
==== Front
Vet Med Sci
Vet Med Sci
10.1002/(ISSN)2053-1095
VMS3
Veterinary Medicine and Science
2053-1095
John Wiley and Sons Inc. Hoboken

10.1002/vms3.70010
VMS370010
Case Report
DOGS
Case Report
Craniofacial malformations in a stillborn mixed‐breed dog as a cause for dystocia
BERNARD et al.
Bernard Megan E. https://orcid.org/0009-0009-5245-6038
1 meb396@cornell.edu

Coffin Hannah R. 2
Taylor Ryan P. 2
Donnelly Callum G. 1
1 Department of Clinical Sciences College of Veterinary Medicine Cornell University Ithaca New York USA
2 Department of Population Medicine and Diagnostic Sciences College of Veterinary Medicine Cornell University Ithaca New York USA
* Correspondence
Megan E. Bernard, Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA.
Email: meb396@cornell.edu

11 9 2024
9 2024
10 5 10.1002/vms3.v10.5 e7001024 4 2024
11 1 2024
23 8 2024
© 2024 The Author(s). Veterinary Medicine and Science published by John Wiley & Sons Ltd.
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

Abstract

This case report describes the findings of craniofacial anomalies associated with dystocia in a mixed‐breed bitch. A bitch in labour was presented for evaluation of dystocia, and an emergency caesarean section was performed. Two pups with craniofacial abnormalities were delivered by hysterotomy. One pup was stillborn, with congenital anomalies including palatoschisis (cleft palate), cheiloschisis (cleft lip), an open fontanelle, and a narrow teardrop‐shaped skull. The second pup was delivered alive and had cheiloschisis. Craniofacial malformations are a reported cause of dystocia in the dog, usually due to obstruction. However, dystocia in the reported case is presumed to have developed because the pup's craniofacial malformations prevented stimulation of uterine contractions. To the authors’ knowledge, this is the first case report to describe craniofacial abnormalities affecting 100% of the litter and is the first known report to describe the relationship between craniofacial abnormalities and presumptive primary uterine inertia.

Dystocia in a mixed‐breed bitch was associated with congenital craniofacial abnormalities. Craniofacial abnormalities, including cranioschisis, palatoschisis, and cheiloschisis, affected the entire litter. These malformations contributed to the development of primary uterine inertia via inadequate stimulation of uterine contractions.

caesarean
cheiloschisis
congenital malformation
craniofacial
dystocia
inertia
obstetrics
palatoschisis
source-schema-version-number2.0
cover-dateSeptember 2024
details-of-publishers-convertorConverter:WILEY_ML3GV2_TO_JATSPMC version:6.4.8 mode:remove_FC converted:11.09.2024
Bernard, M. E. , Coffin, H. R. , Taylor, R. P. , & Donnelly, C. G. (2024). Craniofacial malformations in a stillborn mixed‐breed dog as a cause for dystocia. Veterinary Medicine and Science, 10 , e70010. 10.1002/vms3.70010
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pmc1 INTRODUCTION

