Retrospective Analysis of the Incidence of Retained Placenta in 3 Large Colonies of NHP

Abstract

During 1999 through 2014, retained placenta was the most common cause of clinical admission for reproductive complications in breeding colonies of baboons (approximate colony size, 2000 animals), cynomolgus macaques (approximately 1000), and rhesus macaques (approximately 500) at the Southwest National Primate Research Center. Retained placentas occurred in 2.7% of baboons, 3.3% of cynomolgus macaques, and 1.0% of rhesus macaques. Apparent risk factors for retained placenta included stillbirth or abortion and at least one prior cesarean section. There was a significant association between stillbirth and retained placenta in all species. Cesarean sections were performed routinely for baboons to meet research objectives but occurred only as needed for cynomolgus and rhesus macaques. Having had at least one prior cesarean section was an incidence factor for retained placenta in 37.0% of baboons and 4.7% of cynomolgus macaques; none of the rhesus macaques with retained placentas had undergone cesarean section previously. More than 90% of dams with retained placenta returned to a successful reproductive life or assignment to a nonbreeding research protocol. Advances in reproductive management will benefit from prospective studies that capture additional data from all members of a breeding group prior to reproductive complications.

Retained placentas and other reproductive problems are unavoidable complications encountered in association with NHP production colonies and are difficult to diagnose, because most births occur at night, when human observation is minimal, and because the dams routinely consume the placenta.^41,44,45 There is extensive information regarding retained placentas in dairy cattle,^7,25,20 and humans,^{3,13,24,35,36,40} but little is documented about this problem's health hazard and effect on future reproduction in NHP,^16,17,23,49 with 3 documented cases reported as isolated reports between 1991 and 2009.^16,17,23 The first documented case of a retained placenta in a NHP was that of a female chimpanzee (Pan troglodytes).¹⁷ Clinical signs for that case included depression, poor maternal care, and vaginal hemorrhage 1 wk after delivery. The chimpanzee was treated successfully, and the infant was returned to the dam with no further complications. Another documented case involved a golden lion tamarin (Leontopithecus rosalia),¹⁶ which had experienced prolonged labor resulting in a stillbirth. After continued placental retention, the tamarin was hysterectomized. Histopathologic evaluation revealed that placental infiltration into the myometrium was the cause of retention.¹⁶ The third documented case occurred in a bonobo (Pan paniscus) housed in a sanctuary in the Democratic Republic of Congo.²³ The animal was treated with oxytocin injections; after manual removal of the placenta, the dam and infant were reunited, and maternal recovery was uneventful.

In addition, in an unpublished case, one of the current authors (TH) treated a mandrill (Mandrillus sphinx) by using oxytocin injection and manual removal of the placenta, after which the dam and infant were reunited, and maternal recovery was uneventful. Several other unpublished cases documented in the medical records of the breeding colonies at the Southwest National Primate Research Center (SNPRC) involved species baboons (Papio spp.), cynomolgus macaques (Macaca fascicularis), and rhesus macaques (Macaca mulatta). Clinical veterinarians had deemed all of these animals to be healthy prior to their placement into breeding groups and were rechecked semiannually concurrent with tuberculin testing. Body condition varied from lean to obese, but body condition score was not recorded. We retrospectively reviewed these records to determine the risk factors and incidence of retained placenta within the 3 NHP colonies over 15 y.

Materials and Methods

A retrospective analysis was conducted by using computerized clinical records from 1999 through 2014 in the rhesus macaque, cynomolgus macaque, and baboon breeding colonies. Breeding occurred throughout the reporting period in the rhesus and baboon colonies and ceased in 2008 in the cynomolgus colony. Colony populations were approximately 2000 baboons, 1000 cynomolgus macaques, and 500 rhesus macaques. All birth events were identified during this time period, and record review was focused to include only those animals with a documented retained placenta. Recorded conditions relating to potential risk factors surrounding incidences of retained placenta included stillbirth, premature delivery, prior cesarean section, parity, prior retained placentas, and trauma. Data were analyzed, and the incidence of retained placenta was determined. Whenever possible with the available data, odds ratios with confidence intervals were calculated by using Medcalc (https://www.medcalc.org/calc/odds_ratio.php). Recorded life-history factors included age, weight, and total number of offspring produced.

