The correlation between craniofacial and long bone growth An experimental investigation in normal rabbits.код для вставкиСкачать
THE AMERICAN JOURNAL OF ANATOMY 177:519-525 (1986) The Correlation Between Craniofacial and Long Bone Growth: An Experimental Investigation in Normal Rabbits PER ALBERIUS AND PER-ERIK ISBERG Departments ofAnatomy (PA.) and Statistics (PE.I.), University of Lund Sweden ABSTRACT The present study was undertaken to elucidate the relationships between craniofacial and long-bone growth. Nine male New Zealand white rabbits received spherical tantalum bone markers in the tibial epiphyses and in the nasal, frontal, and parietal bones. The animals were followed from 30 to 143 days of age. Growth changes were calculated with a roentgen stereometric system, and the results statistically evaluated. Except for the final interval when all variables varied at random, high correlations between tibial and frontonasal or coronal sutural growth were demonstrated; and the respective linear regression lines were homogenously assembled. The relationship between the tibia and the sagittal suture displayed great variations between individual animals as well as between the suture’s parts,. although growth at the interfrontal suture was clearly correlated to tibial growth upon exclusion of the time factor. The first principal component of the three neurocranial sutures was calculated and seemed accurately correlated to long-bone growth. The present study concluded that growth at the frontonasal and coronal sutures normally seems to parallel general somatic development, while growth at the sagittal suture appears individually displaced in time. Nevertheless, when the principal component of the combination of the coronal suture and the neurocranial section of the sagittal suture was computed, this was highly correlated to body growth. The mechanisms regulating enchondral and intramembranous bone growth are not yet fully understood. Several factors, such as heredity, age, species, nutritional status, and endocrine responses seem to affect growth in general. Other factors have localized effects, e.g., blood-flow changes (Wray and Goodman, 1961; Sunden, 1967) and oxygen tension (Persson, 1968) in long bone growth, as well as soft-tissue expansion (neural mass growth) causing bone separation at neurocranial sutures (Moss and Young, 1960; Moss, 1975). These examples and others lead us to assume that the growth process is regulated by an intricate interaction between manifold systemic, regional, and local influences. The skull and the long bones grow in response to both cartilaginous tissue growth and desmal bone growth. Cranial development is determined by growth of all its components, but is essentially characterized by differential growth between the neurocranium and splanchnocranium. The greater facial growth may contribute to orthocra- 0 1986 ALAN R. LISS, INC. nialization in some species, which process has been studied mainly in rats (e.g., Baer, 1954; Moss, 1958; Hoyte, 1971; Moss and Vilmann, 1978). Moreover, the facial skull has shown differential growth of its splanchnocranial components (the respiratory and masticatory components; Pucciarelli, 1981). So far, few investigations using concomitant registrations of long bone and craniofacia1 bone growth have been conducted. Young (1959) used tibial length as a skeletal indicator for comparisons between experimental and control animals when studying the influence of cranial contents on skull growth in rats. This was due t o the tendency of the experimental animals t o lag behind controls in general somatic development and to the existance of variations in skeletal maturation between control animals of the same age. Hinrichsen and Storey (1968) used heliAddress reprint requests to Dr. Per Alberius, Hjalmshultsgatan 1, 5-252 41 Helsingborg, Sweden. Received January 28, 1986. Accepted July 13, 1986. 520 P. ALBERIUS AND P.