Introduction

Cases of conjoined twinning in veterinary medicine are exceedingly rare. In this report, we present a dog with supernumerary organs and structures that we suspect suffered from parasitic twinning or caudal duplication. Because these cases are rare, reporting cases that received treatment is important to know more about these conditions.

Case Report

A 6 mo old 13.5 kg (29.7 lb) male intact American Staffordshire terrier was referred to the Auburn University Small Animal Veterinary Teaching Hospital with a history of a supernumerary pelvis and associated pelvic limbs and malodorous discharge from a supernumerary prepuce and penis. At birth, the supernumerary pelvis, limbs, and penis on the right side of the dog were noted cranial to the primary pelvic limb and all four pelvic limbs were equal in size. Four other littermates were normal and at 6 mo of age, slightly larger in size. The primary pelvic limbs functioned normally and developed in proportion to normal growth. The supernumerary limbs did not develop as rapidly. The malodorous discharge, both feces and flatulence, from the supernumerary penis was life-long and the odor would reportedly improve with antibiotic therapy. The dog urinated and defecated normally from its primary penis and anus. No urination had ever been identified from the supernumerary penis, and the supernumerary anus had atresia ani at birth. The owner’s expectation was control of the odor and not surgical intervention of the supernumerary pelvis.

On presentation to the Auburn University Small Animal Veterinary Teaching Hospital, physical examination revealed a supernumerary pelvis and associated pelvic limbs on the right side of the dog, cranial to the primary right pelvic limb. A vestigial tail was noted with an imperforate anus on the supernumerary pelvis. A supernumerary prepuce and penis were appreciated on the right ventral abdomen (Figure 1). An inguinal hernia was noted caudal to the supernumerary prepuce on the right side. When the area was palpated, contents of the hernia could be pushed into the abdomen. Palpation resulted in flatulence and malodorous discharge from the supernumerary prepuce. One descended testicle was palpated in the primary scrotum. The primary right pelvic limb could not achieve a normal range of motion due to the supernumerary pelvic limbs; however, the dog was able to ambulate well despite this. With forward motion of his primary right pelvic limb, the supernumerary pelvic limbs would move, with the left moving caudally and right moving cranially. Motion of the supernumerary limbs was attributed to displacement by his primary right pelvic limbs, rather than conscious motion of the supernumerary limbs. The vestigial tail would actively wag when the dog was excited.

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Clinicopathologic abnormalities included an anemia (4.44 × 10⁶ red blood cells per µL [reference range, 6.02–8.64 $\times$ 10⁶ red blood cells per µL]; hemoglobin, 9.6 g/dL [reference range, 13.1–20.1 g/dL]; hematocrit, 30.1% [reference range, 38.7–59.2]), hypoalbuminemia (2.6 g/dL; reference range, 3–4.3 g/dL), low blood urea nitrogen (8.3 mg/dL; reference range, 9–34 mg/dL), and low creatinine (0.4 mg/dL; reference range, 0.5–1.6 mg/dL). Urine specific gravity was 1.019 and a mild proteinuria was seen (32.4 mg/dL).

Radiographic findings included the presence of a second pelvis at the level of L5, with paired ilia and ischia (Figures 2, 3). No pubis or sacrum were identified on the supernumerary pelvis, and the ilial wings appeared fused proximally. Two formed hind limbs were seen to articulate with this pelvis. Focal loss of the right body wall at the attachment of the supernumerary pelvis was noted. A second os penis was appreciated on the right lateral body wall. A suspected diverticulum of the colon was seen extending towards the supernumerary pelvis. The lumbar vertebrae caudal to L2 were malformed with scoliosis present towards the right. The malformed lumbar vertebrae had two spinous processes.

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Ultrasound findings included an enlarged left kidney, absence of the right kidney, and a single descended testicle in the primary scrotum. An intra-abdominal testicle was located adjacent to the urinary bladder. The primary colon was displaced dorsally by a second distended segment of colon. Small intestine was identified entering the distended supernumerary colon. Irregular areas of mixed echogenicity were noted in the caudal abdomen.

A computed tomography scan with excretory urogram was performed. Neuromuscular abnormalities included rotation of the spinal canal in a clockwise fashion with right-sided deviation from L2-L7, an accessory pelvis with two associated hind limbs, and a foreshortened sacrum. No osseous continuity was noted between the accessory pelvis and the primary spinal column of the dog (Figure 4). The hind limbs attached to the accessory pelvis appeared well developed. At L4-L5, a linear soft tissue opacity extended from the right vertebral foramen through the abdominal wall and into the accessory pelvis. There was duplication of the transverse process of L5 on the right side with incomplete fusion of the dorsal lamina in multiple lumbar vertebrae. The dorsal paraspinal musculature on the right was smaller than the contralateral side starting at L2. Only one kidney was identified located on the left side, and the ureter was followed to the urinary bladder (Figure 4). The urethra of the accessory pelvis was connected to the gastrointestinal system. A second colon extended to the accessory pelvis and communicated with the accessory urethra. Two masses were unidentifiable, one at the level of L3 on the right side and another at L4-5 on the right side.

