Establishing a Body and Pelvic Biometric Standard and determining their Relationship in the French Bulldog
The dimensions of the pelvic diameter, which are directly obtained from radiographic images, are known as radiographic pelvimetry. This technique allows the determination of the standard pelvimetry for each breed and the anatomical classification of the pelvis. A radiographic study of the pelvimetric aspects of 20 French Bulldog bitches was performed to obtain data on the pelvic diameters and correlate these with external body and pelvic measurements. These external body and pelvic measurements were obtained using a metric tape, whereas radiographic pelvic dimensions were obtained directly from the radiographic images. A significant positive correlation was observed between pelvic radiographic measurements of the bi-ischiatic line, coxal tuberosity, and the area of the pelvic entrance and body weight, with a correlation index of 0.75 (P<0.005). A significant positive correlation was also observed between the cranial circumference (CC) and sacral diameter (SAD), with a correlation index of 0.76 (P<0.05). However, correlations between other external and radiographic pelvic measures were of a low magnitude, which indicated a significant association between different measures. Therefore, French Bulldog bitches can be classified as mesatipellic. The CC had a positive correlation with the SAD and several pelvic measurements were correlated with body weight. For reproductive efficiency, it is important to conduct studies within a physical standard; a breed determination, because there is a variation in the size, shape, and weight of the head between different breeds of dogs, and it is therefore important to establish mathematical formulas and normal ranges for each breed or standard.
Keywords: French Bulldog; Biometry; Pelvimetry
Recently, demand for exotic canine breeds in Brazil has increased. Among these exotic breeds, those of small size, including French Bulldogs, are becoming increasingly popular because of their ease of adapting to the smaller domestic environments that are found in big cities. French Bulldog is small sized and brachycephalic dog with a strong robust skeleton, well-developed muscle mass, short hair, and short and flat snout . In commercial kennels, it is essential to obtain a normal biometric standard. Therefore, breeding dogs must be selected that are within the desirable zoo technical profile to ensure better reproductive efficiency.
In Guzerá cattle, OKUDA and others  sought to establish, via pelvimetry, an outline for the standard values of pelvic diameters, such as the true conjugate (TC) and superior and inferior bi-iliac diameters. Additionally, correlation between these pelvic and body measures, i.e., the withers height, was verified. This study showed that several pelvic dimensions presented a strong positive correlation with the height of the animal, thoracic circumference (THC), and body weight. Among these, the withers height was the measure that had the highest positive correlation to that of the superior bi-iliac diameter (SBID).
The use of radiographic pelvimetry represents an important tool for the selection of Nelore cows, which give birth easily because they have a good pelvic angle and diameter . However, pelvimetry performed using a pelvimeter and digital palpation are not applicable to dogs owing to anatomical implications. Thus, pelvimetry using radiography is a valuable method to evaluate the pelvic shape and diameter in dogs. Radiographic pelvimetry represents the mensuration of the distances and angles between pelvic structures, which can more precisely be performed using radiographic images. This is a routine procedure for evaluating the size of the pelvis in humans  however, this technique has also been used in sheep  and cows  to select the ideal females for reproduction based on their pelvic size.
Considering that French Bulldog is a brachycephalic and chondrodystrophic breed of increasing commercial interest in Brazil, the performance of studies on its reproductive anatomy, especially in females, is of great importance and will provide information on breeding characteristics. Thus, pelvimetric data on this breed should contribute to reducing economic losses associated with low reproductive efficiency .
The objectives of the present study were to measure the average pelvimetric values of French Bulldog bitches to establish an outline of the normal anatomical biometric standards of the pelvis and to verify the correlation between the external body and pelvic measurements, and between the external and internal pelvic measurements.
A total of 20 French Bulldog bitches of different ages, ranging from 2 to 4 years, were assessed, including nulliparous (n=3), primiparous (n=7), and multiparous (n=10) individuals, all of which were not pregnant during the study. Only animals with mature skeletons were included, considering that the closure of the epiphyseal plates of the ilium, ischium, and pubis occurs at approximately 4-6 months of age [7,8]. The animals were from the commercial kennel Grande Canafístula and from private breeders. They were fed with dry commercial canine food and water ad libitum.
