 104 preparations of humerus (74.3%). In 45 foetuses (64.3%) there was noticeable symmetry. In 8 foetuses (11.4%) the nerve was localized on the left side and in 6 (8.6%) was on the right. In the female foetuses Tt location could be found in 44 preparations (42.3%) and in the males in 60 (57.7%), Fig. 3. Comparison of populations of appearance of reciprocality Tn (the layout of radial nerve at medial head of triceps brachii muscle Tn), according to body side and foetus sex as well as results of chi-square test showed that none of body side was privileged (Fig. 3). This feature occurs more frequently for male foetuses but the difference is not statistically important (p > 0.05). Appearance of this type is also not connected with the age of foetus (Fig. 4). There is statistically important dependence of appearance of some morphological types for the same foetuses (Tab. 2, Fig. 5). The position of radial nerve at medial head of triceps brachii muscle (Tn) correlates with position of deep brachial artery at medial head triceps brachii of triceps brachii (Tt). Moreover the position of deep brachial artery at medial head of triceps brachii (Tt) correlates with overlaping of deep brachial artery onto radial nerve (Tab. 3). Among 104 humeruses

6 164 A. Kędzia, J. Woźniak, K. Dudek, M. Rybaczuk with Tn as much as 61 (59%) have also Tt, in contrast for 71 humeruses with Nt as much as 51 (72%) have also Tt. The mean distances between radial nerve and deep brachial artery ant were noticeably greater in variants a for morphological types I and II (Fig. 6). Discussion The analysis of the available literature indicated lack of studies on reciprocality of the radial nerve on the foetus material, fulfilment of this gap consitutes the main purpose of this paper. Appearance of morphological variants of vessels was a subject of various papers found in literature [29], Rodriquez-Niedenfuehr t al. the paper of 2001, analysed variants of upper limb for 192 died adults. They also present their own classification of variants on the basis of literature review. The paper contains single information about variants of deep brachial artery in anastomosis in elbow fossa with brachioradial artery, branching of radial recurrent artery from deep brachial artery as well as anastomosis of radial vessel. Subsequent papers of the same authors [28, 30] contain interesting remarks about appearance of morphological variants during embryonic evolution. According to Singer theory of 1933, which Rodriguez-Niederfuehr et al. [29] consider to be the adult forms of vessels may appear during early embryonic angiogenesis, in turn, median artery, then the ulnar and the superficial brachial and finally anastomosis in the cubital area between the brachial and superficial brachial arteries which originate from initial part of radial artery, whereas the proximal segment reduces to final forms appearing for adults. [26] describes the Singer theory. Newer theories assume that vessel model of upper limb begins to differentiate from primary plexus of vessels, from proximal part to distant one and in forearm with back-front direction due to growth and differentiation of some capillaries and regression of others. He suggests that survival, growth and differentiation of vessels forms from initial plexus which normally allows appearance of normal vessels or disappearing entails risk of appearance of variants of vessels in terminal form of vessels. The authors examined 112 human embryos between 12 and 23 stage of evolution (CRL: mm). During 13 stage (CRL: 5-6 mm) of embryonic evolution, the plexus of vessels begins complicated process of maturation through magnification and differentiation in chosen channels. This remodelling begins from aorta and it is continued from proximal parts towards distant ones. At 15 stage (CRL: mm) the differentiation approaches axillary and subclavian arteries, at 17 stage (CRL: mm) it reaches elbow finally approaching forearm during 18 stage (CRL: mm). During 21 stage (CRL: mm), the final vessel model of upper limb has been formed, the same as for adults [31]. Conclusions It has been found that the best anatomical variant is position of radial nerve at medial head of triceps brachii muscle (types II and III), what takes place in 74.3% of examined cases. This layout is important during fracture of humerus. References [1] R. Bareggi, V. Grill, M. Zweyer et al. (1994) The growth of long bones in human embryological and fetal upper limbs and its relatonship to other developmental patterns. Anat. Embryol. (Berl.) 189: [2] G. Bodner, W. Buchberger, M. Schocke et al. (2001) Radial nerve palsy associated with humerus shaft fracture: evaluation with IS initial experience. Radiology 3: [3] C. Bono, M.G. Grossman, N. Hochwald, P. Tornetta (2000) Radial and axillary nerves anatomic considerations for humeral fixation. Clin. Orthop. Relat. Res. 373: [4] D. Carlan, J. Pratt, J.M. Patterson et al. (2007) The radial nerve in the brachium: an anatomic study in human cadavers. J. Hand. Surg. (Am) 32: [5] B.M. Carlson, Human embriology and developmental. Mosby, St. Louis 1996: 450. [6] M. Chen, Y.H. Lee, Y.H. Lam et al. (2007) First-trimester fetal limb biometry in Chinese population. Prenat. Diagn. 27: [7] N. Coskun, L. Sarikcioglu, B.O. Donmez, M. Sindel (2005) Arterial, neural and muscular variations in the upper limb. Folia Morphol. 64: [8] W. Derkowski, A. Kędzia (2001) Application of computer image processing systems scion for Windows 98 and elf in evaluation of development of anterior cranial fossa during fetal period. VII Computer aided scientific research, Wrocław, 2001: Wroclaw Scientific Research Society (in Polish). [9] P.A. Fabrizio, R.F. Clemente (1997) Variations in the triceps brachii muscle. Clin. Anat. 10: [10] P. Fleming, B. Lenehan, R. Sankar et al. (2004) One-third, two-thirds: relationship of the radial nerve to the lateral intermuscular septum in the arm. Clin. Anat. 17: [11] M. Glonek, A. Kędzia (2001) Evaluation of usability of programs elf and scion for Windows 98 in morphological analysis of lateral ventricle during human fetal period. VII Computer aided scientific research, Wrocław, 2001: Wrocław Scientific Research Society (in Polish). [12] D.J. Gray, E. Gardner (1969) The prenatal development of the human humerus. Am. J. Anat. 124: [13] S. Jayakumari, R. Gayatri, A. Jyoti (2006) Unilateral double axillary and double brachial arteries. Embryological bais and clinical implifikations. Int. J. Morphol. 24:

