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Anatomical variations of nutrient foramina on the long bones of the upper extremities - Importance and application in everyday clinical practice

Anatomical variations of nutrient foramina on the long bones of the upper extremities -... Acta Marisiensis - Seria Medica 2023;69(1):55-60 DOI: 10.2478/amma-2023-0011 RESEARCH ARTICLE Anatomical variations of nutrient foramina on the long bones of the upper extremities - Importance and application in everyday clinical practice 1 2* 1 1 1 1 Lejla Dervisevic , Amela Dervisevic , Zurifa Ajanovic , Eldan Kapur , Almira Lujinovic , Alma Voljevica , Elvira Talović 1. Department of Anatomy, University of Sarajevo, Faculty of Medicine, Sarajevo, Bosnia and Herzegovina 2. Department of Human Physiology, University of Sarajevo, Faculty of Medicine, Sarajevo, Bosnia and Herzegovina Objectiv: Anatomic characterization of the nutrient artery of upper extremity long bones differs among the several textbooks on human anatomy. To elucidate the anatomical features of the nutrient foramen (NF) through which the nutrient arteries pass, we examined the morphol- ogy and topography of the NF on the diaphysis of the long bones of the upper extremities. Methods: A total of 150 (50 humeri, 50 radii, 50 ulnae) macerated and degreased adults, long bones of the upper extremities, unknown age, and gender were used as material in this study. The following parameters were determined for each bone: total number of NF, foramina index (FI), total bone length, position of the NF based on the FI value and the surface of the shaft/body of the bones, and obliquity of the nutritional canal (NC). Results: The largest number of NF was found on the middle third of the anteromedial side of the humerus diaphysis, with NC directed distally, that is, towards the elbow. Radius and ulna had predominantly one NF, on middle third of anterior surface, with NC directed proximally. Conclusion: This study provides ad- ditional and important information on the location and number of NF in the long bones of the upper and lower extremities in the Bosnian and Herzegovinian population. Keywords: humerus, radius, ulna, nutrient arteries, nutrient foramina Received 10 November 2022 / Accepted 21 February 2023 Introduction thritis or morphological changes within the body of each Long bones have three distinct vascular systems that are bone, and both epiphyses were complete and undamaged. interconnected. Nutrient arteries are the main source of Bones with evident damage were excluded from the study. blood for long bones, providing blood to the bone marrow Only NF on the body/shaft of bones was taken into ac- and internal two-thirds of the bone cortex [1,2]. Nutrient count. The NF has been observed macroscopically, using arteries enter the long bone diaphysis obliquely through a slightly raised edge of the NF and a shallow groove that one or more nutrient foramina (NF), leading into the nu- exists proximally to the NF, using a 6× hand magnifier. On trient canal (NC) [2]. each bone, within each group, the total number of macro- The importance of NF research is not only morphologi - scopically observed NF on the bony body was recorded. A cal, but also primarily clinical. Some pathological processes probe was passed through each hole to confirm its exist - in bone, such as developmental abnormalities, impaired ence of the hole. A thin rubber was wrapped around each healing of fractures, or acute osteomyelitis, are viewed to NF and photographed with a digital camera. be associated to changes in the degree of bone vasculari- The precise location of each NF is determined by cal - zation [3]. In view of the above, there is still a need for a culating the Foramina Index (FI), applying the Hughes better understanding of the number, topography and the formula [4]. direction of NC in the bones. The aim of our study was to determine variation regarding NF and NC in body of hu- FI = (DNF / TL) ×100 man long bones of the upper extremity. DNF = distance between the proximal end of the bone and Methods the nutrient foramina The research was design as an observational, descriptive TL = total length of the bone study, conducted on the total of 150 (50 humeri, 50 radii, 50 ulnae) macerated and degreased long bones of the up- In those bones that had two NF and more, the larg- per extremities of adults whose age and gender were not est of them is taken to calculate the FI. The total bone identified. All selected bones were anatomically preserved, length was noted individually for each bone by using the with no visible pathological changes. Specimens were se- osteometric board, within each group and expressed in lected based on the following criteria: no evident osteoar- centimetres (cm), according to the following [5]: humerus: the distance between the top of the humerus head and the superior point of the trochlea; radius: the distance between * Correspondence to: Amela Dervisevic E-mail: amela.dervisevic@mf.unsa.ba the proximal point of the radius head and the top of the 56 Acta Marisiensis - Seria Medica 2023;69(1) styloid process; ulna: the distance between the proximal difference for the continuous independent variables that point of the olecranon and the apex of the styloid process. accompany the normal distribution. The sample size was The whole length of each bone was divided into three calculated using a sample size calculator [8]. The results equal segments: zone I (proximal 1/3), zone II (middle were considered statistically significant ifthe   p value was 1/3) ,and zone III (distal 1/3). Nutritive foramina were less than 0.05. categorized into three groups according to the value of FI, as follows: Results – Type 1: FI lower than 33.33 - the NF is in the zone I The study included 50 humerus [20 (40.0%) right and 30 – Type 2: FI from 33.33 to 66.66 - the NF is in the (60.0%) left], 50 radius [24 (48.0%) right and 26 (52.0%) zone II left] and 50 ulna [27 (54.0%) right and 23 (46.0%) left]. – Type 3: FI larger than 66.66 - the NF is in the zone The average length for right humerus, radius and ulna were III [6]. 