MORPHOMETRIC STUDY OF NUTRIENT FORAMEN IN THE LONG BONES OF LOWER LIMB

Address for Correspondence: Dr. Shalini Ramanathan, Assistant Professor, Department of Anatomy, Dhanalakshmi Srinivasan Medical College and Hospital, Siruvachur, Perambalur, Tamilnadu, India. E-Mail: liniram80@yahoo.com Background: The nutrient foramen allows the passage of the neurovascular bundle to and from the diaphysis of the long bones. The nutrient foramen has a specific position in each long bone. The nutrient artery is the main source of blood supply to the actively growing long bone in children. Materials and Methods: This study was conducted in 450 long bones of the lower limb (150femur, 150tibia, 150fibula). The number, size, location and direction of the diaphyseal nutrient foramen in each of the long bones was noted. The foraminal index was also calculated using the Hughes formula. Results: In femur single nutrient foramen was present in 64% of the bones, double nutrient foramina in 30% of the bones and triple nutrient foramina in 6% of the bones. The most common location of the nutrient foramina in femur was in between the 2 lips of linea aspera, which was noted in 40.84% of the bones and in 88% of the bones the nutrient foramen was located in the middle third of the shaft of femur. In tibia, single nutrient foramen was found in 98% of the bones and double nutrient foramina were found in 2% of the bones. The most common location of the nutrient foramen in tibia was on the posterior surface midway between the interosseous border and soleal line, which was noted in 47.05% of the bones and in 58% of the bones, the nutrient foramen was located in the middle third of the shaft of tibia. In fibula, single nutrient foramen was found in 98.66% of the bones and double nutrient foramina were found in 1.33% of the bones. The most common location of the nutrient foramen in fibula was on the posterior surface on the medial crest, which was noted in 41.44%of the bones and in 90% of the bones the nutrient foramen was on the middle third of the shaft of fibula. Conclusion: The precise knowledge of the nutrient foramen of the long bones of lower limb will help Orthopaedicians and Plastic surgeons during surgeries of the lower limb.


INTRODUCTION
The nutrient foramen is a cavity allowing the passage of a nutrient artery and a peripheral nerve into the diaphysis of a long bone [1].The nutrient artery is the principal source of blood supply to long bones, especially during periods of active bone growth and also in embryonic stages [2].Trueta J, [3] has reported that 70 -80% of intraosseous blood supply to long bones in children is supplied by nutrient arteries and when there is a compromise of this blood supply, ischemia of medullary bone occurs and there is less vascularization of metaphysis and growth plate.The nutrient foramen is generally directed away from the growing end of the bone [4].
The nutrient foramen is located in a specific position in each bone [5].In femur, the nutrient foramen is directed upwards and most commonly located on the Linea Aspera.The main nutrient artery is derived from the 2 nd perforating artery.If there are 2 nutrient arteries, they may arise from the 1 st and 3 rd perforators [4].
In tibia, the nutrient foramen usually lies near the soleal line and is directed downwards.The main nutrient artery is a branch of posterior tibial artery, but sometimes it may also arise at the popliteal bifurcation, or as a branch from anterior tibial artery [4].
In fibula, the nutrient foramen is located slightly proximal to the midpoint of the posterior surface and is directed downwards.The nutrient artery to fibula is a branch of fibular artery [4].Knowledge of the anatomy of nutrient foramen of fibula is very important while raising osteofasciocutaneous free flaps of fibula [5].The vascularized fibular bone grafts are used for stabilization of lost mandible, spine and also tibia.Fibular grafts are also used for reconstructive surgeries after excision of bone tumours and other bony defects [6].
The precise knowledge of nutrient foramina is needed during treatment of bone fractures [7], bone grafting surgeries and also for the interpretation of height of an individual from a fragment of bone in medicolegal cases [8].Hence, the present study was conducted to observe the number, size, location and direction of nutrient foramen in the long bones of lower limb.

