Abstract
Objectives
The aim of this study was to investigate the appearance of body stalk anomalies (BSAs) and amniotic band disruption complex (ABDC) in cats (Felis catus), classify these congenital conditions using a system originally developed for humans and pigs, and provide new insights into the aetiopathogenesis.
Methods
Six cats suspected of having BSAs and/or ABDC were examined. The classification system for BSA, which includes eight types, was applied to these cases. Detailed observations were made regarding physical deformities, presence of amniotic adhesions and degree of impairment. A comparative analysis with similar conditions in pigs and humans was carried out to highlight differences and similarities.
Results
Two of the eight BSA classifications used in human and porcine congenital anomalies were detected in the six cats. In the studied cases, the degree of severity was lower than in pigs. The abnormalities associated with BSAs were attributed to the effect of amniotic bands on already formed organs or to the disruption of organ development, leading to a cascade of abnormal events.
Conclusions and relevance
This study is the first to describe and classify BSAs and ABDC in cats and provides valuable insights into these congenital anomalies. The findings highlight significant differences and similarities between cats and other species, particularly pigs. Understanding the aetiopathogenesis of these conditions is essential to improve clinical management and prognosis. Surgical correction and supportive care can improve the quality of life of affected cats, depending on the severity of the condition. Continued research and collaboration are essential to advance the prevention, diagnosis and treatment of BSAs and ABDC in cats, with wider implications for congenital anomalies across species.
Plain language summary
This study aims to explore body stalk anomalies (BSAs) and amniotic band disruption complex (ABDC) in cats (Felis catus). It classifies these conditions using a system developed for humans and pigs and seeks to understand their causes and management in cats. Six cats with suspected BSAs and/or ABDC were examined. The classification system for BSA, which includes eight types, was applied to these cases. Observations focused on physical deformities, amniotic adhesions and the severity of the conditions. Comparisons were made with similar conditions in pigs and humans. Two of the eight BSA classifications used in human and porcine congenital anomalies were detected in the six cats. In this study, the severity of the condition in cats was lower compared with pigs. The abnormalities were caused by amniotic bands affecting already-formed organs or disrupting organ development, leading to a series of abnormal events. This is the first study to describe and classify BSAs and ABDC in cats. It provides new insights into these congenital conditions and highlights differences and similarities with other species. Surgical correction and supportive care can help affected cats, depending on the severity of their condition. Continued research and collaboration are essential for better prevention, diagnosis and treatment of BSAs and ABDC in cats, with broader implications for congenital anomalies in other species.
Keywords
Introduction
Body stalk anomalies (BSAs) are complex defects of the body wall in which, in addition to a body wall anomaly, there are structural skeletal abnormalities, with or without craniofacial abnormalities, and the umbilical cord is abnormal, absent or rudimentary. 1 Complex body wall defects can occur in conjunction with amniotic band (AB) syndrome. 1 These defects often involve the abdominal and thoracic cavities, leading to significant structural abnormalities. AB syndrome is a rare congenital condition resulting from the entrapment of various embryonic parts by fibrous ABs within the maternal uterus. 1 These bands are formed by the rupture of the amniotic membrane while the chorion remains intact, creating strands that can constrict and disrupt normal development, resulting in anomalies due to disruption of normal morphogenesis, deformation due to distortion of established structures and disruption of structures already formed. 2 The resulting anomalies can range from minor constriction rings to severe deformities, amputations or craniofacial defects, depending on the timing, location and severity of the entrapment. AB syndrome is not usually associated with genetic factors and is considered a sporadic condition. 3 ABs are formed during early fetal development, typically at weeks 3–8 of gestation in humans, corresponding to the embryonic period. This is a critical window during which the amnion is developing, and the fetus is undergoing rapid organogenesis. Similar timing applies to cats, where the equivalent stage occurs at approximately days 10–20 of gestation.4,5 AB syndrome is characterised by isolated or multiple defects that are asymmetrical and do not follow a specific pattern. 6 In human medicine, there is extensive information on ABs causing congenital diseases.2,7,8 Amniotic constriction bands have been suggested as a possible cause for the intrauterine amputation of a porcine head. 9 To our knowledge, the two documented sporadic cases of AB syndrome in animals are in a rhesus monkey 10 and in a pig. 1
AB syndrome is a broad term that refers to a highly variable spectrum of congenital anomalies caused by fibrous bands from the ruptured amnion binding parts of the developing fetus. 1 AB sequence, on the other hand, is considered a more precise term. It refers to the sequence of events and resulting anomalies that occur because of the presence of ABs. 11 The term ‘sequence’ emphasises that these anomalies are secondary to a primary event, which leads to a cascade of developmental disruptions. ABs can restrict blood flow and affect the growth of organs and/or body parts, resulting in malformations such as deformities, amputations and craniofacial abnormalities. In AB syndrome and the AB sequence, the ABs are the known aetiology for all processes; however, they can cause a wide range of anomalies that vary depending on the time the AB acts, whether the disruption is to an already developed structure or whether it disrupts the developmental process. The AB sequence is considered when the AB interrupts the development of a structure, interfering with the developmental process and causing a cascade of events as a result. In contrast, AB syndrome includes a wide range of anomalies caused by the AB acting on an already formed organ, causing constriction, amputation or deformation. AB syndrome and AB sequence are part of the amniotic band disruption complex (ABDC).