-E. ISBERG cal torsion springs to elucidate the effect of abnormal compressive and tensile forces across the midsagittal suture and across the proximal tibial epiphyseal plate in guinea pigs. A procedure with direct clinical consequences has also been presented. As a result of the close temporal relationship between pubertal somatic growth and that of facial dimensions, the evaluation of enchondral skeletal maturation by wrist radiography was introduced by Greulich and Pyle (1950) in order to identify the onset of the pubertal growth spurt in man. This relationship was further investigated by Bjork (1972), and the technique has facilitated orthodontic treatment planning. Trunk length or long bone registrations often have been executed for comparative reasons in studies on the effects of nutritional stresses on craniofacial growth. Interestingly, Riesenfeld (1974) noted that relative face length in rats reacted with greater intensity than the trunk to both growth depression and growth-promoting factors, irrespective of whether the etiological cause was nutritional or hormonal; and Riesenfeld also observed that these factors had limited effects on neurocranial growth. Similarily, Alberius (1983a) reported that, during a brief period of reduced food and water intake, the rabbit frontonasal suture (a splanchnocrania1 suture) and the tibia immediately reacted with reduced growth rates followed by catchup periods. Conversely, mean growth at the coronal suture was only minimally affected, even though increased growth rates were registered in individual animals after resumption of eating. Also, van der Werf(1984), who biometrically investigated the response of cranial and long-bone growth in rabbits to early weaning, found that these growth sites follow identical patterns. No attempt has yet been made, however, to elucidate the specific relationships between neurocranial and facial skeletal growth to long-bone growth under normal circumstances; do these growth sites coincide in general development, and what are their mutual relationships? The purpose of this presentation was to investigate these issues biometrically over a n extended period of time in a n animal model. 21°C (40% relative humidity), with light from 0600 to 1800 hr and with standard pellets and water provided ad libitum. The rabbits were followed until age 143 days. Operative technique The animals were anesthetized by intramuscular neuroleptanalgesia (Hypnorm vet.@: Fluanizon and Phentanyl, 10 and 0.2 mglml, respectively; 0.6 m l k g body weight). The rabbit’s head was shaved, after which the surgical area was cleaned with alcoholic chlorhexidine (5 mg/ml). A para-midline skin incision from the parietal to the nasal region was made. The skin and underlying tissues were reflected laterally, and the calvarial sutures were identified (Fig. 1). Spherical tantalum bone markers (0.8 mm in diameter) were implanted in the nasal, frontal, and parietal bones with a specially constructed instrument (Aronson et al., 1974).Each bone segment received a t least two implants, thereby enabling control of marker stability. The spheres were implanted along bilateral rostral-caudally oriented lines paralleling the median plane, the line connecting each bilateral marker pair being at a right angle to the midline (Fig. 1). Care was taken to minimize periosteal manipulation. After the implantation of bone markers the incision was closed with interrupted 410 Dexon@(polyglycolic acid) sutures and covered with Nobecutan@spray. Thereafter, tantalum balls (0.5 mm in diameter) were percutaneously, under fluoroscopic control, implanted in the proximal and distal tibial epiphyses bilaterally by means of a n angiographic needle with a n outer diameter of 0.97 mm. The animals were left to recover on a warm electric blanket. The postoperative period was uneventful. MATERIALS AND METHODS Animals We used nine 30-day-oldmale New Zealand white rabbits. The animals were kept at 20- Fig. 1. Relevant anatomy of the rabbit calvarium and principles of bone-marker positioning. Bones: 1,nasal; 2, frontal; 3, parietal. Sutures: 4, internasal; 5, frontonasal; 6, interfrontal; 7, coronal; 8, interparietal. 521 CRANIOFACIAL RELATIVE TO LONG BONE GROWTH Roentgen stereophotogrammetry Roentgen stereometric analysis was undertaken with a system developed by Selvik (1974).The animals were examined in a glass calibration cage equipped with tantalum reference markers of known internal positions lying in two parallel planes (Fig. 2). This cage defines a three-dimensional (3-D) laboratory coordinate system. Two simultaneously exposing roentgen tubes were positioned with an approximate focus-to-focus distance of 0.4 m and a focus-to-filmdistance of near 1.0 m. The maximal radiation dose for one examination was 0.6 mGy (Alberius and Selvik, 1983). Skeletal shape was generally disregarded. Initial