Pregnancy in Hystricomorpha: Gestational Age and Embryonic- Fetal Development of Agouti (Dasyprocta Prymnolopha, Wagler 1831) Estimated by Ultrasonography

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Theriogenology 78 (2012) 1278–1285 www.theriojournal.com

Pregnancy in Hystricomorpha: Gestational age and embryonic- fetal development of agouti (Dasyprocta prymnolopha, Wagler 1831) estimated by ultrasonography

F.C.A. Sousaa, F.R. Alvesb,*, E.A.M. Fortesc, M.S. Ferraza, A.A.N. Machado Júniorb, D.J.A. de Menezesd, M.A.M. de Carvalhoe a Animal Science Postgraduate Program, Federal University of Piauí, Socopo, 64049–550, Teresina, Piauí, Brazil b Federal University of Piauí, Department of Animal Science, Planalto Horizonte, 64900-000, Bom Jesus, Piauí, Brazil c Federal University of Piauí, Department of Morphology, Socopo, 64049–550, Teresina, Piauí, Brazil d Federal University of Campina Grande, Academic Unity of Veterinary Medicine, Jatobá, 58700-970, Patos, B. Paraíba e Federal University of Piauí, Department of Veterinary Morphophysiology, Socopo, 64049–550, Teresina, Piauí, Brazil

Received 18 August 2011; received in revised form 2 May 2012; accepted 20 May 2012

Abstract Thirty-one pregnant agoutis, between Days 9 and 103 of gestation (Day 1 ϭ day of detection of sperm in the vaginal smear), underwent B-mode ultrasonography; gestational sac diameter (GSD), crown-rump length (CRL), embryonic-fetal diameter (EFD), and placenta diameter (PD) were measured. There were positive correlations (P Ͻ 0.05) between GSD and CRL (r ϭ 0.98), GSD and PD (r ϭ 0.88), CRL and PD (r ϭ 0.86), days of gestation (DG) and CRL (r ϭ 0.85), and DG and PD (r ϭ 0.73). The gestational sac was first observed on Day 14. The embryo was first seen on Day 18 in 9/31 of pregnant agoutis and on Day 22 in 20/31 of pregnant agoutis. Heartbeats were detected from the Day 25 and placentas were observed in 100% of the animals from Day 25. Early limb bud and ossification of the fetal skull were identified on Days 27 (15/31) and 45 (24/31), respectively. Fetal orientation (head and body) was evident from Day 40, the stomach, liver and lungs were identified on Day 50, the kidneys were reliably seen only on Day 55, and the aorta and vena cava were seen on Day 70. The fetal bowel and the urinary bladder were the last structures to be observed (Day 85). Ultrasonography was effective for early pregnancy diagnosis in agouti and for obtaining information on embryonic and fetal structures that could be used to predict gestational age and birth, thereby contributing to their reproductive management in captivity. © 2012 Elsevier Inc. Open access under the Elsevier OA license.

Keywords: Dasyprocta spp; Hystricomorpha; Ultrasonography; Wildlife; Brazilian Cerrado

1. Introduction difﬁcult [1,2]. Reproductive events widely established in domestic animals [3,4] remain unknown in wild Determining gestational age and characterizing re- species, especially livestock and species with commer- productive behavior among wild species are usually cial interest [5,6]. The agouti (Dasyprocta spp) is a South American rodent that lives in forest habitats [7]. In the state of * Corresponding author. Tel.: (ϩ55 89) 3562 2535; fax: (ϩ55 86) 3562 1866. Piauí, as well as in other Brazilian regions, it was E-mail address: ﬂ[email protected] (F.R. Alves). established as an important source of animal protein,

0093-691X © 2012 Elsevier Inc. Open access under the Elsevier OA license. http://dx.doi.org/10.1016/j.theriogenology.2012.05.023 F.C.A. Sousa et al. / Theriogenology 78 (2012) 1278–1285 1279 but was exploited indiscriminately. Consequently, there period (approximately 12 h light and 12 h dark through- has been substantial reduction in the population density out the year) [28]. of this species in this region and throughout the country 2.2. Ultrasonography [8,9]. Numerous studies have been conducted to char- acterize reproductive physiology of the agouti [10–13]. Ultrasonographic examinations were performed They generally weigh