There are no studies to date on the normal reproductive physiology of African white-bellied pangolins (Phataginus tricuspis). As a reclusive species, little is known about normal gestation, successful parturition, and potential complications during pregnancy. Ten female P. tricuspis were diagnosed as pregnant and monitored under professional care. Five developed complications during pregnancies or during parturition and are detailed in this case series. Dystocia occurred in two dams each, with malposition of a singleton fetus. Both dams were successfully treated with surgical intervention by caesarian section. Of the two individuals, one fetus was nonviable, but the other neonate survived and was reared by the dam to weaning. A third pregnant female died during pregnancy from septicemia resulting in death of the preterm fetus. The two additional dams of the five gave birth to full-term neonates. One fetus was stillborn with evidence of fetal distress, and the other died immediately after birth (perinatal death) with undetermined etiology. Based on this case series, complications associated with pregnancy occur in P. tricuspis, indicating the need for further study and close monitoring during impending parturition.
INTRODUCTION
Pangolins are insectivorous mammals native to Africa and Asia.9 All eight pangolin species are threatened with extinction, with illegal trade for meat consumption and supply to Asian medicine markets as the greatest threats to their survival.2,9,18 Four of the eight pangolin species are found only in Africa and include white-bellied pangolins (Phataginus tricuspis), black-bellied pangolins (Phataginus tetradactyla), giant ground pangolins (Smutsia gigantea), and Temminck's ground pangolins (Smutsia temminckii).6,9
Because of the intense consumptive pressure on wild populations of pangolins, the development of ex situ conservation programs with expertise in professional care and reproduction have been recommended.19 Such measures require technical expertise that does not yet exist for African pangolin species. Among the knowledge gaps for African pangolin species, is a need to understand normal pangolin reproductive physiolgy.19 This case series describes complications associated with pregnancy in five P. tricuspis.
CASE REPORTS
In 2016, a group of P. tricuspis was brought to the United States to establish an ex situ population living among five zoological institutions. Of these individuals, 10 were confirmed to be gravid and monitored throughout gestation. Five of those females successfully gave birth to healthy offspring without complication at the zoological institutions. The other five had complications that resulted in death of one dam and four neonates (Table 1).
Table 1.
Parturition and pregnancy complications in African white-bellied pangolins (Phataginus tricuspis) and associated pathologic findings.
Case 1—dystocia
An unknown age, unknown weight, female P. tricuspis was observed to have a light yellow clear mucus plug at her vulva during 9:00 AM check (time = 0 hr). Activity was increased, and the pangolin showed no interest in food. A mucus plug was expelled 5 hr later, and 6 hr later active labor commenced. During active labor the dam took a standing position, bracing on the side of the enclosure with her forefeet, head ventrally flexed and tail unfurled. Contractions were observed in the caudal abdomen and were short in duration (18–30 sec) with long intervals of rest (5–15 min). Excessive lacrimation was noted with short, shallow rapid breaths.
By evening (13 hr), abdominal contractions increased in force and the animal had difficulty standing. Contraction duration was longer (5–12 min) with brief resting intervals (10 sec). During this period, anogenital licking occurred, and a clear odorless fluid was expelled from the vulva. By 14–16 hr, vulvar swelling had increased and contractions transitioned to even longer duration (20–30 min) with variable resting intervals and less labored breathing. During the final period of observed labor (16–17 hr), contractions were characterized as less severe than earlier but still could be visualized moving slowly through the caudal abdomen. The dam appeared lethargic, but movement of the fetus was visible within the abdomen.
The next morning (22 hr), the dam was lying quietly in her hiding box. Contractions were still observed, but less intense than previous and no neonate was present. Dystocia was presumed and radiographs were acquired before general anesthesia to assess fetal position before surgical intervention. Radiographs confirmed malposition of the fetus with ventral/downward deviation of the head and anterior fetal presentation (Fig. 1).
Figure 1.