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Based on the diagnostic findings, an exploratory laparotomy was performed to remove the connection between the supernumerary penis and GI tract. The dog was premedicated with dexmedetomidine (5 µg/kg) and morphine (0.37 mg/kg) intramuscularly and induction was achieved with propofol (3.7 mg/kg) IV. The dog received carprofen (3.7 mg/kg) subcutaneously and an epidural of morphine (0.07 mg/kg) and bupivacaine (0.55 mg/kg). Cefazolin (22 mg/kg) was administered IV q 90 min intraoperatively.

Exploratory surgery was performed via a ventral midline incision, curving parapreputially to the right between the two prepuces. At the entry of the ileum into the colon, two ceca were noted, each with a separate colon (Figure 5). One colon extended to the primary anus of the dog; the second colon extended to the supernumerary pelvis and was fluid filled and dilated with gas. A mass was noted in the normal area for a right kidney. A renal artery and vein were identified entering the mass, and what grossly appeared to be a severely dilated ureter was seen exiting the mass and anastomosing with the supernumerary colon at its entrance into the supernumerary pelvis. An intra-abdominal testicle was attached to the right kidney mass and supernumerary colon. Caudal to the right kidney, a 5-cm diameter mass was present that could not be identified as a particular structure. A second intra-abdominal testicle was located near the bladder. An inguinal hernia was present in the right inguinal area with a significant body wall defect. A branch of the aorta extended to the supernumerary pelvis dorsal to the supernumerary colon. Multiple bifurcations of this vessel extended into the supernumerary pelvis, typical of a normal caudal aortic bifurcation.

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The supernumerary cecum and colon were separated from the ileum and primary colon using a stapling device^a. The right renal artery and vein were ligated using 2-0 silk and vascular clips, and the kidney tissue was dissected free and removed. The mass caudal to the right kidney was also removed. At the entrance of the supernumerary colon to the supernumerary pelvis, a mass of tissue was surrounding the colon, the ureter, and the testicular attachment and was dissected free of surrounding vasculature. The ilia of the supernumerary pelvis were closely adhered and minimal dissection of the colon through the pelvis could be performed. The supernumerary colon was transected at its entrance into the supernumerary pelvis using a stapling device^b. The colon, right kidney, and testicle were removed en bloc. The second intra-abdominal testicle was extirpated. The single descended testicle was removed through the inguinal hernia, which was then closed using 3-0 polypropylene suture.

After removal of the supernumerary colon, right kidney mass, and testicle, the mass of tissue surrounding the distal portion of the colon was removed. A stricture of the accessory colon was present proximal to a dilated segment of tubular tissue, thought to either be continuation of the colon or a urethra. The supernumerary ureter traveled through the mass and entered the colon caudal to the stricture (Figure 6).

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The patient remained hospitalized for standard postoperative care (IV fluids and analgesics). The dog recovered well with no complication postoperatively.

Histologic evaluation of the resected structures revealed normal colonic tissue, marked diffuse renal dysplasia with pyelonephritis, and confirmation of two retained testicles (both the one in the caudal abdomen and the one attached to the accessory colon and right kidney). The unidentifiable mid-abdominal mass was lymphoid hyperplasia.

A follow-up phone call with the owner 5 mo after surgery revealed the dog was doing well but continued to have a small amount of discharge from the supernumerary penis with reduced frequency and no odor was associated with this discharge. The portion of the supernumerary colon from the supernumerary pelvis to the supernumerary prepuce and atresic anus could not be removed because of the owner’s wish to not disturb the supernumerary pelvis and associated limbs. We suspect this mild residual discharge is from material located within the supernumerary colon, which was not completely resected. Because the supernumerary colon no longer connects to the gastrointestinal tract, further discharge is not expected once the residual contents have been expelled.

Discussion

Two conditions in human medicine have been recognized in similarity to this case. The first, heteropagus twinning, also known as parasitic twinning, refers to a conjoined twinning where a small parasitic twin is attached to and dependent upon a normal host, which is referred to as the autosite.^1,2 The morphology of heteropagus twinning is quite varied and naming is performed by location of attachment to the autosite.^1,3–5 A strong female predisposition is observed with true conjoined twins, but reports of heteropagus twinning indicate an equal or male predisposition.^1,2,6 The parasitic twin is acardiac, except in rare cases, but may have other organs such as lung, liver, gastrointestinal tract, or urogenital tract present.^1–3,6 Ischiopagus parasitic twinning is common, with the parasite lower limbs attached to the lower abdomen and pelvis of the autosite.^5,6 Duplicate genitalia is common in ischiopagus parasitic twinning, typically rotated 90 degrees from the normal axis. The gastrointestinal system is typically single, except in rare cases in which the rectum may divide and end in two separate ani.⁷ Visceral communication of the parasite with the autosite is rare.^1,2 Of 12 cases in the human literature in which the parasite had bowel, only two cases showed communication with the autosite bowel.^2,4 Bony communication is also rare. Most parasitic limbs do not have the capacity for movement, and in some cases, dissection reveals lack of musculature.² Abdominal wall and spinal defects of the autosite are common, and correspond to the attachment site of the parasite.² Unilateral renal agenesis was seen in one heteropagus twinning case,² with an atrophic right kidney in a second case.³