approximately 1.5 to 2.8 kg [14] with a Pie Medical Scanner 100 LC, equipped with a and reach sexual maturity at 6 mo of age [15]. In recent multifrequency (5–7.5 MHz) microconvex transducer studies, the duration of the estrous cycle averaged 32.05 Ϯ (Pie Medical, Campinas, SP, Brazil). The agoutis were 4.17 days, with progesterone concentrations increasing not sedated or anesthetized and were restrained in dor- rapidly 24 h after detection of estrus [16]. Gestation sal recumbency. The ventral abdomen was shaved and ranges from 104 to 120 days, with one or two pups ultrasound gel was applied. Ultrasound examinations delivered per year [10] and mean birth weight of 147.6 were performed by four sonographers, specialists in the g [17]. area, with the same image calibration, and trained with Hystricognath rodents like agouti have unique pla- the same level of accuracy to obtain the images. The centation [18–20]. The placenta is spherical, divided animals usually remained relaxed during the whole into lobes separated by interlobar trophoblast, and lo- examination (ϳ45 min), and the environment was kept cated on the mesometrial side of the uterus [6]. The calm. subplacenta is a highly vascular structure [21], closely The examination started in the inguinal area, using related to the main placenta. The standard arrangement the anechoic urinary bladder as an acoustic window. of cytotrophoblast and syncytiotrophoblast, supported The examination continued along the abdominal and by lamellae of connective tissue, is similar to that in pelvic cavities to evaluate the topography and syntopy other species, including the guinea-pig, chinchilla, rock of the uterine horns. Identification of a gestational sac cavy, and agouti [6,22–24]. However, all information confirmed a diagnosis of pregnancy. Thereafter, gesta- were obtained from postmortem investigations by mor- tional age was evaluated by observing sonographic phologic descriptions, with a need for in vivo confir- markers, including embryonic development, placenta mation [6,13,25,26]. The objective of the present in- echogenicity, fetal skeleton, fetal heart pulsation, and vestigation was to use ultrasonography to observe fetal abdominal viscera [3]. features that could be related to gestational age in In all animals, an ultrasonographic evaluation was pregnant agouti (Dasyprocta prymnolopha). done once daily from Days 9 to 103. The following were measured: gestational sac diameter (GSD: largest 2. Materials and methods diameter of the gestational sac in a sagittal section); crown-rump length (CRL: from the cranial portion of 2.1. Animals the embryo-fetus to its caudal end); embryonic-fetal This research was authorized by the System for Au- diameter (EFD: largest diameter of the embryo and thorization and Information on Biodiversity (SISBIO) - fetus in a cross section); and placenta diameter (PD: the ICMBio/IBAMA, No. 20169–1. Thirty-one female ag- largest diameter of the placenta in a sagittal section). outis were used from the Center for the Study and The objective was to establish parameters related to Preservation of Wild Animals (NEPAS) of the Federal morphologic changes that would facilitate accurate pre- University of Piauí (Registration, No. 02/08–618). diction of gestational age and parturition date in this They were housed in four groups, with a 5:1 female- species. to-male ratio, and constant monitoring of the estrous The growth rates of GSD, CRL, EFD and PD were cycle. After mating, vaginal cytology was checked measured in each of the three-thirds of pregnancy, and thrice daily; the presence of sperm in the vaginal smear the means were compared using a Student’s t test. The was used to define Day 1 of gestation, as reported [27]. degree of linear association between variables (GSD Once a female was designated as having mated, she was and PD; CRL and PD) was assessed by determining separated and replaced by another female, to retain the 5:1 Pearson’s correlation coefficient. Furthermore, GSD ratio. Groups of animals were housed in pens that were and CRL were submitted to linear regression to estab- 400 ϫ 400 ϫ 200 cm (length ϫ width ϫ height) and fed lish their relationships with gestational age. For all rodent food and fresh vegetables, with ad libitum ac- statistical analyses, P Ͻ 0.05 was considered signifi- cess to water. They were exposed to a natural photo- cant. 1280 F.C.A. Sousa et al. / Theriogenology 78 (2012) 1278–1285