As a result of the peculiarities of cat parturition, it is challenging to determine the appearance of body wall closure defects, such as BSA and/or ABDC. In cases where kittens have a body wall closure defect, the mother may consume the eviscerated organs, making it difficult to detect these conditions. Even when such defects are observed during caesarean sections in a clinical setting, they are often not reported or recorded. Dead animals are typically discarded, and live animals with severe defects may be euthanased. The lack of study and reporting does not imply that these conditions are rare or of no clinical or scientific interest. The aim of this study was to examine several cases of body wall defects in cats to classify them and to evaluate the presence of ABs, providing a comprehensive analysis of congenital anomalies.
Materials and methods
This study was an observational cadaveric study. Six cats with body wall closure defects and/or AB presence were included. The cats’ characteristics are shown in Table 1. All animals were obtained in accordance with European Union regulations (Directive 2010/63/EEC) and Spanish legislation (RD 53/2013). The study was carried out at the Laboratory for the Study of Congenital Malformations, located in the Departmental Section of Anatomy and Embryology, School of Veterinary Medicine, Universidad Complutense de Madrid, Madrid, Spain. Comprehensive gross evaluations of the six specimens were carried out using conventional anatomical methods. The study also included radiographic examinations and axial CT scans as well as three-dimensional reconstruction to further characterise the anomalies. Animals were diagnosed and graded for BSA according to the criteria established by Martín-Alguacil et al12,13 in the pig and in humans. 14 Cases were classified according to the diagnostic tool developed for BSA in pigs (Figure 1). 13
Data for the six cases detailing sex, weight, length, defect size, breed, delivery type, maternal age, litter size, gestation and mating type
BWD = body wall defect; V-C = length of vertex cauda
This modified decision tree, created by Martin-Alguacil et al, 13 assists in the diagnosis of body stalk anomaly (BSA), which is characterised by an abnormal umbilical cord, based on various structural anomalies and defects. It guides the user through a series of decisions, starting with the presence of anal atresia, genital and/or urinary defects, and branching out to specific types of structural anomalies. Each path leads to a specific BSA type diagnosis
Results
A summary of the abnormalities observed in the six cats is provided in Table 2, with cases illustrated in Figure 2. ABs were identified in cases 2 and 3. In case 2, amniotic adhesions were observed at the site of the cranial dysraphism defect and on hepatic lobes trapped within the extraembryonic coelom (Figure 3a), while in case 3, adhesions were noted in the occipital region. Case 6 presented with epidermolysis bullosa in the occipitocervical region (Figure 3b). Structural spinal defects were observed in cases 2, 4 and 5 (Figures 4 and 5a,b). Arthrogryposis was seen in cases 1 (Figure 5c), 2–4 and 6, and ectrodactyly in cases 2 (Figure 6a) and 4. A structural limb defect – left forelimb amelia – was identified in case 5 (Figure 6b). Craniofacial anomalies were present in cases 2, 3 and 4, including cleft palate in cases 2 and 3, and cleft lip and palate in case 4.