MATERIALS AND METHODS
The present study was conducted on 450 long bones of lower limb (150-femur, 150-tibia and 150-fibula) of unknown age and sex.The bones were obtained from the Department of Anatomy, Dhanalakshmi Srinivasan Medical College and Hospital, Perambalur, Tamilnadu.The bones which were complete and fully ossified were included for the study.Incomplete bones and those with pathological changes were not included in the study.Only the diaphyseal nutrient foramen was observed for the study.
The number of nutrient foramina in each bone was noted.The size of the nutrient foramen was measured using a hypodermic needle.Nutrient foramina which did not allow the passage of a size 24 gauge needle were considered as secondary nutrient foramina.Nutrient foramina which allowed the passage of size 24 gauge needle were considered as dominant nutrient foramina [9].The direction of the nutrient foramen was assessed by passing a hypodermic needle into the nutrient foramen.
The location of the nutrient foramen in each long bone was noted in relation to the nearby anatomical structures.
The distance of the dominant nutrient foramen (DNF) from the highest point of the proximal part of the long bones was measured with a vernier calipers.The total length (TL) of the bone was measured using an osteometric board.The location of the nutrient foramen in the upper, middle or lower third of the bone was determined using Hughes formula for foraminal index (FI).FI= DNF / TL X 100.
The nutrient foramen was localised to the proximal, middle and distal third of the shaft of the bone based on the foraminal index as follows: FI less than 33.33 -the nutrient foramen was in the proximal third of the bone FI from 33.33 to 66.66 -the nutrient foramen was in the middle third of the bone FI greater than 66.66 -the nutrient foramen was in the distal third of the bone.
All the observations were carefully tabulated and statistically analysed using Microsoft excel worksheet.

Number of nutrient foramina observed:
In femur, single nutrient foramen was observed in 64% of the bones, double nutrient foramina (Figure 1) was observed in 30% of the bones and triple nutrient foramina (Figure 2) was observed in 6% of the bones (Table 1).
In tibia, single nutrient foramen was observed in 98% of the bones and double nutrient foramina (Figure 3) were observed in 2% of the bones (Table 1).
In fibula, single nutrient foramen was observed in 98.66 % of the bones and double nutrient foramina (Figure 4) were observed in 1.33% of the bones (Table 1).Nutrient foramina in femur: All the nutrient foramina observed in femur were directed upwards.88.26% of the nutrient foramina allowed the passage of 24 gauge needle and were considered as dominant nutrient foramina.11.73 % of the nutrient foramina were observed to be secondary nutrient foramina (Table 2).The nutrient foramina were most commonly located between the 2 lips of linea aspera (Table 2).The average total length of femur was found to be 42.19 + 3.46 cm.The average distance of the dominant nutrient foramen from the highest point on the proximal part of the bone was 17.11 + 5.42 cm.The average foraminal index was 40.55 + 8.32.88% of the nutrient foramina were observed in the middle third of the shaft of femur (Table 3).were dominant nutrient foramina and 17.64% of the nutrient foramina were secondary nutrient foramina (Table 4).The most common location of the nutrient foramen was posterior surface of tibia-midway between interosseous border and soleal line (Table 4).

RESULTS
The average total length of tibia was found to be 36.58+ 2.38 cm.The average distance of the dominant nutrient foramen from the highest point on the proximal part of the bone was 12.70 + 3.64 cm.The average foraminal index was 34.74 + 4.08.58% of the nutrient foramina were observed in the middle third of the shaft of tibia (Table 5).Nutrient foramina on fibula: All the nutrient foramina observed in fibula were directed downwards.82.89% of the nutrient foramina observed were dominant nutrient foramina and 17.10% of the nutrient foramina were secondary nutrient foramina (Table 6).The most common location of the nutrient foramina was on the medial crest on the posterior surface of fibula (Table 6).The average total length of fibula was found to be 35.36+ 3.26 cm.The average distance of the dominant nutrient foramen from the highest point on the proximal part of the bone was

Number of bones Percentage
Proximal third 15 10%

Middle third 135 90%
Distal third --14.12+ 3.75 cm.The average foraminal index was 39.93 + 7.32.90 % of the nutrient foramina were observed in the middle third of the shaft of fibula (Table 7).