31.21 ± 2.27 cm, 23.41 ± 1.51 cm and 25.27 ± 2.02 cm, The location of each NF was determined by taking into respectively, and 31.30 ± 2.51 cm, 22.86 ± 1.53 cm, 24.85 account the sides of the bone shaft on which it is located ± 1.82 cm for left humerus, radius and ulna. There were and the distance from the edges of the bone. The surfaces not statistically significant differences in length between considered for each bone were: humerus - anteriorlateral, right and left extremity for humerus, radius and ulna (p anteriormedial and posterior; radius: anterior, lateral, and = 0.902, p> 0.05; p = 0.204, p> 0.05; p = 0.44; p> 0.05, posterior; ulna: anterior, medial and posterior [7]. respectively) (Table I). The size of the NF was determined by pulling a 25 G On the bones of the right side, one NF was observed in diameter (MedCare, Italy) needle through NF. NF with 13 (72.2%) humerus, 22 (91.7%) radius and 19 (70.4%), diameter smaller than 0.56 mm were considered second- and on the bones of the left side on 18 (60.0%) humerus, ary NF, while those 0.56 mm in diameter or larger were 21 (91.3%) radius and 19 (82.6%) ulna. Double NF were considered dominant NF. present on 5 (27.8%) humerus, 2 (8.3%) radius and 7 A thin, subcutaneous needle, which was passed through (25.9%) ulna from right side, and on 9 (30.0%) humerus, the NC was used to determine the direction of the canal 2 (8.7%) radius and 4 (17.4%) ulna from left side. Tri- (whether it is directed towards the proximal or distal end ple NF were observed on 3 (10.0%) left humerus and 1 of the bone) and its obliqueness. (3.7%) right ulna (Table II). On 39 (81.2%) humerus NF was located on the an- Statistical analysis teromedial surface [12 (66.7%) right and 27 (90.0%) The Social Sciences (SPSS) software version 13, (IBM, left]. On 8 (16.7%) humerus NF was located on the pos- Chicago, Illinois, United States of America) was used for terior surface [6 (33.3%) right and 2 (6.7%) left]. Only in the data analysis. Frequencies and percentages were used to one humerus on the left side, 1 (2.1%), NF was observed present values of categorical variables. The Chi-square test on the anterolateral side. On a total of 36 (76.6%) ra- or Fisher’s exact test was used to determine the significance dii NF were found on the anterior surface [21 (87.5%) of differences in frequency within relevant subgroups. The right and 15 (65.2%) left]. On the posterior surface NF association between categorical variables was tested with were observed at 11 (23.4%) radii [3 (12.5%) right and 8 the Chi-square test. Depending on the sample size, nor- (34.8%) left]. NFs were not found on the lateral surface. mality of distribution for continuous variables was identi- All 50 (100%) ulnas had NF located on anterior surface fied using the Kolmogorov-Smirnov or Shapiro-Wilk test. (Table III). Independent continuous variables with a normal distri- The frequency of NF on the anteromedial surface on bution are presented as mean and standard deviation (SD). right humerus was 30.8% and 69.2% for left. The fre - The Student’s  t test was used to test the significance of the quency of NF on the posterior surface 75.0% for right Table I. Length of humerus, radius and ulna on right and left extremity Humerus Radius Ulna Right (n=20) Left (n=30) Right (n=24) Left (n=26) Right (n=27) Left (n=23) Length (cm) 31.21±2.27 31.30±2.51 23.41±1.51 22.86±1.53 25.27±2.02 24.85±1.82 Min. 26.3 25.7 20.5 20.2 22.2 21.5 Max. 35.1 35.8 26.0 25.9 30.4 27.8 Table II. Total number NF on the humerus, radius and ulna Humerus Radius Ulna Number of NF Right (n=20) Left (n=30) Right (n=24) Left (n=26) Right (n=27) Left (n=23) n % n % n % n % n % n % 1 13 72.2 18 60.0 22 91.7 21 91.3 19 70.4 19 82.6 2 5 27.8 9 30.0 2 8.3 2 8.7 7 25.9 4 17.4 3 0 0.0 3 10.0 0 0.0 0 0.0 1 3.7 0 0.0 Total 18 100 30 100 24 100 23 100 27 100 23 100 Acta Marisiensis - Seria Medica 2023;69(1) 57 and 25.0% for left. Due to sample size, we did not analyze ulnae on both sides had NC directed toward the proximal the frequency of NF on the anterolateral surface on any end of the bone (Table IV). humerus. Analyzing the correlation between the extremity By analyzing the position of NF based on the value of side to which the humerus belongs and the position of the FI on the humerus, we found that in 46 (95.8%) humer- NF in relation to the body surfaces, we found a statistically us NF were located in the middle third of bone body [17 significant dependence ( χ2 = 5.496; p = 0.02, p <0.05). (94.4%) right and 29 (96.7%) left], in 1 (2.1%) humerus The frequency of NF on the anterior surface was 58.3% from right extremity had NF in the proximal third and in for right and 41.7% for left radius, and 27.3% for right 1 (2.1%) humerus fomr left extremity in the distal third of and 72.7% for left radius on posterior surface. Analyzing the bone body. At 18 (38.3%) radii NF were located in the the correlation between the extremity to which the radius proximal third [13 (54.2%) right and 5 (21.7%) left] and belongs and the position of the NF in relation to the de- at 29 (61.7%) in the middle third bone body [11 (45.8%) fined body surfaces, we did not determine the existence of right and 18 (78.3%) left]. On the ulna, in 12 (24.0%) a statistically significant dependence (p = 0.09, p> 0.05). bones the NF were located in the proximal third of the All ulnae on both the right and left sides had NF on the body [7 (25.9%) right and 5 (21.7%) left], while in 38 anterior body surface (results not present). 