Summary of the anomalies described in the six studied cases and diagnosed as body stalk anomaly (BSA) and amniotic band disruption complex (ABDC)
Case 1 presented with an abdominal wall defect and arthrogryposis in both hindlimbs that was diagnosed as an omphalocele. Case 2 exhibited an abdominal defect, structural spinal abnormalities, non-structural defects in both fore- and hindlimbs, and craniofacial defects, and was diagnosed as BSA type VIII and ABDC. Case 3 had no abdominal wall defect but displayed non-structural defects in the forelimbs, craniofacial defects and an AB attached to the occipital region. This case was diagnosed as ABDC. Case 4 demonstrated an abdominal defect, spinal structural anomalies, non-structural limb defects in the fore- and hindlimbs and craniofacial defects, and was diagnosed as BSA type VIII and ABDC. Case 5 showed thoracoabdominoschisis and structural defects of the spine and limbs, and was diagnosed as BSA type V. Case 6 presented with an abdominal wall defect and arthrogryposis in both hindlimbs, and was diagnosed as an omphalocele and ABDC
AA = anal atresia; AB = amniotic band; Ab = abdominoschisis; BWA = body wall anomaly; CD = cardiac defects; CRA/FA = cranial anomaly and/or facial anomaly; DUV = dispersed umbilical vessels; KLS = kypholordoscoliosis; LA = limb anomaly; OD = other defects; S = scoliosis; SCD = spinal/cranial dysraphism; SPA = spinal anomaly; SUA = single umbilical artery; THAb = thoracoabdominoschisis; UCA = umbilical cord anomaly; UGD = urogenital defects
(a) Left lateral view of case 1 with abdominoschisis and arthrogryposis of the hindlimbs (arrows). (b) Left lateral view of case 2 with abdominoschisis. Note the amniotic adhesions to the cranial dysraphic defect (arrow), the defects in the extremities and the anomalous rotation of the head to the right. (c) Left lateral view of case 3. There is arthrogryposis of the forelimbs, a cranial dysraphic defect to which the amnion is attached (arrow), and exencephaly and exophthalmia. (d) Left lateral view of case 4 affected by abdominoschisis, defects in all four limbs, craniofacial defects and exencephaly (arrows). (e) Left laterodorsal view of case 5 affected by thoracoabdominoschisis, kypholordoscoliosis and amelia of the left forelimb (arrow). (f) Left lateral view of case 6 affected by abdominoschisis and hindlimb arthrogryposis (yellow arrow). Note the cutaneous defect in the occipitocervical region (red arrow)
(a) Ventral view of case 2 showing the adherence of the amnion to the cranial dysraphic defect and to the hepatic lobules located in the extraembryonic coelom (arrows). (b) Dorsal view of the occipitocervical region of case 6 showing epidermolysis bullosa (arrows)
Structural spinal defects observed in cases 2 and 4: (a) right dorsolateral view of the thoracic–cervical segment of the spine of case 2 on three-dimensional volume rendering (VR) CT reconstruction showing the occipitoatlantoaxial malformation (arrows) causing torticollis; and (b) right dorsolateral view of the spine of case 4 on three-dimensional VR CT reconstruction showing the presence of hemivertebrae (arrows) at the thoracic level and costal deformities
(a) Ventrodorsal radiograph of case 2 showing a structural malformation in its spine at the occipitoatlantoaxial level, causing torticollis (arrow). (b) Radiograph of case 5 showing the folding of its spine (kypholordoescoliosis) corresponding to structural defects in its spine (arrow). (c) Laterolateral radiograph of case 1 showing arthrogryposis in its hindlimbs (the plantar surface is dorsally directed) (arrows)
Skeletal defects in the limbs: (a) palmar view of the end of the right forelimb of case 2 showing ectrodactyly of fingers I and II; and (b) left ventrolateral view of case 5 showing amelia of the left forelimb (arrow)
Discussion
BSA is characterised by defects in the body wall, skeletal abnormalities and umbilical cord anomalies. A classification system for porcine BSA has been proposed, categorising cases according to the specific types of body wall and skeletal anomalies.12,13 Russo et al 15 identified two distinct phenotypes in BSA: placentocranial adhesion and placentoabdominal adhesion. Martín-Alguacil 14 suggested that cranial, abdominal and cranioabdominal phenotypes may overlap in BSA cases. Schistosomus reflexus (SR), as traditionally described in veterinary medicine, includes features such as inversion of the spine, exposure of abdominal viscera due to a ventral abdominal wall fissure, ankylosis of the pelvic limbs, abnormal positioning of the thoracic limbs adjacent to the skull and hypoplasia of the lungs and diaphragm.13,16 –18 These abnormalities are consistent with the definition of BSA, originally established in humans and later in pigs. In the literature, two cases of SR have been described in cats.17,19 The first case 17 involved thoracoabdominoschisis with anal atresia, and spinal and limb structural defects, aligning with BSA type I.12,13 The second published case 19 presented with abdominoschisis and structural spinal defects, consistent with BSA type VIII.12,13 Although both cases were diagnosed as SR, the severity of each case was very different, representing the most and least severely affected types within the BSA grading system. The term SR is inappropriate in contemporary clinical practice as it is outdated and encompasses a wide range of anomalies with varying degrees of severity, as shown in the cases above.17,19
