Journal of Pharmaceutical Research International 33(61A): 33-41, 2021; Article no.JPRI.82863 ISSN: 2456-9119 (Past name: British Journal of Pharmaceutical Research, Past ISSN: 2231-2919, NLM ID: 101631759) Correlation of Long Bone Length and Number of Nutrient Foramina – Importance in Everyday Clinical Practice Lejla Dervišević a*#, Amela Dervišević b†, Zurifa Ajanović a#, Ilvana Hasanbegović a‡, Aida Sarač Hadžihalilović a‡, Eldan Kapur a‡ And Emina Dervišević c‡ a Department of Anatomy, Faculty of Medicine, University of Sarajevo, Sarajevo, Bosnia and Herzegovina. b Department of physiology, Faculty of Medicine, University of Sarajevo, Sarajevo, Bosnia and Herzegovina. c Department of Forensic Medicine, Faculty of Medicine, University of Sarajevo, Sarajevo, Bosnia and Herzegovina. Authors’ contributions This work was carried out in collaboration among all authors. Author LD designed the study, wrote the protocol and methods of study and wrote the first draft of the manuscript. Author AD performed the statistical analysis and data curation. Author ZA managed the analyses of the study author IH managed the literature searches and visualization of final manuscript. Author ASH managed conceptualization. Author EK managed supervision and validation. Author ED managed Writing- review and editing. All authors read and approved the final manuscript. Article Information DOI: 10.9734/JPRI/2021/v33i61A35113 Open Peer Review History: This journal follows the Advanced Open Peer Review policy. Identity of the Reviewers, Editor(s) and additional Reviewers, peer review comments, different versions of the manuscript, comments of the editors, etc are available here: https://www.sdiarticle5.com/review-history/82863 Received 20 October 2021 Original Research Article Accepted 27 December 2021 Published 28 December 2021 ABSTRACT Aims: Nutrient artery is the principal source of nutrition to the long bones. The topography of nutrient foramina on long bones is well known, but it has not yet been established whether the number of nutritive foramina (NF) is related to total bone length. The objective of the present study was to study the correlation of total number of nutrient foramina and long bone length of upper and lower limb to provide detailed data on such features. _____________________________________________________________________________________________________ # Associate profesor, † 2Assistant Profesor, ‡ Full profesor, *Corresponding author: E-mail: lejla.dervisevic@mf.unsa.ba;  Dervišević et al.; JPRI, 33(61A): 33-41, 2021; Article no.JPRI.82863 Study Design: A cross-sectional, descriptive study Place and Duration of Study: Department of anatomy, Medical Faculty University of Sarajevo. Study duration was 3 months. Methodology: In the present study, 300 adult human long bones of the upper (50 humeri, 50 radii, 50 ulnae) and lower (50 femora, 50 tibiae, 50 fibulae) limbs were investigated to determine the number of their nutrient foramina. The nutrient foramina were identified analysed macroscopically and total number of nutrient foramina for each bone was recorded. Total length of each bone within a group was recorded. Statistical analysis was performed to determine correlation between total bone length and number of nutrient foramina, by using SPSS version 17.0 for Windows. Results: A statistically significant negative correlations between the left humerus length and the number of NF was found. A positive correlations between the length of the right radius and the number of NF, the left ulna length and the number of NF, the right ulna length and the number of NF were found. A negative correlations between the length of the left radius and the number of NF and between right humerus length and number of NF were found. A positive correlation between the length of the right and left femur and the number of NF were found. A negative correlation between the length of left tibia and the number of NF was found, as well as negative correlation between the length of right and left fibula and number of NF. Conclusion: Total bone length is not related to the number of nutrient foramina. The number of nutrient foramina does not depend on the total length of the bone, which is important when assessing the success of grafts for transplantation on long bones in taller people. Keywords: Nutritive foramina; long bones; morphology; number. 