3. Results growth hindered measurements of the total diameter directly from the monitor image. 3.1. Gestational sac diameter 3.2. Crown-rump length The first uterine morphologic changes were observed on Day 9. The gestational sac had an initial diameter of The initial crown-rump length, on Day 18, was 1.57 Ϯ 1.23 Ϯ 0.07 cm. On Day 14, it was filled with liquid, 0.06 cm. In the first, middle and last thirds of pregnancy, confirming the beginning of pregnancy. In the first third of the CRL was 2.07 Ϯ 0.20, 3.21 Ϯ 0.75 and 8.38 Ϯ 0.51 pregnancy (Days 9–30), GSD was 3.27 Ϯ 0.87 cm. The cm, respectively. The embryo-fetal growth was clearly GSD in the middle third of pregnancy (between Days 31 progressive, with wide differences between the means of and 60) was 5.51 Ϯ 0.87 cm. There was a progressive the first (1.57 Ϯ 0.06) and last (10.8 Ϯ 0.09; Fig. 1b). increase up to Day 52, when the GSD measured 6.22 Ϯ Similar to GSD, the CRL was monitored for only 76 days 0.03 cm. From this point forward, development was more after mating. Thereafter, its size prevented viewing its rapid, with mean GSD of 10.39 Ϯ 0.63 cm at Day 63, and entirety to obtain accurate measurements. the last diameter measured of the gestational sac was 10.89 cm (Fig. 1a). 3.3. Embryonic-fetal diameter In the present study, the gestational sac was moni- Embryonic-fetal diameter measurements were ob- tored for only 76 days after mating. Thereafter, GSD tained from Day 21. The initial mean was 0.77 Ϯ 0.02

Fig. 1. Prenatal growth curves (regression curve) based on ultrasonographic measurements showing the: (a) gestational sac diameter (GSD), (b) crown-rump length (CRL); (c) correlation between GSD and placenta diameter (PD); and (d) between CRL and PD of agouti observed by ultrasonography during 76 d of pregnancy. F.C.A. Sousa et al. / Theriogenology 78 (2012) 1278–1285 1281

Fig. 2. Ultrasound images of agouti gestational development. (a) Uterine dilatation on Day 9 (circle). (b) Gestational sac with embryo on Day 18 (arrowheads). (c) Placenta on Day 25 (circle). (d) Limb buds (LB) visualized on Day 27 (arrows). (e) Early fetal orientation (solid line: head, body: dotted line). (f) Calcification of the skull (CSK) and mandible (MD) on Day 45. cm. In the first, middle and last thirds of pregnancy, the Age ϭ 5.26 ϫ CRL ϩ 18.359, R2 ϭ 0.9102, EFD was 1.01 Ϯ 0.13, 1.48 Ϯ 0.32, and 2.71 Ϯ 0.43 ϭ Ͻ cm, respectively. F7,79 334.28, P 0.05 3.4. Placenta diameter 3.6. Sonographic fetal organ visualization The placenta was first visualized on Day 21 (PD There was an initial increase in uterine volume ob- 2.22 Ϯ 0.09 cm). In the middle third of pregnancy, PD served on Day 9 in 3/31 animals and on Day 13 in Ϯ Ϯ was 2.75 0.32 cm, and in the last third, it was 3.49 12/31 animals (Fig. 2a). The gestational sac, an an- 0.23 cm. The PD progressively increased until Day 60, echoic structure, with a thin and hyperechoic wall, was Ϯ reaching a mean diameter of 4.71 0.12 cm. From this observed on Day 14 in 11/31 of the animals. The point forward, the PD decreased until the last measure- embryo was initially seen on Day 18 as an elongated Ϯ ment on Day 90 (3.31 0.08 cm). Until Day 60 of echogenic structure located eccentrically within the gestation, there were significant positive correlations gestational sac in 9/31 animals (Fig. 2b). On Day 22, between GSD and PD (r ϭ 0.88, P Ͻ 0.05; Fig. 1c) and this structure was already observed in 20/31 of pregnant between CRL and PD (r ϭ 0.86, P Ͻ 0.05; Fig. 1d). agouti. On Day 25, a fluttering echo within the embryo 3.5. Linear regression analyses was observed, characterizing the heartbeat