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To revisit foetal development of the deep flexor tendons of the hand and foot, we examined the paraffin-embedded histology of 20 mid-term foetuses at 8–15 weeks of estimated gestational age (35–118 mm crown-rump length or CRL). At 8–9 weeks, in front of the metacarpal bones, the flexor pollicis longus and flexor digitorum profundus (FDP) muscles provided a plate-like, common tendon from which the lumbricalis muscles originated. However, in the foot, we had no evidence of such a common tendon. The flexor pollicis tendon was separated from the common tendon at 9–10 weeks possibly due to mechanical stress from the laterally growing thumb. Notably, at the lumbricalis muscle origins at 10–12 weeks, the FDP and flexor digitorum longus tendons remained undifferentiated and the primitive tenocytes were dispersed from them. The dispersed cells seemed to develop into an interface tissue between the lumbricalis muscle fibre and the deep tendon. In 3 of 5 specimens at 15 weeks, we found an excess number of the FDP tendons (5–7) in the proximal side of the lumbricalis muscle origin. However, the excess tendons dispersed in the lumbricalis muscle origin. The development of the lumbricalis muscle origin might follow the tendon splitting for four fingers. However, conversely, we hypothesised that the developing lumbricalis muscles re-arranged the deep flexor tendons to provide a configuration of “one deep tendon per one finger (or toe)”. The quadrates plantae muscle seemed not to contribute on the re-arrangement. (Folia Morphol 2012; 71, 3: 154–163)
The digastricus and omohyoideus muscles are digastric muscles with two muscle bellies. An insertion tendon of the posterior belly becomes an intermediate tendon in digastricus muscles, whereas a single band-like muscle in omohyoideus muscles may later be interrupted by an intermediate tendon, possibly due to muscle cell death caused by mechanical stress. In human foetuses, an intermediate tendon provides the temporal origins of the tensor veli palatini and tensor tympani muscles. Some reptiles, including snakes, carry multiple series of digastric-like axial muscles, in which each intersegmental septum is likely to become an intermediate tendon. These findings indicate that many pathways are involved in the development of digastric muscles. A review of these morphologies suggested that the flexor digitorum superficialis (FDS) muscle was a digastric muscle, although the intermediate tendon may not be visible in the surface view in adults. The present observations support the hypothesis that the proximal anlage at the elbow develops into a deep muscle slip to a limited finger, while the distal anlage at the wrist develops into the other slips. The findings suggest that, in the FDS muscle, the proximal and distal bellies of the embryonic digastric muscle fuse together to form a laminar structure, in which muscle slips accumulate from the palmar to the deep side of the forearm. (Folia Morphol 2018; 77, 2: 362–370)
Background: At birth, the ductus arteriosus (DA) merges with the aortic arch in the slightly caudal side of the origin of the left subclavian artery (SCA). Since the SCAs (7th segmental arteries) were fixed on the level of the 7th cervical-first thoracic vertebral bodies, the confluence of DA should migrate caudally. We aimed to describe timing and sequence of the topographical change using serial sagittal sections of 36 human embryos and foetuses (CRL 8–64 mm; 5–10 weeks), Those made easy evaluation of the vertebral levels possible in a few section. Materials and methods: The DA or 6th pharyngeal arch artery seemed to slide down in front of the sympathetic nerve trunk along 1.0–1.2 mm from the second cervical vertebral level at 5–6 weeks and, at 6 weeks (CRL 14–17 mm), the DA confluence with aorta reached the 7th cervical level. Because of the highly elongated common carotid artery, the sliding of DA confluence seemed to be much shorter than the cervical vertebrae growing from 1 mm to 2.4 mm. Results: At the final topographical change at 6–7 weeks, the DA confluence further descended to a site 1-vertebral length below the left SCA origin. From 6 to 9 weeks, a distance from the top of the aortic arch to the left SCA origin was almost stable: 0.3–0.5 mm at 6 weeks and 0.4–0.6 mm at 9 weeks. Conclusions: The heart descent and the caudal extension of the trachea and bronchi, those occurred before the DA sliding, were likely to be a major driving force for the sliding. (Folia Morphol 2019; 78, 4: 720–728)