DISCUSSION
Femur: In the present study 64% of the femur bones showed a single nutrient foramen.Kizilkanat et al. [10] in his study on Turkish population & Longia et al, [8] in his study on Indian population have reported that single nutrient foramen in femur is commonly present.
Mysorekar VR [11], has reported a 50% incidence of occurrence of double nutrient foramina in Indian population.Forriol Campos et al.
[12] has reported 60% occurrence of double nutrient foramina in Spanish population.Sendemir and Cimen [13] in Turkish population have recorded 46% occurrence of double nutrient foramina.In the present study, it was 30% (Table 1).
Mysorekar VR [11], has also reported the occurrence of triple nutrient foramina in femur.Mazengenya et al. [14] has reported the occurrence of 6 nutrient foramina on a single femur.Ambekar SA et al. [9] has reported the occurrence of 5 nutrient foramina in 2 femur bones and triple nutrient foramina were observed in 26.9% of the femur bones in their study.
The mean length of femur was 42.19cm which is less compared to other population.The mean femur length of black South African population was 44.34cm and white South African population was 44.96cm [14].Sendemir and Cimen [13], have reported a mean length of 44.3cm in Turkish population, Kizilkanat et al. [10] have reported the length to be 42.6cm in Turkish population and Kirschner et al. [15] have reported a mean femoral length of 40.8cm in Germans.Abledu JK et al. [16] have reported the length of femur to be 44.97 + 2.34cm.Ambekar SA et al. [9] has reported the mean femoral length to be 40.79cm.
Mazengenya et al. [14] has reported that the majority of the nutrient foramina were found between the 2 lips of linea aspera.In the studies by Lutken P [17], 71.1% of the nutrient foramina were on the linea aspera.Patel SM et al. [18] have reported that the nutrient foramina were most commonly located on the posteromedial surface of femur.
ce of 62.5% of secondary nutrient foramina.Patel SM et al. [18] have reported that the nutrient foramina were most commonly located in the upper third of the tibia.Gupta RK and Kumari GA [19], have reported the nutrient foramina to be commonly located in middle third of tibia.Ambekar SA et al. [9] have reported that the nutrient foramina were commonly placed on the proximal third of tibia.Kizilkanat et al. [10] have reported that the nutrient foramina were commonly present in middle third of tibia.
The nutrient foramina is generally directed downwards in tibia [11].Mazengenya et al. [14] have reported that 0.6% tibial nutrient foramina in black South Africans and 1.7% tibial nutrient foramina in white South Africans to be directed upwards.
Fibula: Ambekar SA et al. [9] has reported the presence of one nutrient foramen in 63.5% of fibulae, two nutrient foramina in 7.7% of fibulae and three nutrient foramina in 1.9% of fibulae.Patel SM et al. [18] has reported the occurrence of single nutrient foramen in 80% of fibulae and triple nutrient foramina in 1.3% of fibulae in black South Africans.Double nutrient foramina were found in 8.9% of fibulae of white South Africans.Occurence of only a single nutrient foramen was reported by Kizilkanat et al. [10], Longia et al. [8], and Forriol Campor et al. [12].
Ambekar SA et al. [9] has reported the total length of fibula to be 35.35cm.Kizilkanat et al. [10] has reported the length to be 34.02cm in Turkish population.Mazengenya et al. [14] has reported the length to be 36.76cm in black South Africans and 36.07cm in white South Africans.
Patel SM et al. [18] has reported the most common location for nutrient foramina in fibula to be on the posterior surface and on the medial crest.Mazengenya et al. [14] has reported the most common location to be on the posterior surface of fibula, followed by medial surface and then lateral surface of fibula.Nutrient foramen was most commonly located on the medial surface of fibula in the study by Forriol Campos et al. [12], and Sendemir and Cimen [13].
Mysorekar VR et al. [11] has reported the common location to be on the medial crest.
Ambekar SA et al. [9] has reported the nutrient Mazengenya et al. [14] has reported that the majority of the nutrient foramina were on the middle third of shaft of femur.Mysorekar et al.
[11], Longia et al. [8], Kirschner et al. [15], and Kizilkanat et al. [10] have also reported that the nutrient foramina were most commonly located on the middle third of femur.Patel SM et al. [18] has reported the occurrence of 25% secondary nutrient foramina in femur.