and fetal Linear regression analysis of gestational age (in viability, seen in 20/31 of the animals. The placenta days) according to the diameter of the GSD and CRL was seen on Day 21 as a circular structure of hetero- (in cm) produced the following equations for Days 9 to geneous echotexture and hypoechoic wall in 20/31 of 76; Fig. 1a, b: the animals (Fig. 2c). On Day 25, it was seen in all animals. Limb buds (Fig. 2d) were detected on Day 27 Age ϭ 6.99 ϫ DGS ϩ 1.7877, R2 ϭ 0.9271, in 15/31 of the animals. The umbilical cord was seen ϭ Ͻ F2,47 419.47, P 0.05 after Day 30 as a long structure, hyperechoic and with 1282 F.C.A. Sousa et al. / Theriogenology 78 (2012) 1278–1285

Fig. 3. Sonographic fetal organ visualization in agoutis. (a) Lungs (LG), liver (LV) and stomach (*) on Day 50. (b) Spinal canal (SC) on Day 55. (c) Primordial kidney (circle) on Day 55. (d) Aorta (Ao) on Day 70. (e) Urinary bladder (UB) visualized on Day 85. homogeneous echotexture in 17/31 of the animals. The 4. Discussion fetal orientation (head and body) was evident in 15/31 of the animals on Day 40 (Fig. 2e). Calcification of the There are several issues regarding accurate detection skull was first seen on Day 45 in 24/31of the animals of gestational time in agouti. The day of detection of (Fig. 2f). The stomach, lung and liver were visualized sperm detection in vaginal smears was defined as “Day on Day 50 in 17/31 of the animals. The stomach ap- 1”. The duration of gestation was 103 days. Although peared as an anechoic cavity, whereas the lungs were other studies have suggested a range of 104 to 120 days more hyperechoic than the liver (Fig. 3a). The spinal [29,30], we inferred that this large range in length of canal was visualized on Day 55 in 14/31 of the animals gestation was due to failure in accurately determining and it was surrounded by the vertebral body, a highly “Day 1” or failure to detect early pregnancy losses. In reflective and acoustic shadow beyond the mineralized that regard, agoutis display estrus approximately 1 wk area (Fig. 3b). The kidneys were visualized on Day 55 after pregnancy loss [31]; if this was not detected, of gestation in 13/31 of pregnant agouti as a hypoechoic animals could mate again, resulting in incorrect assess- structure with a central anechoic pelvis (Fig. 3c). In ment of length of gestation. 13/31 of the animals, the aorta and caudal vena cava In the present study, the gestational sac was first were visualized on Day 70 (Fig. 3d). The fetal bowel seen on Day 9, with a diameter of 1.2 Ϯ 0.1 cm, when and urinary bladder (anechoic structure) were the last a 7.5 MHz transducer was used. Although some authors structures detected (Fig. 3e); they were first observed reported the presence of a gestational sac in dogs at 10 on Day 85 of gestation in 12/31 of the animals. From days of gestation [32–34], in most cases in dogs and this point onwards, there was only growth in volume of cats it was first detected from 17 to 19 days of gesta- these organs. The sonographic examination of organs tion, using a transducer with the same frequency as that was performed until the end of pregnancy, 103 Ϯ 0.16 used in this experiment [35–37]. days after mating. The main events related to organo- In this study, the gestational sac of the agouti was an genesis in agoutis are summarized (Table 1). anechoic spherical structure, with slightly hyperechoic F.C.A. Sousa et al. / Theriogenology 78 (2012) 1278–1285 1283