76.0%) of the bones NF were located in the middle third All humeri from the right and left extremities had NC of the body [20 (74.1%) of the right and 18 (78.3%) of directed toward the distal end of the bone, and all radii and the left] (Table V). Table III. The location of the NF on the surfaces of the bone body Right side Left side Bone Surface of body n % n % Anteromedial 12 66.7 27 90.0 Humerus Anterolateral 0 0.0 1 3.3 Posterior 6 33.3 1 6.7 Anterior 21 87.5 15 65.2 Radius Posterior 3 12.5 8 34.8 Lateral 0 0.0 0 0.0 Anterior 27 100.0 23 100.0 Ulna Posterior 0 0.0 0 0.0 Medial 0 0.0 0 0.0 Table IV. Obliquity of nutritional canal Bone epiphysis Proximal Distal Bone Right Left Right Left n % n % n % n % Humerus 0 0.0 0 0.0 18 100.0 30 100.0 Radius 24 100.0 23 100.0 0 0.0 0 0.0 Ulna 27 100.0 23 100.0 0 0.0 0 0.0 Table V. Position of NF based on Foramina Index Bone epiphysis Proximal 1/3 Middle 1/3 Distal 1/3 Bone Right Left Right Left Right Left n % n % n % n % n % n % Humerus 1 5.6 0 0.0 17 94.4 29 96.7 0 0.0 1 3.3 Radius 13 54.2 5 21.7 11 45.8 18 78.3 0 0.0 0 0.0 Ulna 7 25.9 5 21.7 20 74.1 18 78.3 0 0.0 0 0.0 Table VI. Correlation between the position of the NF based on the FI and the number of NF Bone epiphysis Proximal 1/3 Middle 1/3 Distal 1/3 Bone p Right Left Right Left Right Left n % n % n % n % n % n % Humerus 1 5.6 0 0.0 17 94.4 29 96.6 0 0.0 1 3.4 χ = 2.27 p=0.32 TOTAL 1 (2.1%) 46 (95.8%) 1 (2.1%) Radius 13 72.2 5 27.8 11 37.9 18 62.1 0 0.0 0 0.0 χ = 5.226 p=0.02 TOTAL 18 (38.3%) 29 (61.7%) 0 (0.0%) Ulna 7 77.3 5 22.7 20 52.6 18 47.4 0 0.0 0 0.0 χ = 3.579 p=0.059 TOTAL 22 (44.0%) 38 (56.0%) 0 (0.0%) 58 Acta Marisiensis - Seria Medica 2023;69(1) We did not find a statistically significant correlation be - merus belongs and the position of the opening in relation tween the position of NF based on the FI value and the to the sides of the bone diaphysis. Results from Pereire number of NF on the right and left humerus (χ2 = 2.27; et al, [16] and Gopalakrishna et al. [17]. showed that in p = 0.32, p> 0.05). Based on the FI value, the frequency 89.7% and 83.09% cases, respectively, NF on humerii are of NF on the proximal third of the bone body in the right located on anteromedial surface. A lower incidence of NF radius was 72.2% and on the left 27.8%. On the middle on the anteromedial surface was found in the study of So- third of the body the frequency was 37.9% in the right lanke et al. [18] and Kizilkanat et al. [19], which can be and 62.1% in the left radius. Statistically significant cor - due to race and national differences. According to FI value relation was observed between the position of NF based in 95.8% of the humerii NF was found in the middle third on the FI value and the number of NF on the radii of the of the body, which is in agreement with Ukoha et al. [6] right and left extremities (χ2 = 5.226; p = 0.02, p <0.05). and Murlimanju et al [13]. Based on our results, we con- The incidence of NF in the proximal third of the bone clude that the essential area of the bone body that should body was 77.3% on the right ulna and 22.7% on the left. be avoided during operative manipulations is middle third In the middle third, the incidence of NF was 52.6% for the of anteromedial side, because in most cases the humerus right ulna and 47.4% for the left. Correlation between the receives vascularization through NF located in that par- position of NF based on FI and the number of NF on the ticular zone. By avoiding the anteromedial aspect of the ulna of the right and left extremities was not statistically humerus during procedures, not only will the nutrient ar- significant ( χ2 = 3.579; p = 0.059, p> 0.05) (Table VI). tery be preserved, but other neurovascular structures also, while it is commonly know that the brachial plexus with Discussion all branches also pass on the medial aspect of a upper arm. Bone tissue is very rich in blood supply, with a developed Nutrient arteries for radius and ulna are often branches network that is different, not only in different bones, but of radial and ulnar artery [20]. Knowledge of variations of also in certain parts of the same bone. The anabolic and NF in the forearm is also important when interpreting ra- catabolic processes of the cells of the skeletal system de- diographs, because NC can appear on the image as a dark pend on the vascularization of the bone [9]. The data hairline, which can be very similar to fractures. Fractures about anatomical variations of the NF on the diaphysis of the body of the radius and ulna are quite common when of the long bones of the upper extremity, in the broad- a strong force acts on it, for example injuries in traffic ac - est sense of the word, as well as knowledge of its relation- cidents, falls from great heights or gunshot wounds. We ships with surrounding structures is of great importance in found that 94.0% of radii and in all 100% ulna, NF were everyday clinical