The external body parameters measured was the external body measurements and weight of the bitches. The external body measurements included the cranial circumference (CC), measured at the zygomatic processes; the THC, measured along the contours of the thorax, tangent to the extremity of the olecranon tuberosity, and caudally to the withers; the abdominal circumference (AC), measured immediately cranial to the ilia; the withers height, measured from the dorsal extremity of the spinous process of the first thoracic vertebrae to the ground; and the body length (BL), measured from the cranial extremity of the scapulohumeral joint to the ischiatic tuberosity [3,9]. All these parameters were measured using a metric tape with a precision of 0.1 cm, while the animals were standing. The animals were weighed with an analogical scale, without restricting food or water intake .
The studied external pelvic parameters were the different pelvic widths, including the external bi-iliac diameter (EBID), measured between the lateral extremities of the right and left coxal tuberosities; external bi-ischiatic diameter (EBIsD), measured between the lateral extremities of the right and left ischiatic tuberosities; and the right and left external ilio-ischiatic diameters (REIID and LEIID, respectively), measured between the lateral extremities of the coxal and ischiatic tuberosities . External pelvic measurements were measured using a metric tape with a precision of 0.1 cm, while the animals were standing on an examination Table.
For the radiographic examination, Equimex X-ray equipment with a maximum potency of 200 milliampere was used. Radiographs of the pelvis and caudal portion of the lumbar column were obtained with the animals positioned in the right lateral and dorsal recumbency. The use of chemical restraint was not required. The focus film distance was 90cm to minimize the object-film distance and image magnification .
Bitches were carefully positioned in such a way that their pelvises were as close and as straight as possible in relation to the radiographic film to obtain symmetrical positions of the pelvis .
Measurements of pelvic dimensions were directly performed on radiographic images (accuracy level of the measurements was 0.5cm) using a millimetric ruler (Figure 1A and 1B). Then, the following measurements were obtained: TC = the distance between the promontory and the cranial portion of the pubic symphysis; diagonal conjugate (DC) = the distance between the promontory and the caudal portion of the pubic symphysis; vertical diameter (VD) = the vertical distance between the end of the cranial portion of the pubic symphysis and the sacrum; sacral diameter (SAD) = the vertical distance between the craniocaudal extremity of the sacrum and the symphysis; sagittal diameter (SGD) = the distance between the caudoventral extremity of the sacrum and the symphysis; coxal tuberosity diameter (CTD) = the horizontal distance between both coxal tuberosities; SBID = the horizontal distance between the ilia; inferior bi-iliac diameter (IBID) = the horizontal distance between both acetabula; and the bi-ischiatic diameter (BICD) = the horizontal distance between both ischiatic tuberosity.
In addition, several ratios were calculated, including the height/width (VD/IBID, SGD/CTD, and SGD/IBID), and the pelvic inlet and outlet areas. The pelvic inlet area (PIA) was calculated based on the methodology described by OCAL and others  using the equation (TC/2 + SBID/2)2 × π and the pelvic outlet area (POA) was calculated using the equation (VD/2 + IBID/2)2 × π .
External and internal pelvimetric values and body dimensions were described as means, standard deviations, and coefficients of variation. They were submitted to the Bartlett and Cramer-von Mises tests for homoscedasticity and normality, respectively. The parametric data were submitted to analysis of variance (ANOVA), and correlations between external body and pelvic measurements, height/width ratios, and inlet and outlet pelvic areas were calculated using Pearson’s correlation test. Differences were considered statistically significant at P values less than 0.05.
The results obtained in the present study are presented in the following tables and are based on the following parameters: mean of external body measures (Table 1), mean of external pelvic measures (Table 2), mean of internal pelvic measures during pregnancy (Table 3), mean of height: width ratios of the radiographic pelvic measures and pelvic areas (Table 4), and correlation between body and pelvic external measures and pelvic radiographic measures (Table 5).
The estimated correlation coefficients for the possible associations among external body and pelvic diameters and radiographic pelvic measures are shown in Table 5. The values found from the correlation analysis among the external body and pelvic measures and radiographic pelvic measures were, in general, low, varying from 0.03, for the correlation between CC and SGD/IBID, to 0.68, for the correlation between THC and SBID, EBIsD and PIA, and body weight and POA. Significant positive correlations (P < 0.005) were observed between the following variables: CC and SAD (r = 0.76 and P < 0.003), body weight and CTD (r = 0.75 and P < 0.005), body weight and EBIsD (r = 0.78 and P < 0.003), and body weight and POA (r = 0.75 and P < 0.005).
Pelvimetry is not usually applied in dogs; hence, there are limited studies that have been undertaken with this species. Direct pelvimetry was used for only one type of pelvis from different dog breeds [11,12]. A general view of the canine pelvis has been described and some examples of pelvic dimensions from different breeds have been cited . A dorsoventral flattening of the pelvis in two short legged, wide headed canine breeds was observed in the Pekingese and Sealyham Terrier .