All NHP were housed at an AAALAC-accredited institution and were on IACUC-approved protocols. The baboons were members of pedigreed and nonpedigreed conventional colonies housed in outdoor groups and corral housing with indoor access available. Groups varied in size from 10 to 750 animals. The larger groups of baboons were multimale–multifemale groups and of unknown pedigree. The smaller groups consisted of a pedigreed single male baboon with multiple females and their offspring. The cynomolgus macaque colony was a conventional colony housed in indoor–outdoor groups. Group sizes ranged from 7 to 25 animals. Breeding group composition consisted of a single male cynomolgus macaque with multiple females and their offspring. The rhesus macaque colony (SPF for SIV, simian retrovirus type 2 [gp20], simian T-cell leukemia virus [p21], HTLV types 1 and 2, and Macacine herpesvirus) was housed in indoor–outdoor groups. Group sizes ranged from 5 to 15 animals. Breeding groups comprised a single male rhesus macaque with multiple females and their offspring.

Results

The baboon colony had 5864 birth events. The overall stillbirth rate in the colony was 5.5% (n = 324). The incidence of retained placenta was 2.7% (n = 158). The mean age of dams at time of retention was 11.1 y (range, 5.3 to 20.2 y), with a median of 10.8 y and a mode of 8.0 y (Figure 1). The average weight of the dam was 17.5 kg (11.7 to 29.2 kg) and median of 17.3 kg (Figure 2). Of the 158 incidences of retained placenta, 10.1% (n = 16) were from animals that had multiple occurrences of retention, 9.5% (n = 15) were coupled with premature delivery, 53.8% (n = 85) were coupled with stillbirths, 36.1% (n = 57) had at least one previous cesarean section, and 10.8% (n = 17) had at least one prior stillbirth. The odds ratio of stillbirths associated with a retained placenta was 26.63 (95% confidence interval, 18.98 to 37.37; P < 0.0001). Multiple offspring occurred in 87.3% (n = 138) of the baboons, with retained placenta associated with the first parturition in 32.9% (n = 52) and the last parturition in 43.7% (n = 69; Figure 3). In addition, 9 baboons had vaginal tears, 7 had positive bacterial cultures (Staphylococcus spp., Streptococcus spp., or Escherichia coli), and 3 were noted to be gestational diabetics. The mean parity was 3.30, with a median of 4 and mode of 3. Death or euthanasia was the outcome in 6.3% (n = 10) of the cases of retained placenta among baboons; successful resolution of the retained placenta occurred in all other cases. The mean time to documented complete resolution of retained placenta was 9.6 d (range, 0 to 55 d; Table 1).

Figure 1.

Distribution of retained placenta relative to age (black, baboons; white, cynomolgus macaques; gray, rhesus macaques).

Figure 2.

Distribution of retained placenta relative to weight (black, baboons; white, cynomolgus macaques; gray, rhesus macaques).

Figure 3.

Distribution of retained placenta relative to parity (black, baboons; white, cynomolgus macaques; gray, rhesus macaques).

Table 1.

Summary of data relative to the occurrence of retained placenta (RP) in each breeding colony

	Baboons	Cynomolgus macaques	Rhesus macauqes
Breeding period	1999–2014	1999–2008	1999–2014
Total no. of births	5864	1958	926
Mean no. of offspring per animal	4.50	5.10	4.60
No. (%) of stillbirths	324 (5.5)	264 (13.5)	71 (7.7)
No. (%) of animals with RP	158 (2.7)	64 (3.3)	9 (1.0)
No. of multiple RP	16	7	0
No. with multiple offspring	138	59	9
No. died or euthanized	10	5	0
No. (%) with stillbirth + RP	85 (53.8)	30 (46.9)	6 (66.7)
No. (%) with premature delivery + RP	15 (9.5)	not applicable	not applicable
No. (%) with prior cesarean section + RP	57 (36.1)	3 (4.7)	0 (0)
No. (%) with prior stillbirth + RP	17 (10.8)	15 (23.4)	2 (22.2)
No. (%) with RP at first birth	52 (32.9)	9 (14.1)	1 (11.1)
No. (%) with RP at last birth	69 (43.7)	32 (50.0)	2 (22.2)
Mean time (d) to resolution of RP	9.6	4.6	7.7
Parity (no.) at RP: mean, median, mode	3.3, 4, 3	4.3, 4, 3	3.2, 3, 2
Weight (kg) at RP
Mean	17.3	5.2	8.0
High, median, low	29.2, 17.3, 11.7	8.5, 5.5, 2.2	10.1, 8.3, 5.3
Age (y) at RP
Mean	11.1	13.2	10.7
High, median, low	20.2, 10.8, 5.3	26.7, 13.5, 6.2	18.6, 9.5, 4.9
Mode	8	16	9