Right lateral (A) and dorsoventral (B) radiographs obtained awake, without anesthesia, of Phataginus tricuspis (case 1 pangolin) with dystocia. Note the fetal malposition, anterior position, and downward deviation (ventroflexion) of head/neck of fetus in utero. Dam required surgical intervention; fetus was nonviable at the time of caesarian section.
General anesthesia was induced with isoflurane (5% induction, 2–3% maintenance; Isothesia™ isoflurane, USP, Henry Schein Animal Health, Dublin, OH 43017, USA) by facemask. Heart rate of the dam ranged between 120 and 164 beats/ min, and respiratory rate between 40 and 80 breaths/min during the procedure. The dam was positioned in dorsal recumbency and aseptically prepared, and a caesarian section was performed using standard surgical techniques.12,22 In brief, a linear skin incision was made along the midline extending from pelvic brim to just caudal to the umbilicus. The linea alba was incised allowing exteriorization of uterine body and horns. The intestinal tract was exteriorized cranially to maximize accessibility to the gravid uterine horn. A 4-cm incision was made in the uterine wall. The amniotic sac was ruptured and neonate removed. The umbilicus of the fetus was clamped with hemostatic forceps; surrounding placental tissues were removed, and the uterus was lavaged (Normosolt-R, USP, Hospira Inc., Lake Forest, IL 60045, USA).
The uterine wall was closed with 4-0 polyglactin 910 (Vicryl™, Ethicon Inc., Guaynabo, Puerto Rico 00969, USA) in a continuous horizontal mattress pattern and Utrecht Cushing pattern oversew. The abdomen was lavaged (Normosol-R), and abdominal wall was closed using 3-0 polydioxanone (PDS, Monosorb™, Henry Schein Animal Health) in a simple interrupted pattern. Skin was closed using the same suture in a continuous intradermal pattern. Skin glue (3M Vetbondt Tissue Adhesive, St. Paul, MN 55144, USA) was applied topically to the length of the incision.
Postsurgery, the dam received an analgesic (meloxicam, Eloxiject™, Norbrook Laboratories Limited, Newry, Northern Ireland BT35 6PU; 0.2 mg/kg subcutaneous [SC]), an antibiotic (cefovecin sodium, Conveniat, Zoetis Inc., Kalamazoo, MI 49007, USA; 8 mg/kg SC), and fluids (warmed Normosol-R; 120 ml SC) and recovered normally. The surgical site was cleansed daily with dilute chlorhexidine scrub (Dermachlor™ solution, VetUS™, Henry Schein Animal Health) and treated with Vetericynt VF +Plus Hydrogel (Innovacyn Inc., Rialto, CA 92377, USA). The incision healed well with no postsurgical complications.
The fetus removed during the caesarian section was fully developed but was nonresponsive on removal from the dam. Resuscitation was attempted and was unsuccessful. A postmortem examination was not performed on the fetus.