Background: Prenatal twisting of the femoral neck seems to result in an angle of anteversion or torsion, but the underlying process has not been elucidated. Materials and methods: This study analysed sagittal, frontal and horizontal sections of 34 embryo and foetal specimens of gestational age (GA) 6–16 weeks (crown-rump length 21–130 mm). At GA 6–7 weeks, the iliopsoas (IP) and gluteus medius (GME) muscles were inserted into the anterior and posterior aspects of the femur, respectively, allowing both insertions to be viewed in a single sagittal section. Results: At GA 8 weeks, the greater trochanter and the femoral neck angle became evident, and the GME tendon was inserted into the upper tip of the trochanter. At GA 9 weeks, the location of IP insertion was to the medial side of the GME insertion. After 9 weeks, the IP insertion consisted of a wavy, tendinous part of the psoas muscle and another part of the iliacus muscle, with many fibres of the latter muscle attached to the joint capsule. After GA 12 weeks, the IP was inserted into the anteromedial side of the greater trochanter, while the aponeurotic insertion of the GME wrapped around the trochanter. At GA 15–16 weeks, a deep flexion at the hip joint caused an alteration in the relative heights of the lesser and greater trochanter, with the former migrating from the inferior to the slightly superior side. Conclusions: These findings indicate that twisting of the femoral neck started at GA 8–9 weeks. (Folia Morphol 2019; 78, 2: 408–418)
Development of a long muscle belly in foetal extremities generally requires a definite bony insertion of the long tendon. However, in adults, the pes anserinus and the semimembranosus tendon (SMT) are inserted into fasciae. Development of fascial insertions in foetuses was investigated by examining serial histological sections obtained from 7 foetuses at 8–9 weeks and 8 foetuses at 14–16 weeks. The presence of matrix substances and macrophages was also examined by immunohistochemistry. At 8 weeks, the tendons of the semitendinosus, gracilis, sartorius and semimembranosus muscles were straight and inserted into the initial shaft-like proximal end of the tibia on the proximal side of the popliteus muscle. At 9 weeks, however, the medially extending popliteus muscle appeared to push the pes anserinus tendons superficially, with a loss of cartilage insertions. The SMT obtained an attachment to the popliteus muscle. At 14–16 weeks, the SMT divided into thick and thin bundles: the former contained abundant macrophages and inserted into the tenascin-positive perichondrium of the enlarged proximal tibia, while the later without macrophages ended at the joint capsule. The pes anserinus tendons, negative for both versican and tenascin-c, took highly tortuous courses toward the fascia cruris. Because the medial extension of the popliteus muscle was associated with the enlargement of the proximal tibia, the topographical relationship of the popliteus muscle with these 4 tendons changed drastically, resulting in a loss of cartilage insertion of the pes anserinus tendons as well as the division and reconstruction of the SMT. (Folia Morphol 2016; 75, 4: 503–511)
Using longitudinal semiserial sections of 12 lower extremities from 8 human foetuses at 15–18 weeks, we compared foetal morphologies of the knee in specimens with and without fabellae. We also compared the fabella, if present, with the hallucal sesamoid in the same foetus. Cartilaginous fabella, positive for versican and tenascin by immunohistochemistry, was found in 5 of the 8 foetuses. This structure was embedded in a thick and tight lateral fibrous band, providing a common origin of the plantaris muscle and the lateral head of the gastrocnemius muscle. The plantaris was covered by the lateral head of the gastrocnemius, but these 2 muscles were separated by a distinct fascia or space. Notably, the foetal fabella did not attach to the joint capsule. In the 3 specimens without fabellae, the lateral fibrous band was thin, containing a fibrous mass, negative for versican and tenascin, in place of the fabella. The “medial” head of the gastrocnemius faced or covered the plantaris, while the lateral head was continuous with the plantaris. A hallucal cartilaginous sesamoid, positive for versican and tenascin, was present in all 8 specimens. It carried a flat surface facing the joint cavity and was covered by tendons of the short muscles of the foot. Because of the difference in topographical relation of muscles between specimens with or without fabella, rather than mechanical stress to the tendon, fabella development may require a distinct plantaris muscle independent of the gastrocnemius. We discussed about an evolutionary aspect of the fabella and plantaris muscle. (Folia Morphol 2017; 76, 1: 87–93)