The nutrient foramina are directed away from the fast growing ends of the bone.In the lower limb the nutrient foramina are directed away from the knees [11].Hence the nutrient foramina is directed upwards in femur.
Tibia: Patel SM et al. [18] have reported that there was only a single nutrient foramen in tibia.
Gupta RK and Kumari GA [19], have reported the occurrence of 2 nutrient foramina in 2 tibiae.Kizilkanat et al. [10] have reported 2% occurrence of double nutrient foramina.Mazengenya et al. [14] have reported 1.7% occurrence of double nutrient foramina in white Africans and 0.6% occurrence in black Africans.Mazengenya et al. [14] have reported the mean tibial length to be 38.44cm in black South Africans and 37.12 in white South Africans.Nagel A [20], has reported the tibial length to be 34.8cm in Americans.Kizilkanat et al. [10] in Turkish population have reported the length to be 35.8cm.Length of tibia in the present study is similar to Ambekar SA et al. [9] who have reported it to be 36.19cm.
In the present study the length of tibia is 36.58cm.Patel SM et al. [18] from India have reported that the most common location of nutrient foramina was on the posterior surface closer to the interosseous border.
Mazengenya et al. [14] have reported the nutrient foramina to be located in posterior surface in 75.6% of black South Africans and 77.8% in white South Africans.Mysorekar et al.
[11] has reported 74% occurrence of nutrient foramina in the posterior surface.Sendemir and Cimen [13], have reported 90% occurrence of nutrient foramina in the posterior surface.In present study, all the nutrient foramina were on the posterior surface and commonly located midway between the interosseous border and soleal line.Gupta RK and Kumari GA [19], have reported that there was no secondary nutrient foramina in tibia.Patel SM et al. [18] has reported occurren-foramina to be located in the middle third of the fibula.Patel SM et al. [18] has reported the nutrient foramina to be in the middle third in 93.8% of fibulae and in 4.1% of fibulae the nutrient foramina were in the in the distal third.Mysorekar VR et al. [11] have reported the nutrient foramina to be directed downwards in fibula.It was directed downwards in all the nutrient foramina observed in fibula.
The nutrient artery should be preserved during tumour resection and fracture surgeries [21].
Accidental ligation of nutrient artery will decrease the blood supply to bones and may lead to malunion and non-union.Nutrient foramen appears linear in radiographs which can mimic a fracture.
The nutrient foramen is also considered as a potential area of weakness in some patients [22].Longitudinal stress fractures associated with nutrient foramen are commonly seen in Tibia and have been reported to occur less frequently in femur, fibula and patella [7].Fibula is commonly used for bone grafting.Hence location of nutrient foramen will help during bone transplantation surgeries.
The precise knowledge of the location, direction, number and size of the nutrient foramina of long bones of lower limb will help the orthopaedicians during fracture repair surgeries, tumour resection and also during bone grafting surgeries.The nutrient artery is essential to maintain the growth of osteophytes, hence the nutrient foramina should be preseved during tumour resection surgeries on the bones.

Table 1 :
Number of nutrient foramina observed in the long bones of lower limb.

Table 2 :
Position and number of dominant nutrient foramina and secondary nutrient foramina observed in femur.

Table 3 :
Location of nutrient foramina based on foraminal index.

of nutrient foramen on the shaft of femur Number of bones Percentage Proximal third 18 12%
Nutrient foramina in Tibia: All the nutrient foramina observed in tibia were directed downwards.82.35% of the nutrient foramina observed

Table 4 :
Position and number of dominant nutrient foramina and secondary nutrient foramina observed in Tibia.

in Tibia Number of nutrient foramina Percentage of nutrient foramina Number of dominant nutrient foramina Number of secondary nutrient foramina Posterior surface-midway between interosseous border and soleal line
Kalyanasundaram Mohan et al.MORPHOMETRIC STUDY OF NUTRIENT FORAMEN IN THE LONG BONES OF LOWER LIMB.

Table 5 :
Location of nutrient foramina on tibia based on foraminal index.

Table 6 :
Position and number of dominant nutrient foramina and secondary nutrient foramina observed in Fibula.

Table 7 :
Location of nutrient foramina on fibula based on foraminal index.