Case 2—dystocia
An unknown age, 2.38-kg, female pangolin was observed in labor after passing a mucus plug and actively straining with only the tail of the fetus protruding from the vaginal canal. Radiographs were obtained (Fig. 2D, E) without anesthesia and indicated posterior presentation with lateral deviation of fetal body. Manual exam confirmed the infant was viable and still responsive to stimulation (curled tail when touched). The dam was anesthetized with sevoflurane (MWI, Boise, ID 83705, USA) as previously described,1 and manipulation of fetus within the birth canal was attempted. The fetus could not be extracted through the birth canal and efforts to retropulse to change fetal position were unsuccessful. Surgical intervention was necessary, and a caesarian section was performed.12,22 In brief, a 10-cm midline skin and linea incision was made to enter the abdominal cavity. The gastrointestinal tract was exteriorized to allow uterus visualization. The fetus was present in the left horn and positioned with the rostrum of the fetus at the proximal tip of the uterine horn closest to the oviduct, and the tail of the fetus was protruding through the vulva. A 5-cm longitudinal incision was made along the lateral uterine wall (over the back and head of the fetus), and the fetus was removed. The uterus was closed with 3-0 PDS (PDS Plus antibacterial suture, Ethicon Inc.) using a simple interrupted pattern followed by a continuous horizontal mattress (inverting) pattern. Oxytocin (VetOne, MWI; 10 IU intramuscular [IM]) was given to initiate uterine contractions and assist with expulsion of the placenta. The linea was closed with 4-0 PDS (PDS Plus antibacterial suture, Ethicon Inc.) using a simple continuous pattern. Bupivacaine (Hospira; 1.25 mg 0.5% bupivacaine diluted 1: 1 in sterile water) was administered in the linea incision for analgesia. Skin was closed using a subcuticular pattern with 4-0 PDS and additional bupivacaine was injected subcutaneously along the incision. Tissue glue was used to oppose skin edges over the caudal knot of the subcuticular suture, and skin staples (Weck Visistat 35W, DuPont Tyvek, Research Triangle Park, NC 27709, USA) were placed 0.5 cm apart along the incision. The skin incision was covered and protected with adhesive surgical drape impregnated with providine-iodine (Jorgensen Laboratories Inc., Loveland, CO, USA).
Figure 2.
Right lateral (A), ventrodorsal (B), and left lateral (C) projection radiographs of a pregnant Phataginus tricuspis (case 2 pangolin) imaged under general anesthesia 4 wk before parturition with fetus in anterior presentation. Right lateral (D) and dorsoventral (E) radiographs obtained of the same pangolin dam without anesthesia during prolonged parturition. Note the tail (white arrow) of the neonate protruding from the vulva, indicating dystocia (posterior presentation, lateral body position). Surgical intervention by caesarian section was required for successful birth. Both survived, and the dam raised the neonate to weaning.
During recovery, fluids (lactated Ringer's solution, Hospira; 120 ml SC), long-acting antibiotic (ceftiofur crystalline free acid, Excedet 200 mg/ ml, Zoetis; 30 mg SC) and analgesics (buprenorphine hydrochloride, Par Pharmaceutical, Chestnut Ridge, NY 10977, USA; 0.024 mg q6hr IM; meloxicam, 5 mg/ml, OstiLox VetOne, MWI; 0.45 mg SC) were provided.
After caesarian delivery, the neonate appeared viable; the umbilicus was clamped and 100% oxygen supplementation was provided by facemask. The male neonate (126 g, 30 cm long, Fig. 3B, C) was breathing with a strong and rapid heart rate (150 beats/min). Thermal support was provided using a warm air blanket (3M Bair Hugger Warming Unit 505, 3M Health Care) and a reflective blanket. Within 1 min of birth, the neonate became acutely apneic and bradycardic (70–80 beats/min) but maintained a palpebral reflex. The neonate continued to be apneic despite continuous stimulation. Strong pulses were visible in the umbilical artery, but because of continued apnea and bradycardia, stimulation of the philtrum was attempted without any observed response. Atropine (atropine sulfate, Med-Pharmex, Pomona, CA 91767, USA; 0.005 mg intravenous [IV]) was administered via the umbilical vein followed by doxapram hydrochloride (WestWard, Eatontown, NJ 07724, USA; 0.4 mg IM, followed by 0.4 mg IV). Thereafter, intermittent respiration was observed, and clear serous discharge was suctioned from the mouth via a red rubber catheter and syringe. Small cotton-tipped swabs were used to clear out the oral cavity, which appeared to stimulate the neonate, and movement was noted with a more regular respiratory rate. Heart rate returned to the initial rate (150 beats/ min) and respiratory rate increased to 30 breaths/ min with 98% oxygen saturation (lingual pulse oximeter, Masimo Set Rainbow Rad-57, Masimo Corporation, Irvine, CA 92618, USA). Within several minutes, the infant became responsive, started ambulating, and appeared strong with good gripping strength. The umbilical cord was ligated with 3-0 PDS (PDS Plus antibacterial suture, Ethicon Inc.) by one circumferential ligature, and the umbilicus was transected distal to the ligature.