The vascular content of retrodiscal tissue in the temporomandibular joint (TMJ) plays a critical role in joint function, and its morphology is therefore likely related to TMJ pain. Using histological sections of human foetuses as well as T2-weighted magnetic resonance images (MRI), we measured the vascular content of retrodiscal tissue. MRI showing no pathology in and around the TMJ were obtained from 18 young patients who had been suffering from headache. In 10 small foetuses (12–14 weeks of gestation) as well as 10 larger foetuses (30–37 weeks), the vascular content showed individual variations exceeding 5 times the minimum value (0.24 vs. 0.04 mm² per 1 mm²), but no difference between foetal stages was evident. In the MRI from young adults, the variation was less than twice the minimum value (13.6 vs. 8.7 mm² per 100 mm²). The vascular density appeared to be lower in adults than in foetuses. In both foetuses and adults, the thickness (anteroposterior length) of the tissue did not correlate with the vascular sectional area. These findings suggest that the considerable inter-individual differences evident in the vascular content of foetal retrodiscal tissue may be reduced during further development. (Folia Morphol 2014; 73; 2: 153–158)
Ligament of Henle is one of muscle-associated connective tissues of the rectus abdominis muscle, but it has been confused with the conjoint tendon (a common aponeurosis for insertion of the inferomedial end of the obliquus internus and transversus abdominis muscles). To reconsider the inguinal connective tissue structures, we examined 20 mid-term foetuses (10 males and 10 females) at approximately 14–20 weeks of gestation (crown rump length 100–170 mm). In female horizontal sections, we consistently found the ligament of Henle as a wing-like aponeurosis extending from the lateral margin of the rectus tendon behind the superficial inguinal ring. The ligament was separated from and located behind the conjoint tendon. In all male foetuses, instead of the ligament, the conjoint tendon was evident behind the superficial ring and it winded around the posterior aspect of the spermatic cord. Therefore, although a limited number of specimens were examined, the ligament of Henle was likely to be a female-specific structure. The ligament of Henle, if developed well, may provide an arch-like structure suitable for a name “falx inguinalis” instead of the inferomedial end of the conjoint tendon. In addition, a covering fascia of the iliopsoas muscle joined the posterior wall of the inguinal canal in male, but not in female, specimens. (Folia Morphol 2013; 72; 2: 147–154)
Using D2-40 immunohistochemistry, we examined the morphology of lymphatic vessels (LVs) in, along and around the uterus of 10 donated female cadavers (mean age, 85 years). All these women had 1 or 2 children with vaginal delivery, but the other obstetrics information was unknown. When compared with the bladder, vagina and the subperitoneal tissue, the percentage area of LVs in a 3 × 2 mm square including the hot spot was extremely high along the uterine artery and superficial uterine vein, in spite of the silent physiology of the elderly uterus. Notably, the LVs along the uterine artery and superficial uterine vein were highly dilated and embedded in the tight connective tissue around the artery and vein. In contrast, the LVs were separated from the artery and vein in the so-called vesico- -uterine ligament. Thus, surgical separation of the LVs from the artery and vein, i.e., skeletonisation, appears very difficult along the uterine artery and superficial uterine vein. This may become a major factor limiting the future application of robot-assisted surgery for uterine cancers. (Folia Morphol 2016; 75, 2: 232–239)