Craniofacial malformations are an uncommon congenital disorder in dogs. When present, craniofacial malformations can vary in clinical severity, ranging from mild cosmetic defects such as cheiloschisis (cleft lip) to severe life‐limiting defects such as choanal atresia. A variety of congenital craniofacial malformations, many of which have concurrent brain or neural tube defects, have been described in dogs in veterinary literature (Marcolongo Pereira et al., 2021; Martínez et al., 2006; Nonato et al., 2019). Some of these defects are catalogued in the Online Mendelian Inheritance in Animal (OMIA) database, which details known genetic single‐locus variants contributing to these traits (Nicholas & Tammen, 2023). Examples include cranioschisis (OMIA 000237–9615), anencephaly (OMIA 000044–9615), and otocephaly (OMIA 001127–9615) (Marcolongo Pereira et al., 2021; Martínez et al., 2006; Nonato et al., 2019). Palatoschisis, or cleft palate (OMIA 000197–9615, OMIA 001714–9615), and cheiloschisis, or cleft lip (OMIA 000444–9615, OMIA 001140–9615), are the most commonly reported forms of craniofacial malformation seen in canine veterinary medicine (Nobre Pacifico Pereira et al., 2019; Noden & DeLahunta, 1985). Craniofacial development is a highly conserved developmental mechanism in mammals in which the tissues of the primary and secondary palates must develop, migrate, and fuse on midline to form the respective adult structures, including the lip, philtrum, nasal passages, incisive bone, hard palate, and soft palate (Noden & DeLahunta, 1985; Van den Berghe et al., 2010). Disruptions in this process often lead to failure in fusion, with the extent and phenotype of the failure ranging from mild cosmetic defects to severe life‐limiting defects (Van den Berghe et al., 2010). The aetiologies of these anomalies can include genetic, environmental teratogens, and nutritional causes, and may be multifactorial (Noden & DeLahunta, 1985; Van den Berghe et al., 2010). In dogs, a genetic basis is presumed the primary mechanism of cleft palate and cleft lip, as certain breeds with these anomalies are overrepresented, with up to 30% risk documented for brachycephalic breeds (Fawcett et al., 2019; Nobre Pacifico Pereira et al., 2019; Van den Berghe et al., 2010). The mechanism of inheritance of these genetic anomalies is unclear, and likely involves multiple genetic factors, although autosomal recessive inheritance has been documented (Moura et al., 2012; Nicholas & Tammen, 2023). Gene mutations implicated in the development of cleft lip and cleft palate in the dog include ADAMTS20 and DXL6 (Moura et al., 2012; Nicholas & Tammen, 2023).

Cleft lip and cleft palate in the neonate can be life‐threatening. Malformations of the lip and palate impede normal suckling and swallowing due to the communication between the nasal and oropharyngeal cavities and the neonate's inability to create suction to nurse (Nobre Pacifico Pereira et al., 2019). This puts the individual at risk of malnourishment and aspiration pneumonia. Patients with cleft palate and lip must be intensively medically managed until surgical options are available (Nobre Pacifico Pereira et al., 2019). Many neonates die or are euthanised because of the risks of these malformations.

Congenital craniofacial anomalies also pose clinical concern for the dam during parturition due to the risk for dystocia. The incidence of dystocia in dogs is low, approximately 5%, but certain populations such as brachycephalic breeds suffer a higher risk of obstructive dystocia due to maternal narrow pelvis and fetuses with large, wide heads (Forseberg, 2015). While maternal factors, such as primary and secondary uterine inertia, account for approximately 75% of cases (Forseberg, 2015), fetal factors can play an important role in dystocia. Significant fetal malformations, that is, anasarca, fetal monsters, and hydrocephalus, or fetal malposition, that is, transverse or breech presentation, will often result in obstructive dystocia (Darvelid & Linde‐Forsberg, 1994; Forseberg, 2015). The current case describes dystocia in a bitch due to presumptive primary uterine inertia associated with significant fetal craniofacial malformations.

1.1 Case summary

An approximately 2‐year‐old intact female primiparous mixed‐breed, bully‐type dog weighing 25 kg presented for evaluation of dystocia. The owners reported a 1°F rectal temperature drop 48 h prior and described green‐brown vaginal discharge approximately 12 h prior to presentation. The owners reported seeing no abdominal contractions in the 12 h prior to admission. The bitch had delivered no pups on her own. The breeding was unintentional, and the bitch had received no pre‐ or post‐breeding veterinary examination and was not up to date on vaccinations. No information regarding the sire of the litter was provided.

Transabdominal ultrasonography revealed a nonviable fetus (no heartbeat) near the pelvic canal, but not engaged, and in cranial presentation. Another fetus was evaluated with a normal heart rate ranging from 180–220 bpm (reference range 180–300 bpm (Forseberg, 2015)). There was no obstruction palpable on digital vaginal exam, and a weak Ferguson's reflex could be initiated. Point‐of‐care bloodwork was unremarkable (Table 1).

TABLE 1 Point‐of‐care haematologic and serum biochemical analyses of a bitch presented for evaluation of dystocia caused by craniofacial malformations of a stillborn puppy.