1. INTRODUCTION through which nutritional arteries pass. Each long bone has its own nutritional artery, and Numerous developmental factors, both some bones often have more. They are usually genotypic and phenotypic, can influence the the collateral blood vessels of the limb arteries. development of skeletons and soft tissues, and lead to minor or major deviations from the most Many scholars have studied the NF of long common anatomical features called variations bones [5,6,7]. Most of these studies were [1]. Accurate knowledge of the variables in the performed many years ago, and mainly focused structure of the human body is important to on the number, location, and direction of the improve diagnostic and therapeutic effects, nutrient foramina. especially in the field of modern imaging diagnostic techniques such as The position and the direction of the NF are echocardiography, magnetic resonance imaging, known to vary in human long bones. The blood computed tomography, endoscopy and supply of the femur has been described in detail laparoscopy. by Lexer, Kuliga and Turk [8]. Nutrient foramina of the femur and humerus have been Adequate blood supply is the basis of bone investigated by Lutken [9], Kinoze [10], Laing vitality and growth, resistance to infection and [11] and Carroll [12]. Nutrient foramina on the the ability to heal fractures [2]. Apart from the radius and ulna have been studied by Shulman importance of nutrient arteries in fracture [13]. Hughes [14] has formulated an interesting healing, some other conditions of bones, such as explanation for the normal and abnormal developmental abnormalities and hematogenic direction of the NF and has stated that osteomyelitis, are also dependent on the anomalous canals are frequent in the femur, but vascular system of bones [3]. rarely occur in the radius and seldom in the other bones. None of the above workers has studied Long bones have three different vascular all the long bones together and it was thought systems that are interconnected. These are the worth while to reinvestigate the problem in all the metaphysical complex, the nutritional system long bones. Few studies were specific to and the periosteal capillary system. The correlation of number of NF and length of the nutritional system is the largest, supplying blood long bones in upper and lower extremities [15]. to the bone marrow and the inner two-thirds of the bone cortex [4]. Nutrient foramina (NF) are Given the significance of NF in clinical and the largest openings in the trunk of long bones morphological fields, it is of paramount 34  Dervišević et al.; JPRI, 33(61A): 33-41, 2021; Article no.JPRI.82863 importance that the characteristics of NF are studied on an ongoing basis in order to validate Humerus: distance between the top of the head the findings from literature and to explore and of the humerus and the superior point of the discover new findings that can play a critical role trochlea. in the field of medical science. In this study, we systematically observed the number of NF and Radius: distance between the proximal point of their relation to the length of the specific bones. the radius head and the top of the styloid process. 2. MATERIALS AND METHODS Ulna: distance between the proximal point of the The research was conducted at the Department olecranon and the apex of the styloid process. of Human Anatomy, Faculty of Medicine, University of Sarajevo. The bones examined Femur: distance between the proximal point of were obtained from the osteology collection held the head and the most distal lying point on the in the Department of Anatomy, Faculty of medial condyle. Medicine, University of Sarajevo. It is a cross- sectional, descriptive study, in which we Tibia: distance between the proximal point of the analysed and interpreted the results obtained by medial condyle and the tip of the medial observation on bone material. The material for malleolus. this study consisted of a total of 300 macerated and degreased adults, long bones of the upper Fibula: distance between the top of the head and lower extremities (50 humerus, 50, radius, and the top of the lateral malleolus 50 ulna, 50 femur, 50 tibia, 50 fibula). Sample size was determined using sample size 2.1 Statistical Analysis calculator [16]. All selected bones were anatomically preserved, with no noticeable Categorical data were expressed in frequencies pathological changes. Bones with noticeable (n) and relevant percentage (%). Mean and damage were not included in the study. The age standard deviation (SD) were determined for the and gender of the people from whom the bones independent continuous variables that follow the originate were not known. Specimens were normal