Evaluation of semiserial sections of 14 normal hearts from human foetuses of gestational age 25–33 weeks showed that all of these hearts contained thin veins draining directly into the atria (maximum, 10 veins per heart). Of the 75 veins in these 14 hearts, 55 emptied into the right atrium and 20 into the left atrium. These veins were not accompanied by nerves, in contrast to tributaries of the great cardiac vein, and were negative for both smooth muscle actin (SMA) and CD34. However, the epithelium and venous wall of the anterior cardiac vein, the thickest of the direct draining veins, were strongly positive for SMA and CD34, respectively. In general, developing fibres in the vascular wall were positive for CD34, while the endothelium of the arteries and veins was strongly positive for the present DAKO antibody of SMA. The small cardiac vein, a thin but permanent tributary of the terminal portion of the great cardiac vein, was also positive for SMA and CD34. A few S100 protein-positive nerves were observed along both the anterior and small cardiac veins, but no nerves accompanied the direct drainage veins. These findings suggested that the latter did not develop from the early epicardiac vascular plexus but from a gulfing of the intratrabecular space or sinus of the atria. However, the immunoreactivity of the anterior cardiac vein suggests that it originated from the vascular plexus, similar to tributaries of the great cardiac vein. (Folia Morphol 2019; 78, 2: 283–289)
In adults, the oblique cord or chorda obliqua separates the origins of the flexor pollicis longus (FPL) and flexor digitorum profundus (FDP) muscles from the supinator muscle and elbow joint. This study examined the topographic anatomy of the oblique cord and related muscles in foetuses. Semiserial sections of five mid-term foetuses of gestational age (GA) 14–16 weeks and 12 late-stage foetuses of GA 28–30 weeks were histologically examined and three forearms at GA 30 weeks were macroscopically evaluated. Late-stage foetuses showed a fascial structure between the supinator and FDP muscles. The latter extended proximally to the elbow joint and the muscle origin thickened the distal, ulnar part of the capsule. The FPL origin also extended proximally but did not reach the joint capsule. These morphologies were consistent with macroscopic examinations. The brachialis muscle was widely inserted into the proximal, anterior part of the capsule. In addition, the medial collateral ligament was not covered by the pronator-flexor muscles but by the triceps brachii muscle. The oblique cord apparently did not form prenatally. After birth, the proximal parts of the FDP and FPL muscles were likely replaced by collagenous tissues, providing a specific type of intermuscular septum i.e., the oblique cord. This type of muscle-ligament transition was observed in the annular ligament of the radius. The foetal elbow joint was characterised by strong support by the FDP, brachialis and triceps brachii muscles. Therefore, the foetal elbow is not a miniature version of the adult elbow. (Folia Morphol 2016; 75, 4: 493–502)
Background: The human tensor fasciae latae muscle (TFL) is inserted into the iliotibial tract and plays a critical role in lateral stabilisation of the hip joint. We previously described a candidate of the initial iliotibial tract that originated from the gluteus maximus muscle and extended distally. Materials and methods: This study extended our observations by examining 30 human embryos and foetuses of gestational age (GA) 7–14 weeks (crown-to-rump length 24–108 mm). At GA 7 weeks, the TFL appeared as a small muscle mass floating in the subcutaneous tissue near the origins of the gluteus medius and rectus femoris muscles. Results: Subsequently, the TFL obtained an iliac origin adjacent to the rectus femoris tendon, but the distal end remained a tiny fibrous mass on the vastus lateralis muscle. Until GA 10 weeks, the TFL muscle fibres were inserted into a vastus lateralis fascia that joined the quadriceps tendon distally. The next stage consisted of the TFL muscle belly “connecting” the vastus fascia and the gluteus fascia, including our previous candidate of the initial iliotibial tract. Until GA 14 weeks, the TFL was sandwiched by two laminae of the connecting fascia. Conclusions: These findings suggested that, when the vastus lateralis fascia separated from the quadriceps tendon to attach to the tibia, possibly after birth, the resulting iliotibial tract would consist of a continuous longitudinal band from the gluteus maximus fascia, via the vastus fascia, to the tibia. Although it is a small muscle, the foetal TFL plays a critical role in the development of the iliotibial tract. (Folia Morphol 2018; 77, 4: 703–710)