Table 1 Consistent with other domestic mammals and other Gestational period and organogenesis in agouti measured by rodents, most of the anatomical changes in agoutis ultrasonography. occurred after Day 30 days [19,36,45]. However, the Structure Day (%) (Ͼ60%) Animals heartbeat and the limb buds appeared on Days 25 and Increase in uterine volume 9 9.7 3 27, respectively [4]. 13 38.7 12 The placenta was observed on Day 25 of gestation as Gestational sac 14 35.5 11 Embryo 18 29 9 a circular structure with a hypoechoic wall and heter- 22 — 64.5 20 ogeneous echotexture. Placenta morphology was de- Fetal viability (heartbeat) 25 — 64.5 20 scribed for agouti [20] and paca (Agouti paca L) [25] Placenta 21 — 64.6 20 mesometrially located, discoidal to ellipsoid or globular 25 — 100 31 in shape and prominently lobulated, and largely vascu- Limb buds 27 48.4 15 Umbilical cord 30 54.8 17 lar, with characteristics similar to those observed in Fetal orientation (head and 40 48.4 15 other rodents, such as the guinea-pig (Cavia porcellus) body) [6] and capybara (hydrochaeris hydrochaeris) [12]. Calcification of the skull 45 — 77.4 24 There was progressive increase in the placenta up to Lung, liver and stomach 50 54.8 17 Spinal canal 55 45.2 14 Day 60 and a decrease in size from that point until Day Kidney 60 41.9 13 90. Corroborating this, a recent morphologic study Aorta, caudal vena cava 70 41.9 13 showed the presence of fully developed and vascular Fetal bowel and urinary 85 38.7 12 placenta in capybaras from Day 70 [18]. bladder Although the transition between the main placenta and subplacenta not been well defined, we suggest that during the sonographic evaluation, the subplacenta pro- margins, defined and easily measurable, similar to de- vided important contributions to identify the size of the scriptions made for bitches [34,38]. In rats, embryonic vesicles were round or oval structures of intermediate main placenta over the gestational development in the echogenicity in the lumen of the uterine horn on Days agouti. In fact, in the guinea-pig, the subplacenta 9 through 11 of pregnancy [39]. For wild rodents, e.g., reaches its maximum weight at 40 to 45 days and the European brown hare, the gestational sac was first gradually decreases in size thereafter [48]. Later, it was observed between Days 6 and 8 [40]. Otherwise, in reported that the agouti placenta regressed to 10% of other rodents, such as the guinea-pig, the gestational the weight of the main placenta and that it had com- sac was seen only on Day 23 [41–43]. pletely degenerated by 58 days [49]. The embryo was thin and adopting a C-like-shape on The placenta has been considered an area of high Day 18 and the embryonic-fetal length could be mea- metabolic activity [11] and important for trophoblast sured [3,44]. In moles, the embryo is seen within the invasion associated with the maintenance of pregnancy gestational sac from 150 to 163 days of gestation with in the guinea-pig, chinchilla and capybara [15].Inthe a “cigar shaped” or “curled layers” [45]. There was a present study, the placenta was regarded as a vascular significant increase in the embryonic growth rate after structure closely related to the fetus, consistent with the 22 days when the embryo could be identified in 64.5% positive correlation between embryonic-fetal length of the animals. An exponential increase in length was and placenta diameter. In contrast, it was suggested that also observed in pregnant bitches at 22 and 23 days of the subplacenta of the agouti (Dasyprocta leporina L) gestation [46,47]. Such a feature was also observed in secretes hormones into the fetal circulation [6]. hares from 11 to 20 days of gestation and rats at 16 days The beginning of organogenesis in domestic mam- [40]. mals was detected with ultrasonography ranging main Regression analysis results were similar to those in from 17 to 23 days of gestation, especially visualization other rodents, such as the European brown hare [40], of heartbeats [50,51]. Nevertheless, in the present for which regression analysis was used to predict the study, the distinction between head and the body was diameter and length of the embryo sac at 30 days. In only visible at approximately Day 40, when the embryo our evaluations, these data could be measured up to adopted a bipolar shape (fetal orientation) and the limb Day 76, which represents 70% of gestation in agouti. buds were visible [41,45,52,53]. Similar descriptions These results should be useful for estimating gesta- were made in a recent comparative study regarding tional age in agouti, although other studies of both embryonic development of South-American Hystrico- ultrasound and morphologic nature are necessary. morpha rodents, including the paca (Cuniculus paca), 1284 F.C.A. Sousa et al. / Theriogenology 78 (2012) 1278–1285 agouti (Dasyprocta leporina), capybara (Hydrochaeris procta aguti, Mammalia: Rodentia)]. Braz J Vet Res Anim Sci hydrochaeris), and rock cavy (Galea spixxi) [5]. 