practice, whether open or closed fracture present. Most of radii and ulnae had one NF (91.7% right reduction or about the preoperative procedure as part of and 91.3% left radii; 91.7% right and 91.3% left ulna), a bone transplant [10]. More variation can lead to an in- while two NF were observed in 8.3% right and 8.7% left creased risk in terms of injury to important neurovascular radii, and on 25.9% right and 17.4% left ulna. All ob- structures. The biological process of repairing traumatic or served NF on ulna, independent of a number were located surgically induced discontinuity in bone continuity may on anterior surface, while in radii they were located mostly be slow or not develop at all [11]. By knowing the area on also on anterior surface. The rest of NF on radii were where the nutritional artery enters the NC, surgeons can located on posterior surface. We did not determine the prevent further damage to it and minimize or reduce the existence of a statistically significant correlation between possibility of nonunion or delayed fracture healing [12]. the extremity to which the radius belongs and the posi- The humerus received a nutritional artery from a bra - tion of the NF on the radius in relation to the defined chial artery or deep brachial artery, or as a muscular branch sides. While the location of NF on the anterior surface on of the mentioned arteries [13]. In our study we found that the ulna varies from 82.2% [16], 76.62% [18] and 98.9% in 96% of humerii had NF, while 4.0% of humerii had no [21], number and location of NF on radii in our study is NF. The largest number had present one NF (72.2% right in agreement with results from others [19]. With reported and 60.0% left humerii), while two NF were recorded in incidences ranging from 2% to 10%, aseptic nonunion 27.8% right and 30.0% left humerii, and three NF were remains a important late complication of diaphyseal fore- observed in 10.0% left humerii. Analysing the available lit- arm fractures [22]. According to FI value, most of the radii erature, we found similar results. Results from Hemang et (61.7%) and ulnae (76.0%) had their NF in middle third al. [12], Sharma et al. [14], Chandrasekaran et al. [15] are of body, which is in agreement with other reports published in accordance with our results. The results of our and pre - in the literature [17]. The most common forearm fractures vious studies indicate that in most cases the humerus has in adults are the distal radius and ulna fractures, which are one NF, and that it receives vascularization in one place. primarily caused by a fall onto an extended hand [23]. On This is considered a vital, clinically significant point on the the forearm, the muscles cover and connect mainly to the diaphysis. In 81.2% cases these NF were located in antero- proximal half of the radius, but also the ulna. However, medial surface. We also recorded a statistically significant there are no significant muscle insertions on the distal half correlation between the side of the limb to which the hu- of the radius and ulna diaphysis, which corresponds to a Acta Marisiensis - Seria Medica 2023;69(1) 59 lack of NF in that part of the bone. Therefore, nonunion AL: Data curation, Investigation, Writing - original draft or delayed healing of fractures in the distal half of the di- AV: Data curation, Supervision, Validation, Visualiza- aphysis may be directly related to the lack of nutrient arter- tion, Writing - re-view & editing ies in these areas [24]. Although the periosteum of this area ET: Project administration, Validation, Visualization, receives part of the blood from the branches of the adjacent Writing - re-view & editing anterior and posterior interosseous artery, these branches All authors have accepted responsibility for the entire con- can often be damaged during sudden stretching of the in- tent of this manuscript and approved its submission terosseal membrane, especially during sudden pronation. A complete radiologic evaluation of a distal radius and Conflict of interest ulna fracture requires at least two views (posteroanterior None to declare. and lateral) of the wrist [25]. Oblique radiography is often required to fully assess the extent of the fracture, while NC References 1. Sendemir E, Cimen A. Nutrient foramina in the shafts of lower limb long that pass throughout the cortex can often mislead and be bones: situation and number. Surg Radiol Anat 1991;13:105-108. pronounced as a fracture. In our study, all NC on radii and 2. Al-Motabagani MAH. The arterial architecture of the human femoral diaphysis. J Anat Soc India. 2002;51:27-31. ulna were directed toward the proximal part, while NC in 3. Bonafede M, Espindle D, Bower AG. The direct and indirect costs humerii distally penetrated the cortical bone layer, which of long bone fractures in a working age US population.  J Med Econ. is in agreement with other results found in the literature 2013;16(1):169-178. 4. Hughes H. The factors determining the direction of the canal for the [17,26]. Because of such anatomical position of NF, safe nutrient artery in the long bones of mammals and birds. Acta Anat zones for procedures such as insertions of pin on ulna, dur- (Basel) 1952;15(3):261-280. ing pronation, would be along the whole axis between the 5. Caroll SE. A study of Nutrient Foramina of the Humeral Diaphysis. 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Biology of Bone: The Vasculature of the Skeletal openings and their location with regard to age and gender. System. Cold Spring Harb Perspect Med. 2018;8(7):a031559. 