distribution. The significance of the selected according to the following criteria that difference for the continuous independent no significant osteoarthritis or morphological variables that accompany the normal distribution changes within the body of each bone, and that was tested by Student t-test. The correlations bone body and both epiphysis were intact. The between the variables were assessed by following parameters were analysed on the Spearman’s test. Values of p <0.05 were bones of each group: total number of NF and considered statistically significant. Data were bone length. analyzed using Statistical Package for the Social Sciences (SPSS) software version 13 (IBM, Our study was guided by methods of counting Chicago, Illinois, USA). NF from previous studies [17-19]. On each bone, within each group, the total number of 3. RESULTS AND DISCUSSION macroscopically observed NF on the diaphysis was recorded. A probe was passed through An average length for right humerus was 31.21 ± each hole to confirm the existence of the 2.27 cm, and 31.30 ± 2.51 cm for left humerus, foramina. Nutritive foramina were observed only with no statistically significant differences on the diaphyses of long bones. They were between the length of humerus from right and observed macroscopically, using a 6x hand left extremity (p = 0.902; p> 0.05). The right magnifier. On the diaphyses, the NF were radius had an average length of 23.41 ± 1.51 observed by a slightly raised edge of the cm, while left radius had an average length of foramina and by a shallow groove existing 22.86 ± 1.53 cm. The determined difference proximally from the NF. between the average radius length of the right and left extremities was not statistically Determination of total bone length was done significant (p = 0.204; p> 0.05). An average individually for each bone by using an length for right ulna was 25.27 ± 2.02 cm, and osteometric board [12], within each group and 24.85 ± 1.82 cm for left one, with no statistically expressed in centimeters (cm), according to the significant differences between the length of right following: and left ulna (p = 0.44; p> 0.05) (Table 1). 35  Dervišević et al.; JPRI, 33(61A): 33-41, 2021; Article no.JPRI.82863 One NF was observed in 13 (72.2%) right the right ulna length and the number of NF were humerus and 18 (60.0%) left humerus, in 22 found. A negative correlations between the (91.7%) right and 21 (91.3%) left radius, and in length of the left radius and the number of NF 19 (70.4%) right and 19 (82.6%) left ulna. Two and between right humerus length and number NF were recored in 5 (27.8%) right and 9 of NF were found. The identified correlations (30.0%) left humerus, in 2 (8.3%) right and in 2 were not statistically significant (Table 3). (8.7%) left radius, and in 7 (25.9%) right and 4 (17.4%) left ulna. Three NF were found on 3 An average length of right femur, tibia and fibula (10.0%) left humerus and 1 (3.7%) right ulna were 44.30 ± 2.4 cm, 35.73 ± 2.33 cm and 35.20 (Table 2). ± 2.7 cm, respectively, while an average length of left femur, tibia and fibula were 44.38 ± 2.7 A statistically significant negative correlations cm, 36.26 ± 1.85 cm and 35.52 ± 2.1 cm, between the left humerus length and the number respectively. There were no statistically of NF was found. A positive correlations between significant differences between right and left the length of the right radius and the number of femur (p = 0.915; p> 0.05), tibia (p = 0.403; p> NF, the left ulna length and the number of NF, 0.05) and fibula (p = 0.645; p> 0.05) (Table 4). Table 1. Length of humerus, radius and ulna on right and left extremity (cm) Length (cm) Humerus Radius Ulna Right (n=20) Left (n=30) Right (n=24) Left (n=26) Right (n=27) Left (n=23) 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. Max. Min. Max. Min. Max. Min. Max. Min. Max. Min. Max. 26.3 35.1 25.7 35.8 20.5 26.0 20.2 25.9 22.2 30.4 21.5 27.8 Table 2. Representation of number NF on the humerus, radius and ulna Number Humerus Radius Ulna of NF Right Left Right Left Right Left n % n % n % n % n % n % 1 13 72.2 18 60.0 22 91.7 21 91.3 19 70.4 19 % 2 5 27.8 9 30.0 2 8.3 2 8.7 7 25.9 4 82.6 3 0 0.0 3 10.0 0 0.0 0 0.0 1 3.7 0 17.4 Total 18 100.0 30 100.0 24 100.0 23 100.0 27 100.0 23 100.0 Table 3. Correlation between the length of the humerus, radius and ulna with number of NF Variable Number of NF Right r = - 0.143 * Humerus Left r = - 0.438 Right r = 0.059 Radius Left r = - 0.208 Right r = 0.110 Ulna Left r = 0.020 r – correlation coefficient * – p < 