2005;42:130–4. In agoutis, the echogenicity of most abdominal [8] Carvalho MAM, Azevedo LM, Menezes DJA, Oliveira MF, Assis Neto AC, Cardoso FTS, Teixeira MCMO. Segmentos structures was observed later, despite numerous refer- anátomo-cirúrgicos arteriais do rim de cutia (Dasyprocta prym- ences that consider the stomach, bladder, skeleton and nolopha) [Anatomical-surgical arterial segments of the kidney kidney as the first structures visible by ultrasound ex- in agouti (Dasyprocta prymnolopha)]. Pesquisa Veterinária amination during organogenesis [54,55]. In fact, the Brasileira 2008;28:249–52. stomach, liver and kidneys in agoutis were only de- [9] Menezes DJA, Carvalho MAM, Assis-Neto AC, Oliveira MF, tected at Day 50. We suggest that the deposition of Farias EC, Miglino MA, Medeiros GX. Morfologia dos órgãos genitais externos do macho de cutia (Dasyprocta aguti. Lin- abdominal fat impaired early assessment of these and naeus, 1766) [Morphology of the external male genital organs other structures, such as the bladder and bowel which of agouti (Dasyprocta aguti. Linnaeus, 1766)]. Braz J Vet Res were only seen on Day 85, but in pregnant bitches can Anim Sci 2003;40:148–53. be seen on Day 32 [44,56]. [10] Guimarães DA, Ramos RSL, Garcia GW, Ohashi OM. The We concluded that ultrasonography was effective stimulatory effect of male agouti (Dasyprocta prymnolopha) on for identifying early pregnancy in the agouti and mon- the onset of female puberty. Acta Amazonica 2009;39:759–62. itoring organogenesis. Fetal and extraembryonic bio- [11] Heap RB, Ackland N, Weir BJ. Progesterone-binding proteins in plasma of guinea-pigs and other hystricomorph rodents. J metrics should be useful for staging gestation and pre- Reprod Fertil 1981;63:477–89. dicting birth in agouti, thereby contributing to their [12] Miglino MA, Carter AM, Ferraz RHS, Fernandes Machado MR. reproductive management in captivity. Placentation in the capybara (Hydrochaerus hydrochaeris), agouti (Dasyprocta aguti) and paca (Agouti paca). Placenta 2002; 23:416–28. Acknowledgments [13] Rodrigues RF, Miglino MA, Ferraz RHS, Morais-Pinto L. Pla- centação em cutias (Dasyprocta aguti, CARLETON, M.D.): We thank the Federal University of Piauí for logis- aspectos morfológicos [Placentation in agouti (Dasyprocta tical support and the Brazilian National Research Coun- aguti, CARLETON, MD): morphologic aspects]. Braz J Vet Res Anim Sci 2003;2:133–7. cil (CNPq) for financial support (process Number [14] Lange RR, Schmidt EMS. Rodentia – Roedores Silvestres. In: 483247/2009–0). Cubas ZS, Silva JCR, Catão-Dias JL, editors. Tratado de animais selvagens, Roca, 2007, pp. 475–91. [15] Roth-Kolar H. Beitrage zum einem aktionssystem des aguti. References Zeitschrift Tierpsychologie 1957;14:362–75. [16] Guimarães DA, Ramos RL, Ohashi OM, Garcia GW, Vale WG. [1] Drews B, Harmann LM, Beehler LL, Bell B, Drews RF, Hil- Plasma concentration of progesterone and 17␤-estradiol of debrandt TB. Ultrasonographic monitoring of fetal development black-rumped agouti (Dasyprocta prymnolopha) during the es- in unrestrained bonobos (Pan paniscus) at the Milwaukee trous cycle. Rev Biol Trop 2011;59:29–35. County. Zoo Biol 2010;30:241–53. [17] Lopes JB, Cavalcante RR, Almeida MM, Carvalho MAM, [2] Mayor P, López-Gatius F, López-Béjar M. Integrating ultra- Moura SG, Dantas-Filho LA, Conceição WLF. Desempenho de sonography within the reproductive management of the collared Cutias (Dasyprocta prymnolopha) Criadas em Cativeiro do Nas- peccary (Tayassu tajacu). Theriogenology 2005;63:1832–43. cimento até o Desmame em Teresina, Piauí [Performance of [3] Lenard ZM, Hopper