stereoroentgenograms were obtained on the day of implantation and thereafter at regular intervals on the days indicated in Table 1. The films were digitized in a precision instrument for aerial photogrammetry (Wild Autograph A8). Three-dimensional coordinates of the bone markers were obtained by computer processing (Sperry 1100/81) and further analyzed by computer to ascertain distance changes. Longitudinal growth was calculated by a program using the 3-D Pythagorean theorem. Growth rate values for the tibia and the frontonasal and coronal sutures represent means of the right and left side. The accuracy (1 S.D.) is 21.0 pm for each growth registration; thus, 3 pmlday for a 2-week period (Alberius and Selvik, 1983). TABLE 1. Examination Drotocol Intervals 1 Age(days) 30-45 15 Lengthof examination oeriod (days) 2 3 4 5 6 7 45-59 14 59-73 14 73-87 14 87-101 14 101-115 14 115-143 28 sc ss 170 -60 -50 ‘1 i ... -LO 300 - 30 ...... -20 -10 Stereo Examinations Fig. 2. Stereometric examination. The rabbit’s head is positioned on a support in the calibration cage and is simultaneously radiographed by two roentgen tubes (focus 1 and 2). Cage reference markers in the upper and lower planes are indicated. - 5b t f IOO ? t t t days t t Fig. 3. Illustration demonstrating mean craniofacial and tibia1 growth rates (pmlday) during the period investigated (days 30-143). T, tibia; SFN, frontonasal suture; SC, coronal suture; SS, sagittal suture (internasal, IN; interfrontal, IF; interparietal, IP). 522 P. ALBERIUS AND P.-E. ISBERG RESULTS The rabbits exhibited parallel successive reductions in growth rate for the tibia, the frontonasal, and coronal sutures (Fig. 3, Table 2). During the initial interval, the frontonasal suture demonstrated diminished growth activity. Growth at all parts of the sagittal suture gradually increased and peaked between days 59 and 73, after which a slow deceleration in growth activity was registered. The latter suture obtains the greatest coefficients of variation (S.D./M). Linear regressions were calculated for all animals and are presented on an individual basis for all craniofacial variables relative to TABLE 2. Mean (SD)growth rates ( p d d a y ) for investigated growth regions as well as for the first principal components: CF = craniofacial (frontonasal + internasal sutures) and NC = neurocranial (coronal + interfrontal + interparietal sutz~resi. For the tibia and the transverse sutures (frontonasal + coronal), means of the left and right sides are presented Tibia 662.5 (43.7) Frontonasal 231.2 (14.7) suture 47.9 Coronal (8.6) suture Internasal 19.2 (9.2) suture Interfrontal 7.3 (6.7) suture 5.3 Interparietal suture (4.2) CF 0.96 (0.73) NC 0.43 (1.28) 628.7 (60.11 250.8 (18.5) 44.0 (10.1) 23.0 (7.3) 11.1 (7.6) 9.7 (3.2) 1.43 (0.63) 1.21 (1.12) Age intervals 4 5 3 2 1 587.7 (61.8) 220.7 (28.7) 40.0 (7.7) 23.5 (8.5) 15.0 (3.2) 10.9 (4.2) 1.16 (0.94) 1.59 (0.91) 495.1 (46.9) 166.7 (18.9) 30.1 (5.7) 14.0 (6.8) 8.1 (4.4) 8.2 (3.7) -0.08 (0.56) 0.20 (0.89) I, T 6 377.0 (29.4) 126.5 (11.0) 22.5 (2.4) 12.6 (3.61 3.8 (2.6) 6.6 (3.0) -0.64 (0.37) -0.71 (0.61) 7 295.4 (26.1) 90.4 (11.2) 15.7 (4.3) 10.7 (3.5) 3.5 (2.0) 4.8 (2.4) -1.14 (0.37) -1.24 (0.39) 160.5 (22.6) 61.1 (8.41 12.2 (1.6) 6.5 (1.4) 2.6 (1.9) 1.4 (1.4) -1.78 (0.17) -1.91 (0.30) T 600- 500- LOO LOO- 3001 300- 200 sc SFN I00 200 -7 10 303 20 30 40 50 60 1 603 0 500 Loo 303 200 100 P 10 M 30 10 20 30 Fig. 4. Linear regressions of individual tibia1 and craniofacial growth (day 30-143). A: Tibia (T) relative to frontonasal suture (SFN). B: T - coronal suture (SC). C: T - internasal suture (IN). D: T - interfrontal suture (IF). E: T - interparietal suture (IP). Ordinates and abscissae in find day. 523 CRANIOFACIAL RELATIVE TO LONG BONE GROWTH ative t o tibia indicated linearity for most intervals (Table 4). Terminally, though, all investigated variables varied a t random. Plots that included every conducted cranial measurement relative to tibial growth (not presented) disclosed initial spreading of all variables, except for the tibia-interparietal (T-IP) relationship, which was in constant disarray throughout the observation period. The analyzed cranial variables were divided into a craniofacial (CF = frontonasal suture + internasal suture) and a neurocrania1 (NC = coronal -t interfrontal + interparieta1 sutures) group. To investigate the relationship between the tibia and