10. Sañudo JR, Vázquez R, Puerta J. Meaning and clinical interest of the Unfortunately, the study of anatomical variations has anatomical variations in the 21 st century. Eur. J. Anat. 2003;7:1-3. been neglected by recent trends in undergraduate medi- 11. Cahill DR, Leonard RJ. Missteps and masquerade in American medical cal studies, due to reduced dissection, reduced dissected academe: clinical anatomists call for action. Clin Anat. 1999;12(3):220- 222.  specimens, increased use of plastic preparations, computer 12. Joshi H, Doshi B, Malukar O A study of the nutrient foramina of the images, loss of experienced teachers and diminishing mor- humeral diaphysis. National Journal of Integrated Research in Medicine phological approach. The study of anatomical variations, 2011; 2(2):14-27. 13. 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Anatomical variations of nutrient foramina on the long bones of the upper extremities - Importance and application in everyday clinical practice

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Abstract

Acta Marisiensis - Seria Medica 2023;69(1):55-60 DOI: 10.2478/amma-2023-0011 RESEARCH ARTICLE Anatomical variations of nutrient foramina on the long bones of the upper extremities - Importance and application in everyday clinical practice 1 2* 1 1 1 1 Lejla Dervisevic , Amela Dervisevic , Zurifa Ajanovic , Eldan Kapur , Almira Lujinovic , Alma Voljevica , Elvira Talović 1. Department of Anatomy, University of Sarajevo, Faculty of Medicine, Sarajevo, Bosnia and Herzegovina 2. Department of Human Physiology, University of Sarajevo, Faculty of Medicine, Sarajevo, Bosnia and Herzegovina Objectiv: Anatomic characterization of the nutrient artery of upper extremity long bones differs among the several textbooks on human anatomy. To elucidate the anatomical features of the nutrient foramen (NF) through which the nutrient arteries pass, we examined the morphol- ogy and topography of the NF on the diaphysis of the long bones of the upper extremities. Methods: A total of 150 (50 humeri, 50 radii, 50 ulnae) macerated and degreased adults, long bones of the upper extremities, unknown age, and gender were used as material in this study. The following parameters were determined for each bone: total number of NF, foramina index (FI), total bone length, position of the NF based on the FI value and the surface of the shaft/body of the bones, and obliquity of the nutritional canal (NC). Results: The largest number of NF was found on the middle third of the anteromedial side of the humerus diaphysis, with NC directed distally, that is, towards the elbow. Radius and ulna had predominantly one NF, on middle third of anterior surface, with NC directed proximally. Conclusion: This study provides ad- ditional and important information on the location and number of NF in the long bones of the upper and lower extremities in the Bosnian and Herzegovinian population. Keywords: humerus, radius, ulna, nutrient arteries, nutrient foramina Received 10 November 2022 / Accepted 21 February 2023 Introduction thritis or morphological changes within the body of each Long bones have three distinct vascular systems that are bone, and both epiphyses were complete and undamaged. interconnected. Nutrient arteries are the main source of Bones with evident damage were excluded from the study. blood for long bones, providing blood to the bone marrow Only NF on the body/shaft of bones was taken into ac- and internal two-thirds of the bone cortex [1,2]. Nutrient count. The NF has been observed macroscopically, using arteries enter the long bone diaphysis obliquely through a slightly raised edge of the NF and a shallow groove that one or more nutrient foramina (NF), leading into the nu- exists proximally to the NF, using a 6× hand magnifier. On trient canal (NC) [2]. each bone, within each group, the total number of macro- The importance of NF research is not only morphologi - scopically observed NF on the bony body was recorded. A cal, but also primarily clinical. Some pathological processes probe was passed through each hole to confirm its exist - in bone, such as developmental abnormalities, impaired ence of the hole. A thin rubber was wrapped around each healing of fractures, or acute osteomyelitis, are viewed to NF and photographed with a digital camera. be associated to changes in the degree of bone vasculari- The precise location of each NF is determined by cal - zation [3]. In view of the above, there is still a need for a culating the Foramina Index (FI), applying the Hughes better understanding of the number, topography and the formula [4]. direction of NC in the bones. The aim of our study was to determine variation regarding NF and NC in body of hu- FI = (DNF / TL) ×100 man long bones of the upper extremity. DNF = distance between the proximal end of the bone and Methods the nutrient foramina The research was design as an observational, descriptive TL = total length of the bone study, conducted on the total of 150 (50 humeri, 50 radii, 50 ulnae) macerated and degreased long bones of the up- In those bones that had two NF and more, the larg- per extremities of adults whose age and gender were not est of them is taken to calculate the FI. The total bone identified. All selected bones were anatomically preserved, length was noted individually for each bone by using the with no visible pathological changes. Specimens were se- osteometric board, within each group and expressed in lected based on