7 Analysis of reciprocality of anatomical structures of the posterior surface of humerus during fetal period 165 [14] P. Jeanty (1983) Fetal limb biometry. Radiology 147: [15] K.A. Karabulut, T. Ziylan, M. Büuyükmumcu et al. (2006) Brachial plexus variations in human fetuses. Neurosurgery 19: [16] A. Kędzia, W. Derkowski, M. Glonek (2006) Structure and function of skull on the basis of computer image analysis during fetal period. XIII Computer aided scientific research, Wrocław 2006: Wrocław Scientific Research Society. (in Polish). [17] S.M. Kot, J. Jakubowski, A. Sokołowski (2007) Statistics. StatSoft Polska, Warszawa. [18] W.H. Lewis ( ) The development of the arm in man. Am. J. Anat. 1: [19] A.Y. Lim, B.P. Pereira, V.C. Kumar (2001) The long head of the triceps brachii as a free functioning muscle transfer. Plast. Reconst. Surg. 107: [20] M. Maliński, J. Szymszal (1999) Modern mathematical statistics in medicine and calculation sheets. Silesian Academy of Medicine, Katowice. [21] P.R. Manske (1977) Compression of the radial nerve by the triceps muscle: a case report. J. Bone Joint Surg. Am. 59: [22] A. Mazur (2005) Characteristics of terminal wisps of placentas in foetal hipotrophy. PhD thesis, Wrocław School of Medicine, Wroclaw School of Medicine 2005: 9-19 (in Polish). [23] M.T. Merin, R.N. Soubhagya, K. Ashwin et al. (2008) Four-headed biceps and triceps brachii muscles with neurovascular variation. Anat. Sci. Int. 83: [24] J. Morales-Rosello (2001) Doppler Sonographic study of fetal brachial and umbilical artery blood flow during pregnancy. J. Clin. Ultrasound, 29: [25] V.V. Patnaik, G. Kalsey, R. Singla. (2001) Bifurcation of axillary artery in its 3rd part a case report. J. Anat. Soc. India 50: [26] V.V.G. Patnaik, G. Kalsey, R. Singla (2002) Branching pattern of brachial artery a morphological study. J. Anat. Soc. India 51: [27] T. Peştemalci, Y. Ince, M. Yildirim et al. (2007) A study of variable origins of arteries in arm. Eur. J. Plast. Surg. 30: [28] M. Rodriguez-Niedenfuehr, G. J. Burton, J. Deu, J.R. Sanudo (2001) Variations of the arterial pattern in the upper limb revisited: a morphological and statistic study, with a review of the literature. J. Anat. 199: [29] M. Rodriguez-Niedenfuehr, T. Vazquez, L. Nearn et al. (2001) Variations of the arterial pattern in the upper limb revisited: a morphological and statistic study, with a review of the literature. J. Anat. 199: [30] M. Rodriguez-Niedenfuehr, T. Vazquez, I.G. Parkin, J.R. Sanudo (2003) Arterial patterns of the human upper limb: update of anatomical variations and embryological development. Eur. J. Anat. Suppl. 1: [31] P. Solzi, M. Lotem, A. Fried et al. (1971) Radial palsy following muscular effort. A nerve compression syndrome possibly related to a fibrous arch of the lateral head of the triceps. J. Bone Joint Surg. 53B: [32] S. R. Tubbs, E.G. Salter, J.W. Oakes (2003) Triceps brachii muscle demonstrating a fourth head. Clin. Anat. 53: [33] C. Watała (2002) Biostatistics application of statistical methods in research in medicine. a-medica press, Bielsko-Biała [34] W. Wożniak, M. Bruska (2006) The lenght of the humerus in human embryos at developmental stages Folia Morphol. 62: [35] K. Yoshinaga, I. Tanii, K. Kodoma (2003) Superficial brachial artery crossing over the ulnar and median nerves from posterior to anterior: embryological significance. Anat. Sci. Int. 78: [36] N. Yoyota, S. vakov (2004) Unilateral double axillary artery. Clin. Anat. 17: J Alicja Kędzia Department of Anatomy Wrocław School of Medicine Wrocław, Chałubińskiego 6a, Poland

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