these groups the first principal component was calculated for each group. This concept signifies the linear combination of used variables that explains most of the variation observed. The principal component is a standardized measure with zero mean and unit variance. The relationship was plotted displaying initial dispersion and subsequent linearity. Linear regressions generally had similar intercepts high correlation coefficients, and smaller ra ranges (Table 3). Calculated mean values of all principal components disclosed a n increasing tendency extending to the second (CF) or third (NC) intervals, whereafter they diminished successively. The NC group was slightly more scattered as evidenced by the standard deviation computations (Table 2). When the time factor was excluded, the correlation coefficients for the CF group deteriorated due to T-IN instability. The neurocranial suture combination, however, demonstrated a linear appearance with stability within intervals as well as improved correlations for most periods. TABLE 3. Coefficients o f determination, I", (medians and ranges) for the cranial variables and for the first principal components (see Table 2) relative to the tibia r2 Variables* Median Range 0.978 0.944 0.605 0.641 0.568 0.905 0.865 0.850-0.986 0.878-0.990 0.141-0.876 0.078-0.895 0.200-0.885 0.512-0.946 0.476-0.966 T-SFN T-SC T-IN T-IF T-IP T-CF T-NC *T, tibia; SFN, frontonasal suture; SC, coronal suture; IN, internasal suture; IF, interfrontal suture; IP, interparietal suture; CF = SFN + IN; NC = SC + IF + IP. the tibia (Fig. 4a-e). The diagrams clearly demonstrate the homogeneity of frontonasal and coronal sutural expansion relative to tibial growth. Furthermore, the close approximation of these variables is reflected in the respective coefficients of determination (r2 ; Table 3). Conversely, growth a t the sagittal suture relative to tibial growth did not demonstrate similar linearity. Investigated relationships were found to vary greatly between different individuals as well as between the suture's sections. Plotted individual equations were situated at varying levels, having various inclinations and intercepts. Also, no particular pattern between the registered r2 for various cranial to tibial combinations was observed, i.e., a high r2 for the frontonasal and coronal sutures did not imply any specific trait of r2 for the various parts of the sagittal suture. When omitting the time factor, thereby investigating each interval per se, the correlation coefficients for the frontonasal, coronal, and interfrontal sutures rel- TABLE 4 . Pearson correlation coefficients of long-bone (tibia) growth relative to craniofacial growth and to the calculated first principal components (see Table 21 for each interval Variables' T-SFN T-SC T-IN T-IF T-IP T-CF T-NC Age intervals 4 1 2 3 0.742 0.806" -0.050 0.856* 0.850* 0.083 0.911** 0.706" 0.529 0.051 0.744* -0.273 0.242 0.570 0.771* 0.647 0.667 0.511 0.280 0.781" 0.553 0.850** 0.487 -0.465 0.762" 0.587 -0.204 0.803** 5 6 7 0.463 0.705 0.587 0.209 0.409 0.608 0.456 0.815" 0.549 0.724 0.204 -0.108 0.815* 0.244 -0.025 0.210 -0.309 0.127 -0.132 -0.221 0.040 'T, tibia; SFN, frontonasal suture; SC, coronal suture; IN, internasal suture; IF, interfrontal suture; IP, interparietal suture; CF = SFN + IN; NC = SC + IF + IP. *p < 0.050. **p < 0.010. 524 P. ALBERIUS AND P.-E. ISBERG DISCUSSION The purpose of the present study was to characterize and analyze the growth relationships between the long bones and the craniofacial skeleton. To perform any such assessment, it is essential to obtain reliable biometric raw data. We used a roentgen stereophotogrammetric system developed by Selvik, which enables longitudinal growth registrations and offers superior technical accuracy provided distinct measurement points are available (Selvik, 1974; Selvik et al., 1983). Tantalum balls were therefore implanted into the relevant bones, a t least two in each bone. Hereby, control of marker stability was made possible a t each stereo examination. The tantalum bone markers have been previously shown to become completely integrated into bone tissue (Alberius, 1983b). In this study, instability was infrequent and did not interfere with experimental evaluation. The registered growth data were thus considered valid for further treatment. Tibia1 growth as well as growth at the transverse sutures (the frontonasal