Parameter	Patient value	Reference range	
pH	7.445	7.32–7.38	
Na+, mmol/L	147.9	145–151	
K+, mmol/L	4.24	3.9–5.1	
Ca++, mmol/L	1.35	1.18–1.37	
Cl−, mmol/L	110	110–119	
Glucose, mg/dL	118	60–120	
HCT, %	50	42–57	
TS, mg/dL	7.6	5.4–7.5	
BUN, mg/dL	5–15	0–5	
Abbreviations: BUN, blood urea nitrogen; HCT, hematocrit; TS, total solids.

John Wiley & Sons, Ltd.

An emergency caesarean section with ovariohysterectomy was elected. Gastroprotectants (maropitant 1 mg/kg IV and pantoprazole 1 mg/kg IV) were given preoperatively, and anaesthesia was induced with propofol to effect. A lumbosacral epidural was administered with buprenorphine 5 mcg/kg and 0.125% ropivacaine, and the bitch was aseptically prepared for surgery. A midline incision into the abdomen was made, and the uterus was exteriorized. Two pups were delivered by routine hysterotomy. The first pup delivered from the right horn was resuscitated manually, and the second pup delivered from the body of the uterus was stillborn. Routine ovariohysterectomy was performed, and the patient recovered uneventfully from surgery.

The stillborn male pup was noted to have moderate meconium staining and significant craniofacial abnormalities, including a small teardrop‐shaped skull, cleft lip, cleft palate, and open fontanelle on the cranial midline of the skull (Figure 1a,b). The female littermate was mildly meconium stained and was also found to have a cleft lip, an open fontanelle, but no cleft palate (Figure 2). The live littermate weighed 397 g, within the normal range for a 25 kg bitch.

FIGURE 1 (a) Stillborn fetus with craniofacial anomalies delivered by c‐section. Note the meconium staining and cyanotic abdominal skin and caudal extremities. (b) Stillborn fetus with cleft palate.

FIGURE 2 Live born pup delivered by c‐section with unilateral cheiloschisis consisting of incomplete fusion of the left nare. Note the meconium staining.

The stillborn pup was submitted for necropsy, and the littermate and bitch were discharged to the care of the owners. Approximately 2 weeks later, the surviving pup was presented for evaluation of a ruptured eye and was diagnosed with aspiration pneumonia secondary to bottle feeding. The pup was managed medically at home, but later re‐presented emergently for acute neurologic symptoms, and was humanely euthanised. No further diagnostics were pursued.

Gross findings from necropsy confirmed the clinical diagnosis of cleft lip and cleft palate. The cleft was 6 mm wide, included the hard and soft palate, and extended to the upper lip with an incomplete union between the left and right aspect of the upper lip. This cleft defect continued to the midline of the nasal bridge. The bones of the calvaria (nasal and frontal bones) were incompletely fused along the median suture line, leaving an approximately 0.5 cm open fontanelle.

2 DISCUSSION

Congenital malformations are an uncommon but well‐reported mechanism of fetal dystocia. Fetal dystocia typically occurs in cases of fetal maldisposition or abnormal fetal development, but certain congenital anatomic abnormalities may also be contributing factors. Specifically, craniofacial abnormalities are reported to be associated with dystocia in many species, including cattle (Murugan et al., 2014), sheep (Muhammed et al., 2016), goat (Pandey, 2014; Raju et al., 2021), horses (Pannu & Singh, 2014), zebu (Jubara et al., 2021), and rhinoceros (Schaftenaar et al., 2011). Many of these reports describe craniofacial malformations associated with dystocia either due to the inability of the normal maternal pelvis to accommodate the size or shape of the fetus, or fetal malposition associated with the congenital abnormalities. Primary uterine inertia is typically attributed to maternal factors, but fetal impact on the development of primary inertia is underscored in cases of singleton litters, as the singleton provides insufficient stimulation to initiate labour (Forseberg, 2015). An important aspect of eutocia is the fetus’ ability to engage in the birth canal and stimulate expulsive contractions; failure to do so may result in dystocia (Johnston et al., 2001). Although caudal presentation is common and is not typically considered to be a cause of dystocia, in some cases when the first pup to be delivered is in caudal presentation, Ferguson's reflex is not initiated and dystocia may ensue (Forseberg, 2015). In the described case, the suspected mechanism of dystocia is partial primary uterine inertia due to fetal craniofacial malformation. The fetus in the current case did not have an oversized or obviously malpositioned head, as is typically described in dystocia associated with craniofacial abnormalities. Rather, it was found to have a small, tapered head with obvious facial malformations. Based on the passage of meconium, it is likely the pup was alive at the start of parturition. The meconium staining presence was likely a result of fetal hypoxemia as labour was initiated with little to no progress. If the fetus was presumed alive and unobstructed at the beginning of parturition but was not delivered, it follows that other fetal factors contributed to dystocia. We speculate that the small and tapered malformed head failed to engage the birth canal and trigger Ferguson's reflex. The small litter size in the current case may also have contributed in part to primary uterine inertia, however, progression to stage II labour suggests that this contribution was minor.