Figure 3.
Image of Phataginus tricuspis (case 2 pangolin) dam and neonate immediately after caesarian section and successful neonatal resuscitation. (A) Dam was introduced to neonate during recovery from anesthesia (neonate in gloved hand near bottom of photo). Neonate was sexed as male (B) and was fully scaled with open eyes (C) at birth. The dam cared for the neonate after surgical recovery to weaning.
The dam was monitored closely during recovery and was successfully reunited with the neonate during recovery (Fig. 3A). The dam was placed in a warmed air incubator with the neonate, which was active and alert, to allow the neonate to lick at the dam's nipples which were dripping milk. The dam cared for the neonate until weaning several months later. The placenta was passed <24 hr after the caesarian surgery, and histopathologic evaluation of the endotheliochorial placenta was unremarkable.
Case 3—dam and neonate death
An unknown age, 1.34-kg, pregnant pangolin was evaluated for acute lethargy <1 wk after arrival at the zoological institution. This animal had maintained body weight over the week, but appetite decreased throughout the day of presentation until it became acutely lethargic (day 0). On initial examination, the pangolin was obtunded, 5–8% was dehydrated, and had decreased in weight from 1.44 to 1.34 kg over the 24-hr period. Blood tests revealed hypoglycemia (True Metrix Blood Glucose Meter, Walgreens, Deerfield, IL 60015, USA; <20 mg/dl). The animal was treated with 0.9% saline (Baxter, Deerfield, IL 60015, USA; 150 ml SC), dextrose 50% solution (Vedco, St. Joseph, MO 64507, USA; 1.2 ml diluted in 6 ml in 0.9% saline SC) and was tube fed with EmerAid Intensive Care Carnivoret formula (EmerAid LLC, Cornell, IL 61319, USA; 20 ml peroral [PO]). After treatment, the dam quickly resumed consciousness and became bright, alert, and responsive. The animal regained normoglycemia (109 mg/dl). Hematology and serum chemistry results were otherwise unremarkable. Abdominal ultrasound revealed a fluid-filled uterus that contained a viable fetus with fetal heart rate of 90 beats/min, biparietal width of 1.17 cm (Fig. 4A), thoracic width of 1.27 cm (Fig. 4B), and crown-to-rump length of 3.46 cm. The dam was started on a treatment regimen consisting of supplemental tube feeding with EmerAid Intensive Care Carnivore formula (20 ml PO twice daily), 0.9% saline (60 ml SC twice daily), and blood glucose monitoring (twice daily).
Figure 4.
Ultrasound images of Phataginus tricuspis female with fetus in utero (case 3 pangolin) at an unknown length of gestation. Biparietal parameter (1.17 cm) and thoracic diameter (1.27 cm) fetal measurements were obtained during ultrasound (A, B).
The animal remained stable for 2 days with improved appetite, but then had two episodes of acute lethargy and hypoglycemia (days 3 and 4). During both episodes, the animal responded well to fluids and supplemental dextrose therapy. At recheck, white blood cell count was decreased (2,400 cells/µl, previously 8,500 cells/µl), whereas other hematology and serum chemistry parameters were unremarkable. Blood cultures were positive for Enterococcus sp. and Staphylococcus simulans. Tube feeding was increased to three times daily; ranitidine (Pharmaceutical Associates Inc., Greenville, SC 29605, USA; 3 mg PO twice daily), ceftiofur (ceftiofur crystalline-free acid; 9.3 mg SC), sucralfate (Nostrum Laboratories Inc., Kansas City, MO 64120, USA; 200 mg PO twice daily), enrofloxacin (Baytrilt, Bayer, Shawnee Mission, KS 66201, USA; 15 mg SC once daily), calcium glubionate (Henry Schein; 360 mg PO once daily), and a multivitamin supplement (Poly-Vi-Solt, Mead Johnson & Company LLC, Chicago, IL 60606, USA; 0.25 ml once daily) were added to the treatment regimen.