The cynomolgus macaque colony had 1958 birth events, with 13.5% (n = 264) recorded stillbirths. The incidence of retained placenta was 3.27% (n = 64). The mean age at time of retention was 13.2 y (range, 6.2 to 26.7 y), with a median of 13.5 y and mode of 16.0 y (Figure 1). Dam weight at time of retention averaged 5.2 kg (range, 2.20 to 8.5 kg), with a median of 5.0 kg (Figure 2). Among the 64 cases of retained placenta, 10.9% (n = 7) of the cynomolgus macaques had multiple incidents (2 macaques with 3 events; 5 with 2 events). Because gestational age was not estimated or calculated for this colony, the association of retained placenta with premature delivery could not be calculated. Retained placenta occurred in conjunction with a prior cesarean section in 4.7% (n = 3) macaques and was associated with stillbirth in 46.9% of animals (n = 30). The odds ratio of stillbirth associated with retained placenta was 6.26 (95% confidence interval, 3.76 to 10.42; P < 0.0001). Most of the cynomolgus macaques with retained placenta (92.2%; n = 59) had delivered multiple offspring, with 14.1% (n = 9) having retention on the first delivery and 50.0% (n = 32) having retention on the last delivery (Figure 3). One macaque had vaginal tears, but there were no reports of positive bacterial cultures or gestational diabetes among the cases of retained placenta in cynomolgus macaques. The mean parity was 4.3, median was 4, and mode was 3. A single macaque had twins, with both placentas retained. Death or euthanasia was the outcome in 7.8% (n = 5) of the cases of retained placenta in cynomolgus macaques; all other cases resolved successfully. The average time to documented complete resolution of retained placenta was 4.6 d (range, 0 to 24 d; Table 1).

The rhesus macaque colony had 926 births, of which 7.7% (n = 71) were verified stillbirths. The incidence of retained placenta was 1.0% (n = 9). The mean age at time of retained placenta was 10. 7 y (range, 4.9 to 18.6 y), with a median of 9.5 y and mode of 9.0 y (Figure 1). Dam weight at time of retention averaged 8.0 kg (range, 5.3 to 10.1 kg), with a median of 8.3 kg (Figure 2). None of the rhesus macaques had multiple episodes of retained placenta or experienced retained placenta after a cesarean section. Because gestational age was not estimated or calculated for this colony, the relationship between retained placenta and premature delivery could not be determined. Retained placenta was associated with stillbirth in 66.7% (n = 6) of cases. The odds ratio of a stillbirth associated with retained placenta was 26.22 (95% confidence interval, 6.41 to 107.24; P < 0.0001). All rhesus macaques with retained placenta had a history of multiple offspring, with 11.1% (n = 1) having a retained placenta on the first birth and 22.2% (n = 2) on the last birth (Figure 3). No rhesus macaque with retained placenta had vaginal tears, a positive bacterial culture, or gestational diabetes. The mean parity was 3.2, median was 3, and mode was 2; all rhesus macaques recovered successfully after having a retained placenta. The mean time to complete resolution was 7.7 d (range, 0 to 20 d; Table 1).

Discussion

Compared with humans, NHP reach sexual maturity at a younger age and have a shorter lifespan. These characteristics influence the features of the breeding groups in which and age ranges at which reproductive complications might be encountered. Female baboons reach sexual maturity with menarche between 3 and 5 y of age.^10,39,44 The mean gestation of various subspecies of baboon (Papio spp.) is 175 to 187 d,^6,9-11,14,33 with a mean age at first parturition of 3.9 y¹¹ or 6 y.³⁹ Baboons in the colony at SNPRC typically are placed in breeding groups at 4 to 6 y of age and are monitored for good health through semiannual health checks. One report⁹ noted that the oldest pregnant female baboon was 14.1 y, whereas others have noted baboons to have a reproductive life of 12 to 15 y.⁴⁴ At SNPRC, baboons typically are removed from breeding groups between 16 and 18 y of age, despite continuing to produce offspring, and reproductive problems or continued reproductive failure results in earlier removal. Female baboons lactate a mean of 6.6 mo, with infants typically weaned at 6 mo.¹¹ Infants at SNPRC typically were weaned by their mothers at 5 to 6 mo but remained housed with their dams until 9 mo of age. Postpartum, baboon dams may or may not resume cycling while raising their young,^6,10 leading to potentially lengthy interbirth intervals. Given their ample food supply, baboons at SNPRC might be pregnant while nursing an infant, but this scenario is avoided to prevent the dam from being overburdened. Compared with baboons, macaques have a shorter gestation length, that is, 160 to 170 d.^10,28,43 At SNPRC, rhesus and cynomolgus macaques enter breeding groups between 3.5 to 4 y of age and are verified to be in good health at semiannual health checks. Macaques are removed from breeding colonies when they have not produced an offspring for 2 consecutive years despite being with a fertile male. The mean age at removal from breeding is unknown currently and is dictated by production needs and project use. Female macaques were removed from breeding groups earlier when they had multiple reproductive complications or when their genetics no longer needed additional representation.