It is possible that medical management of dystocia with ecbolics would have resulted in the delivery of the pups. The bitch was found to have a weak Ferguson's reflex on digital exam 12 h after the onset of labour at the time of presentation. Due to both prolonged labour and poor response to digital palpation, medical therapy was considered inappropriate. Medical management would be considered in the absence of fetal death or distress. The prompt decision for surgical intervention resulted in the delivery of live progeny and a positive outcome for the bitch in dystocia.

Genetic abnormalities are considered the main cause for craniofacial malformations in dogs, with other causes including teratogenic toxins, viral infection, and nutritional deficiency. In the present case, genetic abnormalities are prioritised as the top differential. Genetic analysis of both offspring to identify potential genetic causes for the observed craniofacial malformations would have augmented the report. Environmental insults such as exposure of teratogenic toxins to the pregnant bitch may be an important differential in this case. Commonly used medications in veterinary medicine, such as corticosteroids, have known teratogenic effects and may result in a high incidence of midline defects, including cleft palate, when used during pregnancy (Hansen, 1999; Kaplan et al., 2018). However, as the patient's owners provided minimal medical or management history, any suspicion of teratology is speculative. Further differentials considered in the workup of congenital malformations include viral infections and nutritional deficiencies. Viruses such as canine herpesvirus have been associated with congenital defects in the dog (Percy et al., 1971), and specific congenital defects such as cerebellar hypoplasia in cats and cattle after infection with feline panleukopenia and bovine viral diarrhoea virus, respectively, are well reported (Grooms, 2004; Sharp et al., 1999). Although nutritional deficiencies are not common in populations of dogs fed complete and balanced commercial pet food, specific conditions such as folic acid deficiency during pregnancy may contribute to the development of cleft palate (Elwood & Colquhoun, 1997). Considering the broad spectrum of potential factors involved in the development of congenital defects, veterinary or genetic counselling is recommended to breeders who have had litters with congenital malformations. In the case where genetic abnormalities are suspected or confirmed as the primary cause for congenital defects, it is typically recommended to remove the parents from the breeding line. Where congenital defects are considered to be acquired due to non‐genetic factors, further veterinary oversight of breeding programs may help reduce incidence of teratogenesis during critical developmental periods for the pregnant bitch.

In conclusion, canine congenital craniofacial abnormalities may contribute to the development of non‐obstructive dystocia. Veterinary oversight of breeding programs can provide genetic counselling, pregnancy management, and prompt intervention during dystocia, which should benefit the producer in reducing neonatal losses secondary to these common problems encountered in dog breeding.

AUTHOR CONTRIBUTIONS

Megan E. Bernard: Conceptualization; Data curation; Investigation; Writing—original draft; Writing—review and editing. Hannah R. Coffin: Formal analysis. Ryan P. Taylor: Formal analysis; Writing—review and editing. Callum G. Donnelly: Conceptualization; Supervision; Writing—review and editing

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

FUNDING INFORMATION

The authors have no funding source to report

ETHICS STATEMENT

The authors confirm that the ethical policies of the journal, as noted on the journal's author guidelines page, have been adhered to. No ethical approval was required as this is a clinical case report with no original research data. Owner consent for use of clinical information as provided.

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.70010

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.
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