Despite supportive care, this pangolin continued to have intermittent episodes of hypoglycemia and unresponsiveness. Repeat ultrasound of the fetus confirmed fetal movement and viability. Despite maintaining weight at approximately 1.4 kg, the pangolin's condition continued to decline with intermittent hypoglycemic crises, lethargy, and developing diarrhea. More intensive fluid therapy was instituted through intravenous administration of 20 ml regular saline supplemented with 5% dextrose once daily in the ventral coccygeal vein, but follow up blood tests showed profound anemia (packed cell volume 8%), hypoproteinemia (total protein 1.7 g/dl; albumin 0.7 g/ dl, globulin 1.0 g/dl), elevated aspartate transaminase (2,641 U/L), and elevated creatine kinase (21,175 U/L). The dam died on day 5.
Postmortem examination confirmed emaciation with marked atrophy of fat, pancreas, and liver. Renal pathology included marked tubular necrosis with pigmentary nephrosis. There was moderate atrophic enterocolitis with focal intestinal ulceration and gastric glandular ectasia. Mild interstitial pneumonia was also found and, along with the intestinal changes, was consistent with low-grade sepsis, which was supported with the positive blood culture. Intestinal changes noted on histopathologic examination were suggestive of a coronavirus or other low-grade viral intestinal infection. Postmortem examination of the fetus (male) revealed mild renal tubular necrosis and hepatic congestion consistent with hypoxia and shock related to the death of the dam.
Case 4—still birth
An unknown age, 2.3-kg female gave birth overnight. Preparturition signs were absent, and parturition was not observed. Grossly, the neonate appeared full term (91.5 g) and had visible blood in the right eye and cloudiness affecting both corneas. The placenta was still attached to the umbilicus (Fig. 5C, D). On postmortem examination of the fetus, the lungs were diffusely atelectic, dark red, and rubbery and sank in formalin. On histopathologic evaluation, fetal alveolar spaces contained mild to moderately increased numbers of amniotic squamous cells and a few bits of meconium. The brain, liver, spleen, kidney, adrenal gland, urinary bladder, thyroid gland, gastrointestinal tract, diaphragm, thymus, skin, heart, trachea, lymph nodes, and placenta were histologically within normal limits. On the basis of pulmonary atelectasis, the fetus did not take a breath after birth and was deemed stillborn. Evidence of aspiration of increased amounts of amniotic squamous cells and a small amount of meconium within the lungs indicated that fetal distress occurred either in utero or during parturition, making dystocia probable. There was no evidence of infectious or developmental disease, and all tissues appeared appropriately developed for a full-term fetus.
Figure 5.
Right lateral (A) and ventrodorsal (B) radiographs of a pregnant Phataginus tricuspis imaged under general anesthesia 10 wk before partition. This animal gave birth to a full-term stillborn pictured below with right lateral (C) and ventrodorsal (D) radiographs. Postmortem of the stillborn fetus (case 4 pangolin) indicated fetal distress with dystocia as the suspected cause leading to death.
Follow-up examination of the dam 2 days after the fetus was born indicated a normal exam. Complete blood work (complete blood count, serum biochemistry) were normal. Abdominal ultrasound indicated visible corpus luteum on one ovary and multistage follicular development on the other ovary with a small amount of fluid in the uterus.
Case 5—early neonatal death
An unknown age, 2.62-kg female gave birth to an apparently full-term fetus. Preparturition signs were absent, and parturition was not observed. Histologically, the changes within the placenta (acute, multifocal, suppurative placentitis) were extremely mild and were of minor clinical significance. The fetus had limited expansion of approximately 30% of the alveoli, suggesting that the neonate was alive at birth and had taken at least one breath postpartum, indicating perinatal death. Signs of fetal distress (squamous debris and aggregates of meconium) were not observed within the lungs, and the neonate had large adipose reserves.