Pregnancy and parturition is a complex process. The analysis of this process across different types of primates involves comparisons across anatomies, hormonal changes, and reproductive cycles. The female reproductive tract of NHP is similar to that of humans,^27,28 leading to a similar birthing process.^32,44 The uterus is simplex in structure, with the ovaries attached laterally by means of the broad and ovarian ligaments. Baboons have a single placenta that is similar in structure to the human placenta, whereas macaques have a bidiscoid placenta.^10,43,44 Baboons have a large perineal sexual skin that swells predictably with the stage of the reproductive cycle.^{21,22,26,44,47} This characteristic allows trained observers to accurately assess the stage of the reproductive cycle and pregnancy without manipulation of the dam. Because macaque species often do not have pronounced perineal sex skin, visible determination of the stage of the reproductive cycle is not accomplished as readily in macaques as in baboons. Development and hormonal shifts during puberty and pregnancy in NHP mirror those of humans. Due to anatomic differences relative to posture between humans and NHP, the birthing process progresses more rapidly in NHP than in humans. Due to the shift of the pelvis in humans to accommodate bipedal locomotion, combined with a larger head, the human fetus must go through coordinated movements to progress through the birthing canal. In NHP, the birthing canal is straight, with no need for coordinated turning movements by the fetus to pass through the pelvic brim.^43,49 Thorough reviews of mammalian and NHP anatomy and physiology are available.^{4,5,34,36,38,50} The roles of hormones responsible for maintenance of pregnancy and onset of parturition have been well described.^{12,32,38,42,48} Miscues in the hormonal cascade and abnormal mechanical parameters can lead to dystocia⁴¹ or retention of the placenta.^{3-5,7,13,24,34-36,38,42,48,50}

Parturition is the last step of the reproductive cycle and is typically subdivided into 3 stages. In humans, these stages can be determined readily, ¹⁸ but distinguishing each stage in NHP is more difficult. The most reliable indication of the onset of parturition in NHP is the presence of a cervical plug¹² or a small amount of bloody mucus discharge from the vagina.¹⁸ The first stage of parturition in primates is the longest and is the period during which hormonal changes are occurring. The second stage of parturition is the active passing of the fetus through the birthing canal, culminating in birth. The third stage is the passing of the placental tissues. Retroplacental myometrial contraction is necessary to shear the placenta from the decidual bed.^13,37,46 These contractions are regulated by various hormones^{12,32,38,42,48} and are necessary to dissociate the placenta from the uterus, allowing for expulsion. Failure of these contractions to shear the placenta from the decidual attachments can result in a retained placenta. Potential causes of this failure include inflammation, infection, uterine atony or uterine inertia, and pathologic attachment of the chorionic villi to the uterine musculature.³⁷

The 3 stages of labor in NHP are described in different ways, with some systems adding a fourth stage. In the time leading to parturition, NHP may demonstrate polydipsia and polyuria, restlessness, increased grooming and manipulation of genitalia, changes in sleeping habits, and a preference for lying in a ventral position.^12,15,23,41 These behaviors are not strict indicators of labor, because they can occur for days prior to delivery.^2,15,31 The first stage of labor (the prepartus phase) begins at the onset of labor and culminates with the first appearance of the fetus.^2,29 The characteristic postures include standing, squatting, crouching with cyclic regularity, having an arched or hollow back, stretching the legs, investigation of the anogenital region, licking, and straining.^{1,2,12,14,15,29,31,32} Because cervical dilation is not checked routinely and because the timing between labor pains can be difficult to determine, many researchers have used the cyclicity of the labor postures to indicate the onset of this first stage.² The second stage of labor (partus) consists of the delivery of the fetus and is usually of short duration, approximately 1 to 5 min^1,2,29 but can last as long as 1.25 h.⁴⁹ During this stage, the animal may adopt positions that will enable forceful contractions to propel the fetus through the birthing canal. The most common posture assumed by the female NHP during this phase is squatting.^{1,2,12,14,29,32,43} The dam may aid in the delivery of the fetus by manually pulling on the baby as it emerges, thus speeding up the second stage of parturition and aiding in positioning the baby on the ventrum.^{12,14,15,29,32,43} The third stage of labor (postpartus) comprises the time from fetal delivery to the expulsion of the placenta and fetal membranes.^2,29 Unlike humans, NHP seem to have a low incidence of postpartum hemorrhage,⁴⁹ thereby enabling the treatment of retained placenta to be delayed for a day or more without endangering the animal's life. In rhesus macaques, delivery of the placenta required as long as 12 h (range, 1 to 711 min)^2,49 but typically occurred 10 to 15 min after birth.^14,15,32,41 The macaque that needed 711 min to deliver the placenta had had 2 cesarean sections previously.² Some researchers have classified a fourth stage of parturition in NHP, which represents the time from the expulsion of the placenta to the last effort of the dam to eat the placenta.² As for many mammals, many NHP dams consume the placenta after its expulsion,^12,32,37,44 but this behavior is not universal across or within species. Therefore, the absence of a placenta is not diagnostic for retained placenta in NHP; other clinical signs must also be present.