0,05 Table 4. Length of femur, tibia and fibula on right and left extremity (cm) Femur Tibia Fibula Length (cm) Right (n=29) Left (n=21) Right (n=31) Left (n=19) Right (n=25) Left (n=25) 44,30±2,4 44,38±2,7 35.73±2.33 36.26±1.85 35.20±2.7 35.52±2.1 Min. Max. Min. Max. Min. Max. Min. Max. Min. Max. Min. Max. 38,0 48,5 39,2 49,0 31.5 39.9 33.3 40.0 29.6 39.5 30.3 39.9 36  Dervišević et al.; JPRI, 33(61A): 33-41, 2021; Article no.JPRI.82863 One NF was recorded in 1 (32.1%) right and 10 nutritional canal. But so far, no systematic (52.6%) left femur, in 31 (100.0%) right and 16 studies have been done to examine whether the (84.2%) left tibia and in 19 (90.5%) right and 21 number of NF is correlated with bone length. (100.0%) left fibula. Two NF were recorded in 16 Most of the long bones in our study had one NF, (57.1%) right and 8 (42.1%) left femur, in 3 which is in agreement with the results of other (15.8%) left tibia and in 2 (9.5%) right fibula. authors [23-25]. Three NF were recorded in 3 (10.7%) right and in 1 (5.3%) left femur (Table 5). Knowing the position of the NF is useful not only during bone surgeries, but also has forensic A positive correlation between the length of the significance. In forensic medicine, it is possible right and left femur and the number of NF were to estimate the total length of the bone if the ratio found. The found correlations were not between the total length of the bone and the statistically significant. A negative correlation distance of the NF from both ends of the bone is between the length of left tibia and the number of known. This is especially important because NF was found, as well as negative correlation bones broken at one or both ends are between the length of right and left fibula and sometimes sent for examination [26]. In our number of NF. The found correlations were not study, a statistically significant negative statistically significant. Due to the size of the correlation was found between the length of the sample, we were not able to examine the left humerus and the number of NF (r = -0.438). correlation between the length of the right tibia and the number of NF (Table 6). Houssaye et al. [27] revealed a trend for nutrient canals to be generally more numerous and The knowledge about the location of the NF is relatively thinner in less elongated bones. As for highly important because of the increased the canal diameter, the diameters taken at mid- chances of damage to the nutrient artery during length or at the periphery co-vary. These open or closed surgical procedures. The parameters are also the only one to co-vary arrangement of the diaphyseal NF in the long between the humeri and the femora. This shows bones usually follows a defined pattern in which that the diameter of the canals is rather the foramina are located on the flexor surface of constrained. Seymour et al. [28] suggested a link the bones (anterior in the upper limbs and between blood vessel circumference and posterior in the lower) [20-22]. metabolic rates (larger blood vessels to service higher flow rates) and thus that the diameter of Most of the studies done so far on NF of long the nutrient canals would be linked to the bones of upper and lower limb have examined physiology of the organisms. The femur is the NF position, number, and direction of the longest bone in the human body and in our study Table 5. Representation of number NF on the femur, tibia and fibula Femur Tibia Fibula Number Right Left Right Left Right Left of NF n % n % n % n % n % n % 1 9 32.1 10 52.6 31 100.0 16 84.2 19 90.5 21 100.0 2 16 57.1 8 42.1 0 0.0 3 15.8 2 9.5 0 0.0 3 3 10.7 1 5.3 0 0.0 0 0.0 0 0.0 0 0.0 Total 28 100.0 19 100.0 31 100.0 19 100.0 21 100.0 21 100.0 Table 6. Correlation between the length of the femur, tibia and fibula with number of NF Variable Number of NF Right r = 0.219 Femur Left r = 0.260 Right / Tibia Left r = - 0.030 Right r = - 0.164 Fibula Left r = - 0.138 r – correlation coefficient * – p < 0,05 37  Dervišević et al.; JPRI, 33(61A): 33-41, 2021; Article no.JPRI.82863 the largest number of bones with two NF was Larger prospective studies are needed, found in this group, which is confirmed by therefore, to provide clinical data regarding positive correlations between the length of the gender and sidedness and also to explore the femur and the number of NF. Only 15.8% of left effect of shaft length on the number of NF within tibia had two NF in our study, while the study of the shaft. These results are in agreement with Haidara et al. [29] where they found more