DISCUSSION
There is one description of normal birth for P. tricuspis describing a neonate weighing 100 g at birth that was active and born well-developed with open eyes.15 The neonate that survived caesarian in case 2 of this case series was similar in size and description. Normal gestation period and biparietal size during pregnancy is not described for P. tricuspis. Formosan pangolins, an Asian pangolin species, have been more closely studied and cared for by veterinarians and animal care specialists, but neonatal survival in that species is reported to be low.3,4,21 The cause of low neonatal survival is poorly understood. There are descriptions of dystocia, stillbirths, and fatal fetal malformations for all four species of Asian pangolins, indicating susceptibility to complications associated with pregnancy.3,11,16,27,30–32 It is unclear whether African pangolin species have similar challenges, but this case series suggests P. tricuspis are susceptible to pregnancy complications.
Mammalian dystocia is considered a sequela of abnormal expulsive forces, adequacy of the birth canal, size, and disposition of the fetus (including presentation, position, and posture).13,14 In cases 1 and 2, disposition of the fetus likely contributed to dystocia. The fetus of case 1 presented in anterior presentation but had ventral deviation of the head, a malposition described in other mammals.13,14 Although normal presentation is unknown in pangolin, downward head deviation is likely abnormal.13 In case 2, radiograph images obtained earlier in the pregnancy indicated the fetus was in anterior position (Fig. 2A–C) but at the time of dystocia was in the posterior position with lateral body position. In domestic dogs, anterior versus posterior presentation is not associated with dystocia, whereas the position of the fetal head, limbs, and body are.8,13,26 Cases 1 and 2 had differing fetal presentations (anterior and posterior), but the abnormal position of the head and body are likely what affected normal parturition in these two cases.
The surgical technique used to perform a caesarian section has been well described for domestic species,12,17,20 and the surgeries for pangolins in cases 1 and 2 were straightforward and without complication. In case 1, the placenta was removed during surgery, but in case 2 it was allowed to shed naturally, both with similar outcomes.
Early surgical intervention should be considered for any dystocia suspected in P. tricuspis. The paucity of information on gestation length, normal progression of labor, and parturition, fetal monitoring, and signs of normal versus abnormal pregnancy in pangolins makes it challenging to identify when parturition is abnormal. In other mammalian species, the two most active stages of labor are described with predictable clinical signs and duration.7,14,28 Stage 1 labor begins with indiscernible uterine contractions, progressive cervical dilation, and typically within 6–12 hr transitions to stage 2.7,14,28 Transition to stage 2 of labor occurs with visible abdominal straining, strong uterine contractions, and active expulsion of the fetus from the birth canal within 30 min or up to 2 hr.7,10,14,28 In case 1, the pangolin was observed in stage 1 labor (expelled mucus plug, short contractions, excessive lacrimation, short and rapid breaths, and restless behavior), which lasted for approximately 7 hr, a length of time similar to that described for dogs.14 Then stage 2 of labor for this dam was protracted, indicating probable dystocia. Details from the pangolins of cases 1 and 2 suggest that indication for caesarian are similar to other mammals and should be attempted for pangolin when there is (1) a lack of progression from stage 1 to stage 2 labor after 6–8 hr, (2) stage 2 labor with strong active abdominal contractions lasting for 30 min without expulsion of the fetus, (3) stage 2 labor lasting >4 hr, (4) prolonged parturition (stages 1 and 2) lasting >24 hr, or (5) part of the fetus protruding from the vagina without expulsion of the fetus.5,7,14,23
Case 2 indicates that following caesarian, care must be prompt and attentive for pangolin neonates. Techniques used for the case 2 pangolin led to successful neonatal resuscitation and were similar to that described for other mammals, including rapid clearance of fetal membranes, thermal support, brisk rubbing, and supplemental oxygen.13 The acute onset of apnea of the case 2 neonate was complicated by the inability to intubate.1 Vigorous attempts to stimulate respiration while providing 100% oxygen were tried, but when the neonate did not respond, doxapram was administered. Resuscitation with atropine and doxapram using the neonate's umbilical vein may have been lifesaving and should be considered for pangolin neonates if other measures of resuscitation are not successful.