the following criteria: no evident osteoar- centimetres (cm), according to the following [5]: humerus: the distance between the top of the humerus head and the superior point of the trochlea; radius: the distance between * Correspondence to: Amela Dervisevic E-mail: amela.dervisevic@mf.unsa.ba the proximal point of the radius head and the top of the 56 Acta Marisiensis - Seria Medica 2023;69(1) styloid process; ulna: the distance between the proximal difference for the continuous independent variables that point of the olecranon and the apex of the styloid process. accompany the normal distribution. The sample size was The whole length of each bone was divided into three calculated using a sample size calculator [8]. The results equal segments: zone I (proximal 1/3), zone II (middle were considered statistically significant ifthe   p value was 1/3) ,and zone III (distal 1/3). Nutritive foramina were less than 0.05. categorized into three groups according to the value of FI, as follows: Results – Type 1: FI lower than 33.33 - the NF is in the zone I The study included 50 humerus [20 (40.0%) right and 30 – Type 2: FI from 33.33 to 66.66 - the NF is in the (60.0%) left], 50 radius [24 (48.0%) right and 26 (52.0%) zone II left] and 50 ulna [27 (54.0%) right and 23 (46.0%) left]. – Type 3: FI larger than 66.66 - the NF is in the zone The average length for right humerus, radius and ulna were III [6]. 31.21 ± 2.27 cm, 23.41 ± 1.51 cm and 25.27 ± 2.02 cm, The location of each NF was determined by taking into respectively, and 31.30 ± 2.51 cm, 22.86 ± 1.53 cm, 24.85 account the sides of the bone shaft on which it is located ± 1.82 cm for left humerus, radius and ulna. There were and the distance from the edges of the bone. The surfaces not statistically significant differences in length between considered for each bone were: humerus - anteriorlateral, right and left extremity for humerus, radius and ulna (p anteriormedial and posterior; radius: anterior, lateral, and = 0.902, p> 0.05; p = 0.204, p> 0.05; p = 0.44; p> 0.05, posterior; ulna: anterior, medial and posterior [7]. respectively) (Table I). The size of the NF was determined by pulling a 25 G On the bones of the right side, one NF was observed in diameter (MedCare, Italy) needle through NF. NF with 13 (72.2%) humerus, 22 (91.7%) radius and 19 (70.4%), diameter smaller than 0.56 mm were considered second- and on the bones of the left side on 18 (60.0%) humerus, ary NF, while those 0.56 mm in diameter or larger were 21 (91.3%) radius and 19 (82.6%) ulna. Double NF were considered dominant NF. present on 5 (27.8%) humerus, 2 (8.3%) radius and 7 A thin, subcutaneous needle, which was passed through (25.9%) ulna from right side, and on 9 (30.0%) humerus, the NC was used to determine the direction of the canal 2 (8.7%) radius and 4 (17.4%) ulna from left side. Tri- (whether it is directed towards the proximal or distal end ple NF were observed on 3 (10.0%) left humerus and 1 of the bone) and its obliqueness. (3.7%) right ulna (Table II). On 39 (81.2%) humerus NF was located on the an- Statistical analysis teromedial surface [12 (66.7%) right and 27 (90.0%) The Social Sciences (SPSS) software version 13, (IBM, left]. On 8 (16.7%) humerus NF was located on the pos- Chicago, Illinois, United States of America) was used for terior surface [6 (33.3%) right and 2 (6.7%) left]. Only in the data analysis. Frequencies and percentages were used to one humerus on the left side, 1 (2.1%), NF was observed present values of categorical variables. The Chi-square test on the anterolateral side. On a total of 36 (76.6%) ra- or Fisher’s exact test was used to determine the significance dii NF were found on the anterior surface [21 (87.5%) of differences in frequency within relevant subgroups. The right and 15 (65.2%) left]. On the posterior surface NF association between categorical variables was tested with were observed at 11 (23.4%) radii [3 (12.5%) right and 8 the Chi-square test. Depending on the sample size, nor- (34.8%) left]. NFs were not found on the lateral surface. mality of distribution for continuous variables was identi- All 50 (100%) ulnas had NF located on anterior surface fied using the Kolmogorov-Smirnov or Shapiro-Wilk test. (Table III). Independent continuous variables with a normal distri- The frequency of NF on the anteromedial surface on bution are presented as mean and standard deviation (SD). right humerus was 30.8% and 69.2% for left. The fre - The Student’s  t test was used to test the significance of the quency of NF on the posterior surface 75.0% for right Table I. Length of humerus, radius and ulna on right and left extremity Humerus Radius Ulna Right (n=20) Left (n=30) Right (n=24) Left (n=26) Right (n=27) Left (n=23) Length (cm) 31.21±2.27 31.30±2.51 23.41±1.51 22.86±1.53 25.27±2.02 24.85±1.82 Min. 26.3 25.7 20.5 20.2 22.2 21.5 Max. 35.1 35.8 26.0 25.9 30.4 27.8 Table II. Total number NF on the humerus, radius and ulna Humerus Radius Ulna Number of NF Right (n=20) Left (n=30) Right (n=24) Left (n=26) Right (n=27) Left (n=23) n % n % n % n % n % n % 1 13 72.2 18 60.0 22 91.7 21 91.3 19 70.4 19 82.6 2 5 27.8 9 30.0 2 8.3 2 8.7 7 25.9 4 17.4 3 0 0.0 3 10.0 0 0.0 0 0.0 1 3.7 0 0.0 Total 18 100 30 100 24 100 23 100 27 100 23 100 Acta Marisiensis - Seria Medica 2023;69(1) 57 and 25.0% for left. Due to sample size, we did not analyze ulnae on both sides had NC directed toward the proximal the frequency of NF on the anterolateral surface on any end of the bone (Table IV). humerus. Analyzing