In this study, three cases were diagnosed with BSA, two with type VIII and one with type V, and two of them also had ABDC. The remaining three cases were diagnosed, one with omphalocele, one with ABDC and one with both omphalocele and ABDC. Omphalocele is characterised by a central defect in the abdominal wall through which abdominal organs herniate, covered by a membrane, with the umbilical cord inserted into this membrane. In contrast, gastroschisis is a full opening in the abdominal wall without any membranous cover. It is usually a small and isolated anomaly on the side of the umbilical cord. 18 In all cats examined, except for case 3, the umbilical cord was abnormal, with umbilical vessels scattered across the amniotic membrane. One cat (case 1) presented with a single umbilical artery and a single umbilical vein. Russo et al 15 also noted two umbilical vessels in eight cases enabling the placenta–abdominal adhesion phenotype. Proper closure of the ventral abdominal wall and the embryonic folding process is crucial for normal umbilical cord development, and disruptions in this process lead to an abnormal umbilical cord. 1 Three cats in this study were diagnosed with BSA, all displaying an overlapping cranioabdominal phenotype. Although some authors report no sex predilection in BSA, 20 Martin-Alguacil et al 13 observed in their porcine study that 77% of affected animals were female, with 82% of cats with the abdominal phenotype, 64% of cats with the cranial phenotype and 100% of cats with the overlapping cranioabdominal phenotype being female. In our study, among the three cats diagnosed with an overlapping cranioabdominal BSA phenotype, two were female and one was male.
The clinical presentation of ABDC has been classified by Singh and Gorla 8 into four main categories: constrictive rings, limb defects, neural or spinal defects and craniofacial defects. There are two main theories regarding the pathogenesis of ABDC, known as the ‘extrinsic’ and ‘intrinsic’ theories. The intrinsic model 21 suggests that both the abnormalities and the fibrous bands originate from a disruption in the developing germinal disc of the early embryo. In contrast, the extrinsic model 22 suggests that birth defects result from the action of fibrous ABs. Higginbottom et al 23 noted that the specific abnormalities observed can be explained by the timing of the rupture. Although the mechanism of constriction and vascular disruption can explain disruptive birth defects, such as limb amputations and body wall defects, as reported by Al-Qattan 24 and Chen et al, 25 it does not readily explain developmental anomalies. Examples of such anomalies include imperforate anus, 26 polydactyly, 27 septo-optic dysplasia 28 and cleft lip and palate. 29 However, ABs are known to cause a spectrum of limb defects, including ectrodactyly. 30 Based on clinical and experimental research, Lockwood et al 31 proposed that ABDC may not be the consequence of AB formation, but rather the result of a multifactorial process responsible for developmental malformations and fetal ectodermal and mesenchymal disruption, in which ABs are a late reparative event with little or no pathogenic significance. 31
In addition to the controversy about the aetiopathogenesis of BSA and ABDC, anatomical and embryological criteria have been used to classify and diagnose these processes in the cat. These criteria were first used in humans and pigs.12 –14 According to Rittler et al, 32 limb anomalies are classified according to their embryological origin. Structural anomalies result from embryological defects and include conditions such as amelia and phocomelia of the pelvic limbs. In contrast, non-structural anomalies are associated with factors such as ABs and/or fetal movement restriction, resulting in conditions such as arthrogryposis. The same criteria were used for spinal, craniofacial and internal organ defects. Interruptions in blood supply to certain regions during early development can lead to abnormal growth or failure of vertebral segmentation, as seen in hemivertebrae. The spinal anomalies identified in cases 2, 4 and 5 were structural spinal defects and were diagnosed as BSA. Embryonic movement is known to stimulate joint formation and development. In arthrogryposis, joint contractures result from a combination of musculoskeletal underdevelopment and mechanical factors that impede normal limb movement. 33 If the AB compresses peripheral nerves, it may disrupt the development or function of motor neurons, resulting in neuromuscular dysfunction that further limits fetal limb movement 34 and contributes to arthrogryposis. Other examples of non-structural anomalies include phocomelia of the thoracic limbs, ankylosis and anomalous rotation. 12 Non-structural limb anomalies included arthrogryposis in cases 1–4 and 6, and ectrodactyly in cases 2 and 4. Amelia in the left forelimb was the only structural limb anomaly and was observed in case 5. ABs may be present, as in cases 2 and 3, and may be confined to the skin or soft tissue, as in case 3, or may extend deep into the tissue, as in case 2. In case 6, the epidermolysis bullosa observed in the occipitocervical region is characterised by lysis of the suprabasal epidermal cells, leading to blister formation even after minimal trauma. 31 The association of epidermolysis with ABDC is evidence that ABDC is a consequence of epiblastic damage affecting both the amnion and the embryo. 35