Two major theories have been postulated for the development of conjoined twins in human medicine. The fission theory suggests that incomplete fission of the blastocyst results in two centers of axial growth that maintain a connection at some location.^2,8 This typically occurs at 13–15 days after fertilization. The second theory, called the fusion theory, describes two distinct cell masses that coalesce at a later stage.^2,4,8 The cause of asymmetry between the autosite and the parasite is thought to be vascular compromise of the parasite, leading to dependence on collateral circulation from the autosite.² Ischemic atrophy of the parasite is a result of this circulatory compromise.²

The second condition recognized in humans similar to this case is caudal duplication syndrome, or dipygus, which has been described as the occurrence of duplications of various organs in the caudal region, including the distal spine, urinary tract, genitalia, and the distal intestine.^7,9–11 This anomaly is rare in humans and animals and can be characterized by multiple combinations of malformations.^10–12

The theory proposed for development of caudal duplication syndrome is a defect in embryogenesis between day 23 and 25 of gestation.⁹ It is at this time when the spinal cord is formed, except for the most distal portion. At this distal portion, the notochord and neural tube are joined, forming the caudal cell mass.⁹ The caudal cell mass contains the embryonic distal ileum, colon, rectum, and most of the bladder and urethra.¹¹ Division at this point will cause duplication of all of these organs.¹¹ Lack of regression of Kovalevsky’s canal, a transient epithelial structure interconnecting amniotic and yolk sacs that crosses the caudal cell mass, can cause fibrous bands to divide the notochord or mesoderm, resulting in duplication of the spinal cord (diastematomyelia or diplomyelia), gastrointestinal, and genitourinary tracts.^9,11–13 In cases with genitourinary duplication, this results in two bladders, each supplied by a single ureter, and each leading to a single urethra exiting either phallus.¹⁴ In a single case of leg duplication (dimelia), the patient had ipsilateral renal agenesis.¹² It may be important to note that dimelia is not thought to be part of the conjoined twin spectrum.⁷

It is unclear in the case reported here whether this presentation was a result of heteropagus twinning or caudal duplication. Portions of the case fit with either theory. In support of heteropagus twinning is the presence of an abdominal wall defect at the attachment site of the parasite, poorly developed musculature and lack of conscious movement of the parasitic limbs, and lack of bony connection between the autosite and parasite. In contrast to the theory of heteropagus twinning is the duplication of the colon and cecum at the terminal end of the autosite ileum. In many of the case reports of heteropagus twins in humans, the parasitic phallus is located on the parasite, whereas in the case reported here the parasitic phallus was on the ventral abdominal wall of the autosite.

In support of caudal duplication is the duplication of the cecum and colon. Against this theory is the lack of a second urinary bladder. The left kidney was normal in appearance and had a single ureter connecting to the single bladder. The right kidney had severe renal dysplasia and a ureter that anastomosed with the parasitic colon. It is possible that other structures were present caudal to the pelvis in the parasite, but we were unable to determine this due to the owner’s wish to leave the parasite intact.

Incomplete caudal duplication has been reported in the canine species in two separate case reports.^14,15 An additional case report presents true conjoined twins in a canine.¹⁶ Parasitic twinning in a goat has also been reported; the parasite had duplication of the entire gastrointestinal tract from its bifurcation at the jejunum to the colon and two anal openings, both located on the autosite.¹⁷ This was more consistent with ischiopagus twinning, with the parasite on the ventral midline between the autosite limbs. A case of epigastric heteropagus twinning has been reported in a Chihuahua puppy that was euthanized shortly after birth due to additional multiple severe congenital abnormalities of the autosite.¹⁸ In that case, the autosite was additionally affected by focal cranial aplasia cutis, anasarca, lissencephay, palatoschisis, sternal agenesis, and eventeratio. The parasite had atresia ani with intestine that connected to, but was nonpatent with, the jejunum of the autosite.¹⁸ This differs from our patient in that the autosite had no other detectable abnormalities and the supernumerary colon was patent with the autosite ileum and colon in our case (Figure 4).

One report in the human literature alludes to caudal duplication being a form of parasitic twinning.¹⁹ Another report proposes either caudal duplication or parasitic twinning as an etiology for their particular case.¹³ It is known that there is a continuum of changes in either condition, and thus true determination of the origin of this case is impossible.

Conclusion

In summary, we present a case of either heteropagus twinning or caudal duplication. Each is a rare syndrome in itself, and each can present with very different morphologies. The presence of supernumerary limbs should provoke an investigation into the internal abnormalities that may accompany the external abnormalities.