To the best of our knowledge, the present study represents the first to use and compare indirect and radiographic pelvimetry involving the same dog breed. Although the number of examined females was small, it was similar to the number of assessed animals in previous studies in this area and it was adequate for allowing the performance of statistical analyses .
When analyzing data from body biometry, BL, withers height, and THC were in accordance with the standards described by Fédération Cynologique Internationale (FCI). Such observations demonstrated that the animals used in the present study were within the standards established for the French Bulldog breed, presenting characteristic body dimensions.
The mean body weight and standard deviation of the assessed dogs was 10.79 ± 1.79kg, which is in accordance with the official registry of the Brazilian Confederation of Cinofilia and FCI for the French Bulldog breed, which states 11kg as the average weight for this breed.
Regarding the pelvic shape, from analysis of the observed measurements, the pelvises of the female French Bulldogs were classified as being mesatipellic, with SBID and IBID similar to the TC diameter (Figure 2). Morphologically, the pelvis of the French Bulldog female tends to be of a rounded shape, considering its vertical axis, with a discrete narrowing of the caudal portion, as observed in other animals. In a similar study with Holstein cows, different types of pelvises (platypellic, mesatipellic, and dolichopellic) occurred within the studied animals, even though they belonged to the same breed .
In a study by Linde-Forsberg , pelvimetry was a technique found to be useful in dogs. In this study, the relation between the height and width of the pelvic canal was smaller in bitches with obstructive dystocia. It should, thus, be possible to estimate whether a bitch was likely to whelp or suffer from obstructive dystocia by taking X-rays of the pelvis and various pelvic measurements. However, the shape of the pelvis varies between breeds and before pelvimetry can become generally useful in clinical practice, more bitches of various breeds must have their measurements and angles determined, and an index for each breed should be calculated.
The evaluation of the correlation between external body and pelvic measures and internal body measures was performed to verify the possibility of using external pelvimetry as a tool to characterize the pelvis of female dogs, without the need to perform radiographic examination (radiographic pelvimetry), when it is not feasible. Our analysis showed the existence of significant positive correlations between several radiographic pelvic diameters, such as coxal tuberosity, BICD and PIA, and body weight and between SAD and CC. Therefore, body weight represents the most correlated parameter, compared to internal pelvic measures, even though it was influenced by other variables.
The same analysis indicated the existence of moderate significant positive correlations (r = 0.66) between external body measures and radiographic pelvic measures, as observed between TC and CC; between coxal tuberosity, superior bi-iliac and BICD and THC; between coxal tuberosity and withers height; and between POA and BL. A moderate correlation was observed between several external pelvic measures and radiographic pelvic measures, such as among DC and sagittal diameters and EBID and among TC, PIA, and EBIsD.
However, as observed in female buffaloes  and in Jersey cows , the correlation between external body and pelvic characteristics, especially withers height and EBID, which is more commonly correlated to TC, was low (r = 0.44) and not statistically significant (P >0.05). Correlation analysis indicated the existence of low positive correlation between body biometry and internal pelvic measures. Therefore, body biometry is not adequate for predicting the internal pelvic dimensions of French Bulldog females. According to Monteiro and others , in brachycephalic and mesaticephalic cats, body biometrics do not demonstrate good predictive value for determining internal pelvic measurements.
Low positive correlations were also observed between external pelvic measures (right and left BICDs) and all radiographic pelvic measures and between height/width ratios (VD/IBID, SAD/CTD, and SAD/IBID) and all external body measures.
It is important to study the pelvis as a tool for the early diagnosis of congenital pelvic alterations or as a feature to be evaluated by specific programs of reproductive management based on pelvimetric data.
The present study contributes data that can be used as a reference for the establishment of the reproductive management of French Bulldogs, to avoid breeding females that present unwanted pelvimetric measures. Once the pelvis shape is inherited , it is possible to advise breeders on how to breed their dogs based on pelvic X-rays of their animals, and to choose those with good pelvic shape, thus avoiding mating two dogs with poor pelvic shapes.
In conclusion, adult French Bulldog bitches can be classified as having a mesatipellic pelvis, and CC, SAD, coxal tuberosity, BICD, and PIA that are positively correlated to body weight. Thus, pelvimetry can be used as a tool to select dogs for breeding purposes, avoiding the utilization of animals that present unwanted pelvic dimensions.