the correlation between the extremity By analyzing the position of NF based on the value of side to which the humerus belongs and the position of the FI on the humerus, we found that in 46 (95.8%) humer- NF in relation to the body surfaces, we found a statistically us NF were located in the middle third of bone body [17 significant dependence ( χ2 = 5.496; p = 0.02, p <0.05). (94.4%) right and 29 (96.7%) left], in 1 (2.1%) humerus The frequency of NF on the anterior surface was 58.3% from right extremity had NF in the proximal third and in for right and 41.7% for left radius, and 27.3% for right 1 (2.1%) humerus fomr left extremity in the distal third of and 72.7% for left radius on posterior surface. Analyzing the bone body. At 18 (38.3%) radii NF were located in the the correlation between the extremity to which the radius proximal third [13 (54.2%) right and 5 (21.7%) left] and belongs and the position of the NF in relation to the de- at 29 (61.7%) in the middle third bone body [11 (45.8%) fined body surfaces, we did not determine the existence of right and 18 (78.3%) left]. On the ulna, in 12 (24.0%) a statistically significant dependence (p = 0.09, p> 0.05). bones the NF were located in the proximal third of the All ulnae on both the right and left sides had NF on the body [7 (25.9%) right and 5 (21.7%) left], while in 38 anterior body surface (results not present). 76.0%) of the bones NF were located in the middle third All humeri from the right and left extremities had NC of the body [20 (74.1%) of the right and 18 (78.3%) of directed toward the distal end of the bone, and all radii and the left] (Table V). Table III. The location of the NF on the surfaces of the bone body Right side Left side Bone Surface of body n % n % Anteromedial 12 66.7 27 90.0 Humerus Anterolateral 0 0.0 1 3.3 Posterior 6 33.3 1 6.7 Anterior 21 87.5 15 65.2 Radius Posterior 3 12.5 8 34.8 Lateral 0 0.0 0 0.0 Anterior 27 100.0 23 100.0 Ulna Posterior 0 0.0 0 0.0 Medial 0 0.0 0 0.0 Table IV. Obliquity of nutritional canal Bone epiphysis Proximal Distal Bone Right Left Right Left n % n % n % n % Humerus 0 0.0 0 0.0 18 100.0 30 100.0 Radius 24 100.0 23 100.0 0 0.0 0 0.0 Ulna 27 100.0 23 100.0 0 0.0 0 0.0 Table V. Position of NF based on Foramina Index Bone epiphysis Proximal 1/3 Middle 1/3 Distal 1/3 Bone Right Left Right Left Right Left n % n % n % n % n % n % Humerus 1 5.6 0 0.0 17 94.4 29 96.7 0 0.0 1 3.3 Radius 13 54.2 5 21.7 11 45.8 18 78.3 0 0.0 0 0.0 Ulna 7 25.9 5 21.7 20 74.1 18 78.3 0 0.0 0 0.0 Table VI. Correlation between the position of the NF based on the FI and the number of NF Bone epiphysis Proximal 1/3 Middle 1/3 Distal 1/3 Bone p Right Left Right Left Right Left n % n % n % n % n % n % Humerus 1 5.6 0 0.0 17 94.4 29 96.6 0 0.0 1 3.4 χ = 2.27 p=0.32 TOTAL 1 (2.1%) 46 (95.8%) 1 (2.1%) Radius 13 72.2 5 27.8 11 37.9 18 62.1 0 0.0 0 0.0 χ = 5.226 p=0.02 TOTAL 18 (38.3%) 29 (61.7%) 0 (0.0%) Ulna 7 77.3 5 22.7 20 52.6 18 47.4 0 0.0 0 0.0 χ = 3.579 p=0.059 TOTAL 22 (44.0%) 38 (56.0%) 0 (0.0%) 58 Acta Marisiensis - Seria Medica 2023;69(1) We did not find a statistically significant correlation be - merus belongs and the position of the opening in relation tween the position of NF based on the FI value and the to the sides of the bone diaphysis. Results from Pereire number of NF on the right and left humerus (χ2 = 2.27; et al, [16] and Gopalakrishna et al. [17]. showed that in p = 0.32, p> 0.05). Based on the FI value, the frequency 89.7% and 83.09% cases, respectively, NF on humerii are of NF on the proximal third of the bone body in the right located on anteromedial surface. A lower incidence of NF radius was 72.2% and on the left 27.8%. On the middle on the anteromedial surface was found in the study of So- third of the body the frequency was 37.9% in the right lanke et al. [18] and Kizilkanat et al. [19], which can be and 62.1% in the left radius. Statistically significant cor - due to race and national differences. According to FI value relation was observed between the position of NF based in 95.8% of the humerii NF was found in the middle third on the FI value and the number of NF on the radii of the of the body, which is in agreement with Ukoha et al. [6] right and left extremities (χ2 = 5.226; p = 0.02, p <0.05). and Murlimanju et al [13]. Based on our results, we con- The incidence of NF in the proximal third of the bone clude that the essential area of the bone body that should body was 77.3% on the right ulna and 22.7% on the left. be avoided during operative manipulations is middle third In the middle third, the incidence of NF was 52.6% for the of anteromedial side, because in most cases the humerus right ulna and 47.4% for the left. Correlation between the receives vascularization through NF located in that par- position of NF based on FI and the number of NF on the ticular zone. By avoiding the anteromedial aspect of the ulna of the right and left extremities was not statistically humerus during procedures, not only will the nutrient ar- significant ( χ2 = 3.579; p = 0.059, p> 0.05) (Table VI). tery be preserved, but other neurovascular structures also, while it is commonly know that the brachial plexus with Discussion all branches also pass on the medial aspect of a upper arm. Bone tissue is very rich in blood supply, with a developed Nutrient arteries for radius and ulna are often branches network that is different, not only in different bones, but of radial and ulnar artery [20]. Knowledge of variations of also in certain parts