BJ, Lester NV, Richardson JL, Robertson agouti (Dasyprocta prymnolopha) bred in captivity according to ID. Accuracy of prediction of canine litter size and gestational sex and parturition in Teresina, Piauí]. Revista Brasileira de age with ultrasound. Aust Vet J 2007;85:222–5. Zootecnia 2004;33:2318–22. [4] Lopate C. Estimation of gestational age and assessment of [18] Kanashiro C, Santos TC, Miglino MA, Carter AM. Growth and canine fetal maturation using radiology and ultrasonography: a development of the placenta in the capybara (Hydrochoerus review. Theriogenology 2008;70:397–402. hydrochaeris). Reprod Biol Endocrinol 2009;7:57. [5] Franciolli ALR, Ambrósio CE, Oliveira MF, Morini AC, Fa- varon PO, Machado MRF, Miglino MA. Os histricomorfos [19] Luckett WP, Mossman HW. Development and phylogenetic sul-americanos: uma análise comparativa do desenvolvimento significance of the fetal membranes and placenta of the African embriológico [South-American hystricomorphs: a comparative hystricognathous rodents Bathyergus and Hystrix. Am J Anat analysis of embryological development]. Pesquisa Veterinária 1981;162:265–85. Brasileira 2011;31:441–6. [20] Mess A. Evolutionary transformations of chorioallantoic pla- [6] Rodrigues RF, Carter AM, Ambrósio CE, Santos TC, Miglino cental characters in rodentia with special reference to hystricog- MA. The subplacenta of the red-rumped agouti (Dasyprocta nath species. J Exp Zoo 2003;299:78–98. leporina L). Reprod Biol Endocrinol 2006;4:31. [21] Miglino MA, Carter AM, Ambrosio CE, Bonatelli M, De Ol- [7] Fortes EAM, Carvalho MAM, Almeida MM, Conde Júnior AM, iveira MF, Dos Santos Ferraz RH, et al. Vascular organization Cruz NEA, Assis-Neto AC. Aspectos morfológicos da tuba of the hystricomorph placenta: a comparative study in the ag- uterina de cutias (Dasyprocta aguti, Mammalia: Rodentia) outi, capybara, guinea pig, paca and rock cavy. Placenta 2004; [Morphological aspects of the uterine tube in agouti (Dasy- 25:438–48. F.C.A. Sousa et al. / Theriogenology 78 (2012) 1278–1285 1285

[22] Davies J, Dempsey EW, Amoroso EC. The subplacenta of the [40] Roellig K, Goeritz F, Hildebrandt TB. Ultrasonographic char- guinea pig: an electron microscopic study. J Anat Lond 1961; acterisation of prenatal development in European brown hares 95:311–24. (Lepus europaeus PALLAS, 1778): an evolutionary approach. [23] King BF, Tibbitts FD. The fine structure of the chinchilla Reprod Fertil Dev 2010;22:448–58. placenta. Am J Anat 1976;145:33–56. [41] Sekulic´RS, LukacˇD, Drapšin M, Cˇ apo I, Laloševic´D, Nova- [24] Oliveira MF, Carter AM, Bonatelli M, Ambrosio CE, Miglino kov-MikicÁ. Ultrasonographic observations of the maturation MA. Placentation in the rock cavy, Kerodon rupestris (Wied). of basic movements in guinea pig fetuses. Eur J Biol 2009;4: Placenta 2006;27:87–97. 58–61. [25] Bonatelli M, Carter AM, Machado MRF, Oliveira MF, Lima [42] Tam WH. Steroid synthesis in vitro by the placenta of the MC, Miglino MA. Placentation in the paca (Agouti paca L.). guinea-pig, and progesterone concentrations in systemic and Reprod Biol Endocrinol 2005;3:1–12. uterine plasma. J Endocrinol 1977;73:483–9. [26] Conceição RA, Ambrósio CE, Martins DS, Carvalho AF, Fran- [43] Zhang J, Croy BA. Using ultrasonography to define fetal-ma- ciolli ALR, Machado MRF, Oliveira MF, Miglino MA, et al. ternal relationships: moving from humans to mice. Comp Med Morphological aspects of yolk sac from rodents of Hystrico- 2009;59:527–33. morpha subordem: paca (Agouti paca) and agouti (Dasyprocta [44] Luvoni GC, Beccaglia M. The prediction of parturition date in aguti). Pesquisa Veterinária BrasileiraBras 2008;28:253–9. canine pregnancy. Reprod Domest Anim 2006;41:27–32. [27] Tong TY, Goh VH, Tain CF, Mok H, Tsang S. Direct effects of [45] Roellig K, Drews B, Goeritz F, Hildebrandt TB. The long varying doses of oestradiol on early embryonic development in gestation of the small naked mole-rat (Heterocephalus glaber in vitro culture of rat’s two-cell embryos. Can J Physiol Phar- RU¨ PPELL, 1842) studied with ultrasound biomicroscopy and macol 2000;78:453–6. 