and coronal sutures) generally decreased during the observation period, while all three parts of the sagittal suture accelerated slowly and peaked between days 59-73 of age, after which a uniform deceleration was monitored. Growth activity at the frontonasal suture, however, seemed markedly diminished during the initial interval, possibly due to effects of the surgical procedure (bone-marker insertion), e.g., reduced food intake postoperatively or posttraumatic growth inhibition (see Alberius and Selvik, 1984). Interestingly, only a facial suture thus displayed a period of consistent pronounced growth reduction, implying that during development the facial skeleton is rather vulnerable. This interpretation is supported by Riesenfeld's (1974) previously mentioned observation in rats, that the splanchnocranium seems more susceptible to external influences than both the neurocranium and body skeletal length. Speculatively, this sensitivity t o general health fluctuations indicates that even small disturbances, especially when extended for long periods of time, could aggravate potential facial skeletal abnormalities and, conversely, that these defects might partly reflect previous periods of non-health. Comparisons of normal growth data from other biometric investigations have already been published in detail (Alberius, 1983a; Al- berius and Selvik, 1983, 1986) and are thus omitted here. All variables were plotted and showed initial spreading, with values thereafter tending to approximate a line. Individual linear regressions for the two transverse sutures (frontonasal and coronal), were homogenously assembled; and the coefficients of determination, r2, were generally near 1.0. Also, when excluding the time factor, the correlation coefficients for both sutures principally showed linearity except during the last interval, when all investigated variables varied haphazardly. Normally, these sutures thus seem to parallel closely general somatic development during the period investigated, showing limited interindividual variations; and definite differences between the two could not be discerned. Growth rates at the sagittal suture, on the other hand, varied substantially, and the relationship between the syndesmosis and the tibia was not linear. The coefficients of determination differed greatly, and great disparity between individual animals as well as between the suture's different growth sites were registered. The plotted linear regressions were positioned on varying levels, having diverging inclinations and intercepts. Thus, growth a t this suture, including each of its parts, seems to exhibit temporal displacement of growth phases. This phenomenon is hard to explain on a functional anatomic basis as the suture covers both facial and neural structures, and growth at the transverse sutures seemed unaffected. Hypothetically, the variation in growth rates might reflect asymmetric and uncoordinated transverse cerebral expansion as well as a normal biological variation in growth velocity a t a particular age. Moreover, the small growth rates, a t period approaching the technical error, may induce doubts as to whether monitored values are correct. However, investigated intervals were compensatorily extended to minimize this risk. Nevertheless, when the time factor was ruled out, the interfrontal suture displayed high correlation coefficients for most intervals. This part of the sagittal suture has previously showed great plasticity, rapidly reacting to growth disturbances. Unilateral coronal suturectomy (Alberius et al., 1984) and bilateral coronal suture immobilization (Alberius and Selvik, 1984) have been found to change growth significantly at the interfrontal suture. Evidently, this suture, cover- CRANIOFACIAL RELATIVE TO LONG BONE GROWTH 525 nial sutural immobilization in rabbits. J. Neurosurg., ing the frontal cerebral lobes, which are 6Or166-173. surrounded only by a narrow skeletal casing, Alberius, P., and G. Selvik 1986 Long-term analysis of is more easily affected by growth derangecalvarial growth in rabbits. Anat. Anz., 162:153-170. ments than the posteriorly situated interpari- Alberius, P., G. Selvik, and L. Ekelund 1984 Roentgen stereophotogrammetric analysis of neurocranial sutureta1 suture. The latter suture, on the other ectomy in rabbits. J. Neurosurg., 60:158-165. hand, overlies a substantially greater mass Aronson, A.S., L. Holst, and