Atypical craniofacial abnormalities, such as encephalocele, facial clefts and cleft lip/cleft palate, may occur in cases of ABDC. 8 The presence of midline cleft palate in cases 2, 3 and 4 can be explained by the action of ABs during early embryonic development.6,36 Palatoschisis caused by amniotic bands is different from clefts that occur due to the failure of structures to migrate or converge at the midline, which is the typical cause of most clefts. 37 Bamforth 38 identified a subset of ABDC cases with additional findings not consistent with the classic ABDC mechanism, including cleft lip and palate, congenital heart defects and renal anomalies, all of which are malformations representing developmental abnormalities. These observations have fed into the ongoing debate about the pathogenesis of ABDC and the role of fibrous bands in causing these birth defects. In this study, other examples of developmental abnormalities that cannot be explained by the mechanisms described for ABDC include the cardiac and genitourinary defects in case 5 and bilateral cryptorchidism in cases 1 and 4. These may represent a malformative sequence initiated earlier in development. The craniofacial clefts in case 2, combined with amniotic adhesion to the cranial dysraphic defect and hepatic lobes within the extraembryonic coelom, can be explained by the temporally and spatially coincident mesenchyme, which is susceptible to adhesion. Weinstein et al 39 reported a novel variation of complex craniofacial clefts and bands connecting ipsilateral hands to facial clefts, concluding that this type of adhesion strongly supports the intrinsic and adhesion theories of AB syndrome aetiology. Robin et al 40 also reported a case showing multiple congenital anomalies typical of ABDC alongside additional findings that do not align with the extrinsic model. These resembled features in a case described by Guion-Almeida and Richieri-Costa, 41 suggesting a potentially unrecognised syndrome. They concluded that at least a subset of ABDC cases – particularly those with associated malformations such as cleft lip and palate – may have a genetic basis. Therefore, the two processes included in the ABDC complex – the AB syndrome and the AB sequence – likely represent distinct malformative mechanisms explaining the anomalies described in this study.
Conclusions
Only 2/8 BSA classifications – originally developed for human and porcine congenital anomalies – were detected in the six cats. The characteristic abnormalities observed in BSA can be explained by either the action of ABs on already-formed organs or by the interruption of the development and formation of an organ or part of the body, leading to a cascade of abnormal events. In some cases, surgical correction of deformities may be possible, especially if the condition is diagnosed early. Surgical intervention can include removal of constriction bands and repair of associated defects. The prognosis for cats affected by BSA and/or ABDC varies widely, depending on the severity of the condition. Although mild cases may enjoy a good quality of life with appropriate care, severe cases may require euthanasia if the deformities significantly impact the cat’s ability to function. The clinical interest in BSA and ABDC in cats spans genetic research, understanding pathophysiological mechanisms, improving clinical management and leveraging comparative studies to enhance knowledge of BSA and ABDC across species. Collaboration across disciplines is key to advancing the prevention, diagnosis and treatment of this complex congenital condition.
Footnotes
Acknowledgements
The authors would like to thank Pedro Plaza Serrano for his help with the three-dimensional reconstruction of the diagnostic scans taken at DB Diagnóstico por Imagen, Alcorcón, Madrid.
Conflict of interest
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
Ethical approval
The work described in this manuscript involved the use of non-experimental (owned or unowned) animals. Established internationally recognised high standards (‘best practice’) of veterinary clinical care for the individual patient were always followed and/or this work involved the use of cadavers. Ethical approval from a committee was therefore not specifically required for publication in JFMS. Although not required, where ethical approval was still obtained, it is stated in the manuscript.
Informed consent
Informed consent (verbal or written) was obtained from the owner or legal custodian of all animal(s) described in this work (experimental or non-experimental animals, including cadavers, tissues and samples) for all procedure(s) undertaken (prospective or retrospective studies). No animals or people are identifiable within this publication, and therefore additional informed consent for publication was not required.