3D-ultrasonography. PLoS ONE 6(3);6:e17744. [28] Ferraz MS, Menezes DJ, Pessoa GT, Cabral RM, Illera MJ, [46] Carniel P. Echographie de l’de l’appareil reproducteur de la Silva AR, Carvalho MAM, et al. Collection and evaluation of chienne. Point VétérinaireVet 1987;19:601–6099. epididymal sperm in captive agoutis (Dasyprocta aguti). Ther- [47] Wynn RM, Corbett JR. Ultrastructure of the canine placenta and iogenology 2011;75:459–62. amnion. Am J Obstet Gynecol 1969;103:878–87. [29] Nowak RM. Order Rodentia. Walker’s Mammals of the World, [48] Ibsen HL. Prenatal growth in guinea-pigs with special reference 6th ed. Johns Hopkins University Press. 1999, p. 1243–714. to environmental factors acting weight at birth. J Exp Zool [30] Pinheiro RM, Andrade SA, Cunha JN. Preservação e exploração 1928;51:51–91. de animais silvestres nativos: preá, Cutia e mocó [Preservation [49] Uhlendorf, Kaufmann P. Die Entwicklung des Plazentastieles and exploration of native wild animals: guinea pig, agouti and beim Meerschweinchen. Anat Histol Embryol 1979;8:233–7. rock cavy]. Caatinga 1989;6:28–49. [50] Concannon P, Tsutsui T, Shille V. Embryo development, hor- [31] Weir BBJ. Some observations on reproduction in the female monal requirements and maternal responses during canine preg- agouti, Dasyprocta aguti. J Reprod Fertil 1971;24:203–11. nancy. J Reprod Fertil Suppl 2001;57:169–79. [32] Aissi A, Alloui N, Slimani S, Touri S. Preliminary study of the early ultrasonic diagnosis of pregnancy and fetal development [51] Silva LA, Ginther OJ. An Eearly Eendometrial Vvascular Iin- in the dog. J Anim Vet Adv 2008;7:607–11. dicator of Ccompleted Oorientation of the Eembryo and the [33] Concannon PW. Canine pregnancy and parturition. Vet Clin Rrole of Ddorsal Eendometrial Eencroachment in Mares. Biol North Am Small Anim Pract 1986;16:453–75. Reprod 2006;74:337–43. [34] Yeager AE, Mohammed HO, Meyers-Wallen V, Vannerson L, [52] Di Salvo P, Bocci F, Zelli R, Polisca A. Doppler evaluation of Concannon PPW. Ultrasonographic appearance of the uterus, maternal and fetal vessels during normal gestation in the bitch. placenta, fetus, and fetal membranes throughout accurately Res Vet Sci 2006;81:382–8. timed pregnancy in beagles. Am J Vet Res 1992;53:342–51. [53] Kutzler MA, Yeager AE, Mohammed HO, Meyers-Wallen VN. [35] Davidson AP, Nyland TG, Tsutsui T. Pregnancy diagnosis with Accuracy of canine parturition date prediction using fetal mea- ultrasound in the domestic cat. Vet Rad 1986;27:109–14. surements obtained by ultrasonography. Theriogenology 2003; [36] Kim BS, Chang-Ho S. Time of initial detection of fetal and 60:1309–17. extra-fetal structures by ultrasonographic examination in Min- [54] Holst PA, Phemister RD. Onset of diestrus in the beagle bitch: iature Schnauzer bitches. J Vet Sci 2007;8:289–93. definition and significance. J Vet ResJ Vet Res 1974;35:401–6. [37] Yeager AE, Concannon PW. Association between the preovu- [55] Kang BK, Choi HS, Son CH, Shin CR, Seo DH, Park IC. latory luteinizing hormone surge and the early ultrasonographic Ultrasonographic appearance of the gestational structures detection of pregnancy and fetal heartbeats in beagle dogs. throughout pregnancy in pet dogs. I. Time of initial detection of Theriogenology 1990;34:655–65. the fetal and extra-fetal structures. Korean J Vet Clin Med [38] Luvoni GC, Grioni A. Determination of gestational age in 1997;14:279–86. medium and small size bitches using ultrasonographic fetal [56] Ko JS, Kim BS, Lee SA, Cho YT, Kim JP, Oh KS, Kim SH, measurements. J Small Anim Pract 2000;41:292–4. Kim JT, Park IC, Kim YH, Son CH, et al. Ultrasonographic [39] Ypsilantis P, Deftereos S, Prassopoulos P, Simopoulos C. Ul- appearance of the gestational structures throughout pregnancy trasonographic diagnosis of pregnancy in rats. J Am Assoc Lab in Shih-tzu bitches. Time of initial detection of the fetal and Anim Sci. 2009;48:734–9. extra-fetal structures. Korean J Vet Clin 2004;21:29–34.