G. Selvik 1974 An instruof neural tissue with inherent possibilities of ment for insertion of radiopaque bone markers. Radiolcompensatory growth at several areas of the ogy, 113r733-734. Baer, M.J. 1954 Patterns of growth of the skull as reneurocranium. vealed by vital staining. Human Biol., 26:80-126. The first principal component was com- Bjork, A. 1972 Timing of interceptive orthodontic meaputed in an attempt to differentiate further sures based on stages of maturation. Trans. Eur. Orbetween neurocranial and craniofacial thod. SOC.,48:61-74. growth. This statistical concept amalga- Greulich, W.W., and S.I. Pyle 1950 Radiographic Atlas of Skeletal Development of the Hand and Wrist. Stanmates information concerning two or more ford University Press, Stanford. variables, describing the existing covariation Hinrichsen, G.J., and E. Storey 1968 The effect of force between investigated variables. This implies on bone and bones. Angle Orthod., 38:155-165. that the calculation may be used as an index Hoyte, D.A.N. 1971 Mechanisms of growth in the cranial vault and base. J. Dent. Res., Suppl6; 5Or1447-1461. for cranial growth. In this study, the princi- Moss, M.L. 1958 Rotations of the cranial components in pal components of the two cranial compothe growing rat and their experimental alteration. Acta nents generally conformed to and, moreover, Anat., 32:65-86. elucidated and compressed the information Moss, M.L. 1975 Functional anatomy of cranial synostosis. Child's Brain, Ir22-33. obtained in the previously discussed anal- Moss, M.L., and H. Vilmann 1978 Studies on orthoceyses. The pattern of the neurocranial suture phalization of the rat head. I. A model system for the group, however, was more homogenous and study of adjustive cranial growth processes. Gegenconstant in appearance. Conversely, the reg- baurs Morpb. Jb., 124.559-579. M.L., and R.W. Young 1960 A functional approach istered instability of the internasal suture- Moss, to craniology. Am. J. Phys. Anthrop., 18:281-292. to-tibia relationship disrupted the craniofa- Persson, B.M. 1968 Growth in length of bones in change of oxygen and carbon dioxide tensions. Acta Orthop. cia1 suture combination when evaluated for Scand., Suppl. 117. each interval. A seemingly haphazard variaH.M. 1981 Growth of the functional compotion was observed; and consequently, growth Pucciarelli, nents of the rat skull and its alteration by nutritional at the frontonasal suture alone appears to effects. A multivariate analysis. Am. J. Phys. Anmore accurately parallel genera1 somatic throp., 56:33-41. Riesenfeld, A. 1974 Endocrine and biomechanical congrowth increments. trol of craniofacial growth: an experimental study. HuTo conclude, frontonasal and coronal su- man Biol., 46531-572. ture growth or the first principal component Selvik, G. 1974 A Roentgen Stereophotogrammetric of neurocranial suture expansion (coronal Method for the Study of the Kinematics of the Skeletal System. Thesis, University of Lund, Lund, Sweden. interfrontal interparietal sutures) exhibit G., P. Alberius, and A.S. Aronson 1983 A roenthigh and uniform correlations relative to Selvik, gen stereophotogrammetric system. Construction, callong-bone (tibia) growth. ibration and technical accuracy. Acta Radiol., (Diagn.), + + LITERATURE CITED Alberius, P. 1983a Pattern of membranous and chondral bone growth. A roentgen stereophotogrammetric analysis in the rabbit. Acta Anat., 116r37-45. Alberius, P. 1983b Bone reactions to tantalum markers. A scanning electron microscopic study. Acta Anat., 115:310-318. Alberius, P., and G. Selvik 1983 Roentgen stereophotogrammetric analysis of growth at cranial vault sutures in the rabbit. Acta Anat., 117:170-180. Alberius, P., and G. Selvik 1984 Roentgen stereophotogrammetric analysis of restricted periods of neurocra- 24:343-352. Sunden, G. 1967 Some aspects of longitudinal bone growth. An experimental study of the rabbit tibia. Acta Orthop. Scand., Suppl. 103. Werf, F. van der 1984 Response of the longitudinal growth of cranium and long bones to early weaning in the rabbit. Acta. Morphol. Neer1.-Scand., 223-16. Wray, J.B., and H.O. Goodman 1961 Post-fracture vascular phenomena and long-bone overgrowth in the immature skeleton of the rat. J. Bone Jt. Surg., 43A:10471055. Young, R.W. 1959 The influence of cranial contents on postnatal growth of the skull in the rat. Am. J. Anat., 105r383-410.