of the same bone. The anabolic and NF in the forearm is also important when interpreting ra- catabolic processes of the cells of the skeletal system de- diographs, because NC can appear on the image as a dark pend on the vascularization of the bone [9]. The data hairline, which can be very similar to fractures. Fractures about anatomical variations of the NF on the diaphysis of the body of the radius and ulna are quite common when of the long bones of the upper extremity, in the broad- a strong force acts on it, for example injuries in traffic ac - est sense of the word, as well as knowledge of its relation- cidents, falls from great heights or gunshot wounds. We ships with surrounding structures is of great importance in found that 94.0% of radii and in all 100% ulna, NF were everyday clinical practice, whether open or closed fracture present. Most of radii and ulnae had one NF (91.7% right reduction or about the preoperative procedure as part of and 91.3% left radii; 91.7% right and 91.3% left ulna), a bone transplant [10]. More variation can lead to an in- while two NF were observed in 8.3% right and 8.7% left creased risk in terms of injury to important neurovascular radii, and on 25.9% right and 17.4% left ulna. All ob- structures. The biological process of repairing traumatic or served NF on ulna, independent of a number were located surgically induced discontinuity in bone continuity may on anterior surface, while in radii they were located mostly be slow or not develop at all [11]. By knowing the area on also on anterior surface. The rest of NF on radii were where the nutritional artery enters the NC, surgeons can located on posterior surface. We did not determine the prevent further damage to it and minimize or reduce the existence of a statistically significant correlation between possibility of nonunion or delayed fracture healing [12]. the extremity to which the radius belongs and the posi- The humerus received a nutritional artery from a bra - tion of the NF on the radius in relation to the defined chial artery or deep brachial artery, or as a muscular branch sides. While the location of NF on the anterior surface on of the mentioned arteries [13]. In our study we found that the ulna varies from 82.2% [16], 76.62% [18] and 98.9% in 96% of humerii had NF, while 4.0% of humerii had no [21], number and location of NF on radii in our study is NF. The largest number had present one NF (72.2% right in agreement with results from others [19]. With reported and 60.0% left humerii), while two NF were recorded in incidences ranging from 2% to 10%, aseptic nonunion 27.8% right and 30.0% left humerii, and three NF were remains a important late complication of diaphyseal fore- observed in 10.0% left humerii. Analysing the available lit- arm fractures [22]. According to FI value, most of the radii erature, we found similar results. Results from Hemang et (61.7%) and ulnae (76.0%) had their NF in middle third al. [12], Sharma et al. [14], Chandrasekaran et al. [15] are of body, which is in agreement with other reports published in accordance with our results. The results of our and pre - in the literature [17]. The most common forearm fractures vious studies indicate that in most cases the humerus has in adults are the distal radius and ulna fractures, which are one NF, and that it receives vascularization in one place. primarily caused by a fall onto an extended hand [23]. On This is considered a vital, clinically significant point on the the forearm, the muscles cover and connect mainly to the diaphysis. In 81.2% cases these NF were located in antero- proximal half of the radius, but also the ulna. However, medial surface. We also recorded a statistically significant there are no significant muscle insertions on the distal half correlation between the side of the limb to which the hu- of the radius and ulna diaphysis, which corresponds to a Acta Marisiensis - Seria Medica 2023;69(1) 59 lack of NF in that part of the bone. Therefore, nonunion AL: Data curation, Investigation, Writing - original draft or delayed healing of fractures in the distal half of the di- AV: Data curation, Supervision, Validation, Visualiza- aphysis may be directly related to the lack of nutrient arter- tion, Writing - re-view & editing ies in these areas [24]. Although the periosteum of this area ET: Project administration, Validation, Visualization, receives part of the blood from the branches of the adjacent Writing - re-view & editing anterior and posterior interosseous artery, these branches All authors have accepted responsibility for the entire con- can often be damaged during sudden stretching of the in- tent of this manuscript and approved its submission terosseal membrane, especially during sudden pronation. A complete radiologic evaluation of a distal radius and Conflict of interest ulna fracture requires at least two views (posteroanterior None to declare. and lateral) of the wrist [25]. Oblique radiography is often required to fully assess the extent of the fracture, while NC References 1. Sendemir E, Cimen A. Nutrient foramina in the shafts of lower limb long that pass throughout the cortex can often mislead and be bones: situation and number. Surg Radiol Anat 1991;13:105-108. pronounced as a fracture. 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Journal

Acta Marisiensis - Seria Medicade Gruyter

Published: Mar 1, 2023

Keywords: humerus; radius; ulna; nutrient arteries; nutrient foramina

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