double our results, where we did not found statistically foramina in tibia. That might be significant correlation with bone length and explained by the superiority of CT scan used in number of NF. The absence of NF in long bones his study, in comparison to utilizing the is well known [32,37]. It was reported that in naked eye and magnifying lenses in our instances where the nutrient foramen is absent, study. the bone is likely to be supplied by periosteal arteries [15]. In our study we found more frequent double NF in long bones of lower extremity, in compering to In the setting of reconstructive surgery, the use upper extremity long bones. Long bones of lower of vascularized allografts has been proven extremity are longer, but in our study there was effective albeit challenging [38]. Vascularized not statistically significant correlation between bone and joint allograft survival is strongly length of femur, tibia or fibula with number of NF. contingent upon preservation of periosteal and Larger number of NF in femur, tibia and fibula intraosseous blood supply [35]. Hence, graft can be due to the higher force and stress preservation methods as well as surgical transmitted to the lower limbs than to the upper techniques depend upon a thorough limbs in view of the weight bearing and understanding of vascular anatomy. The results locomotive functions of the lower limbs and the of our study showed that there is no statistically relatively finer functions of the upper limbs, significant association between bone length and thereby warranting a more robust blood supply the number of NF, except in humerus. The for the lower limb bones, resulting in a larger correlation between length in human long bones numer of the NF. This finding however has to be and number of NF has been reported in only a confirmed by more extensive studies and with a few papers. Because there have been no larger sample size. Neil J. [30] found found that reference data on the long bones to date, the the dominant NF occurred more frequently in the results reported here are novel data. This should lower limbs than in the upper limbs, and the of use to surgeons [39,40]. In case the graft secondary foramina were more common in the should be taken from a very tall person, it is upper limbs, which were statistically significant. considered that there will be no disruption of the In cases with many NF, although the fracture vascular integrity of the long bone, because may damage some blood vessels, the residual regardless of the length of the bone itself, other intact blood vessels may still be able to provide nutritional arteries can supply bone. In bone the required blood supply to the bone. Although grafts, the nutrient blood supply is crucial and it NF number has not been linked to age, should be preserved in order to promote the multivariate logistic analysis revealed a fracture healing hence a sound knowledge of the significant interaction between the effects of topography and morphometry of nutrient gender and sidedness on foramen number foramina is of importance to orthopaedic (p < 0.01) in a study of NF within the human surgeons and oncologists. femoral diaphysis [31]. Patake [15] and Mysorekar [32] opined that the number of This study has some limitations. These include foramina does not seem to have any significant age and gender differences which were not relation to the length of the bone. Also, considered as we were not able to estimate the according to several other studies [33-35] the age and gender of the bones studied. These distribution of the NF within the long bone shaft differences might alter the results as the of upper and lower limb is not related to the anatomy of foramina might differ in males and length of the shaft. Zhiquan et al. [36] found the females. In old ages, some foramina might also mean total bone length for humerus was get ossified. So it is better to consult a forensic 305.12±16.29 mm. They analysed the expert to segregate the bones relationship between foramen size and humerus and analyse them based on a specific age group length and found no correlation (r=0.094, and gender. Since the NF of the long bones p=0.552). This suggests that clinicians cannot may alter during growth, the sample long estimate the size of nutrient arteries by their bones should be confined in a specific age patients body size. group. 38  Dervišević et al.; JPRI, 33(61A): 33-41, 2021; Article no.JPRI.82863 An accurate knowledge of the number of NF in 3. 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