Birds and reptiles always carry a long and thick artery accompanying the sciatic nerve (i.e. the sciatic artery) whereas mammals do not. We attempted to demonstrate a difference in courses of the nerve and the arteries of foetuses in relation to hip joint posture. Eight mid-term human foetuses (15–18 weeks), five mouse foetuses (E18), and five chick embryos (11 days after incubation) were examined histologically. Thin feeding arteries in the sciatic nerve were consistently observed in human foetuses in spite of the long, inferiorly curved course of the nerve around the ischium. The tissue around the human sciatic nerve was not so tight because of the medial and inferior shift of the nerve away from the hip joint. The foetal hip joint position differed among the species, being highly flexed in humans and almost at right angle flexion in mice and chicks. Because of deep adduction of the hip joint in the mouse, the knee was located near the midline of the body. The mouse sciatic nerve ran through the tight tissue along the head of the femur, whereas the chick nerve ran through the loose space even in the gluteal region. In birds, evolution of the pelvis including the hip joint without adduction seemed to make the arterial development possible. In mammals, highly flexed or adducted hip joint seemed to be one of the disturbing factors against development of the long and thick artery. A slight change in posture may cause significant arterial variation. (Folia Morphol 2013; 72, 1: 41–50)
In the head and neck of human mid-term foetuses, the interface between areas of endochondral ossification and adjacent membranous (intramembranous) ossification is extensive. Using 8 foetal heads at 15–16 weeks, we have demonstrated differences in the matrices and composite cells between these 2 ossification processes, especially in the occipital squama and pterygoid process. Aggrecan-positive cartilage was shown to be invaded by a primitive bony matrix that was negative for aggrecan. At the interface, the periosteum was continuous with the perichondrium without any clear demarcation, but tenascin-c expression was restricted to the periosteum. In contrast, the interface between the epiphysis and shaft of the femur showed no clear localisation of tenascin-c. Versican expression tended to be restricted to the perichondrium. In the pterygoid process, the density of CD34-positive vessels was much higher in endochondral than in membranous ossification. The membranous part of the occipital was considered most likely to contribute to growth of the skull to accommodate the increased volume of the brain, while the membranous part of the pterygoid process seemed to be suitable for extreme flattening under pressure from the pterygoid muscles. (Folia Morphol 2014; 73, 2: 199–205)
The human gluteus maximus muscle (GMX) is characterised by its insertion to the iliotibial tract (a lateral thick fascia of the thigh beneath the fascia lata), which plays a critical role in lateral stabilisation of the hip joint during walking. In contrast, in non-human primates, the GMX and biceps femoris muscle provide a flexor complex. According to our observations of 15 human embryos and 11 foetuses at 7–10 weeks of gestation (21–55 mm), the GMX anlage was divided into 1) a superior part that developed earlier and 2) a small inferior part that developed later. The latter was adjacent to, or even continuous with, the biceps femoris. At 8 weeks, both parts inserted into the femur, possibly the future gluteal tuberosity. However, depending on traction by the developing inferior part as well as pressure from the developing major trochanter of the femur, most of the original femoral insertion of the GMX appeared to be detached from the femur. Therefore, at 9–10 weeks, the GMX had a digastric muscle-like appearance with an intermediate band connecting the major superior part to the small inferior mass. This band, most likely corresponding to the initial iliotibial tract, extended laterally and distally far from the muscle fibres. The fascia lata was still thin and the tensor fasciae latae seemed to develop much later. It seems likely that the evolutionary transition from quadripedality to bipedality and a permanently upright posture would require the development of a new GMX complex with the iliotibial tract that differs from that in non-human primates. (Folia Morphol 2018; 77, 1: 144–150)
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