Case 3 differs from cases 1 and 2 because the dam's death lead to the death of dam and fetus. The dam's septicemia may have originated from gastrointestinal ulceration, as described for other pangolin species.11,19 Advances in understanding pangolin health and disease susceptibility may prevent similar cases in the future.
In cases 4 and 5, no preparturition signs were observed, and the actual births were not observed. In case 4, the neonate was stillborn, but postmortem findings indicated fetal distress, suggesting that death may have been related to prolonged labor from dystocia. In case 5, the fetus died after birth with no evidence of fetal distress on histopathologic evaluation. Monitoring of each dam near parturition by remote cameras or direct observation could have provided additional information and insight to the complications of pregnancy or allowed care staff to intervene appropriately.
Case 5 was thought to be a stillborn fetus until a postmortem examination was performed, revealing that the neonate did take at least one breath after birth. This finding is a reminder that routine postmortem examination can provide insight into factors related to the cause of death. In other mammals, perinatal death is most commonly associated with fetal asphyxia and bacterial infections.24
Possibly P. tricuspis are prone to complications during pregnancy, but further study is needed to understand risks and factors associated with successful pregnancy. Among the five cases presented in this series, only case 2 had a surviving neonate, which is cause for concern within the managed population. These five cases suggest close monitoring using cameras or direct observation is necessary for near-term pregnant P. tricuspis. However, the gestation of this pangolin species is unknown. Broadly, gestation among all
pangolin species is not well studied. The gestation period of Cape pangolins is 139 days.25 Gestation of Indian pangolins is believed to be shorter (65–70 days).16 Chinese pangolins have reported gestation lasting 101–169 days,27,29 but when serum progesterone monitoring was used, a longer gestation (318–372 days) was reported.4 The duration of pregnancy among the P. tricuspis dams in this case series were at least 112–168 days (4–6 mo), suggesting the total gestation may be as long as 7–9 mo.
Complications associated with pregnancy have not been previously described in P. tricuspis. The descriptions in this case series are the first steps to understanding pregnancy in this species and should spur interest in further research. Information regarding normal pregnancy parameters (e.g., gestational length, developmental milestones) in P. tricuspis would provide tremendous insight to evaluating factors that can lead to complications during pregnancy and parturition. Among the P. tricuspis dams described in this case series, the factors that may have affected successful pregnancy and parturition cannot be evaluated. There was no known health or nutritional history for these dams before arrival at the zoological institutions, and each pregnant female arrived at an unknown gestational stage, making it impossible to compare risk factors among these cases.
Although more study is needed to understand normal pangolin pregnancy and parturition, the reports of stillbirths among pangolin species and the complications described in this case series indicate that monitoring (remote or direct) of pregnant pangolins near parturition is essential to better understand the birthing process and identify cases where intervention is necessary.
CONCLUSION
The five cases presented in this case series document complications associated with pregnancy and parturition in P. tricuspis. The findings emphasize the need for improved knowledge of normal parameters of successful pregnancy to characterize risk factors associated with pregnancy complications in this species.
All P. tricuspis under professional care should be carefully monitored during pregnancy with direct or indirect (via camera) observation near parturition. Dams that do not quickly progress through stage 2 of parturition (forceful abdominal contractions to birth of neonate) within 4 hr should be considered for intervention. Surgical intervention using standard veterinary caesarian approach can be successful and life saving for the pangolin dam and neonate. Veterinary teams should be prepared for neonate resuscitation similar to that performed for domestic animals after caesarian section. Additional research into pangolin reproduction is needed to improve fetal survivability to ensure sustainability of rescue populations.