Prolonged labor in NHP can be attributed to advanced age, stillbirth, breech birth, and primiparous status.^15,32,33 The typical presentation of a fetus is head first, and when the fetus presented in a breech position, the time of delivery was increased greatly, and stillbirth frequently occurred.^15,32,33 Once the breech infant is removed, the placenta can be delivered normally.^15,33 After delivery, NHP dams generally resume normal behaviors and do not seem to be weakened from parturition.³² Many births in NHP occur at night, hampering observation of the birthing process.^{1,2,15,29,31-33,37,41,43,44} Giving birth at night is an adaptive advantage allowing the dams to deliver when troops are bedded down for the night, so that infants have sufficient time to develop a good grasp on the dam before the troop begins moving the next day. In wild primates, labor has been noted to stop during the day and resume the next evening.³² Macaque births tend to occur seasonally by location,³² whereas baboons are nonseasonal reproducers.^9,11

In human medicine, retained placentas are a serious health concern and, without rapid intervention, can lead to loss of life of the mother.^3,40,46 Due to the associated hemorrhage, retained placentas are the second leading cause of morbidity and mortality after parturition in women.^3,35,40 The overall incidence of retained placenta in humans is low, ranging from 0.55% to 3.8%,^8,24,35,40 and to minimize risk, intervention is attempted after 30 to 60 min of retention.^23,46 A placenta is considered retained when it is expelled longer than 45 to 60 min after delivery.^37,40 Women who have had a retained placenta have a 2 to 4 times greater risk for recurrence during subsequent parturitions.^3,40 Risk factors identified include previous history of retained placenta, previous uterine surgery, preterm delivery, aged mothers, multiparity (greater than 5), induced labor, small placental weight, and blood loss.^3,35,40 Factors significantly associated with retained placenta in humans include previous cesarean section, previous dilatation and curettage, and previous retained placenta.^35,40 Increased incidence may be due to residual damage to the endometrium, thus predisposing the chorionic villi to penetrate and attach to the uterine musculature.³⁵ Retained placenta occurs in women of all ages and parities, but multiparity may be a significant risk factor due to the uterine atony that progresses with each pregnancy. In this regard, each pregnancy causes muscle fibers to be replaced with fibrous tissue, thus leading to decreased contractile power and an increased risk of retained placenta.³⁵ Blood loss is likely a sequellae to retained placenta rather than a cause.³

Postpartum hemorrhage in NHP seems to be less frequent and less problematic than in humans.⁴⁹ Hemorrhage was not associated with any of the cases in the current study. This feature allows the veterinarians more time to attempt conservative management of a retained placenta than is possible in human medicine. Due to the small sizes of the vaginal opening and birth canal in NHP, manual removal of the placenta can be challenging in these species. Therefore, instruments may be required, and the placenta may need to be removed in sections.³⁶

Prior research has shown that mothers with a stillbirth have decreased future pregnancy success.¹⁹ In other studies, abortion rates in baboons were 20.5% to 60.0% of all deliveries,^11,30 with stillbirths accounting for an additional 8%.¹¹ Stillbirths accounted for a smaller proportion of deliveries at SNPRC (5.5%) than that reported for other colonies. Retained placenta was significantly associated with stillbirth in all 3 of the species we evaluated, with likelihood levels of 26.62 for baboons, 6.26 for cynomolgus macaques, and 26.22 for rhesus macaques. Reported stillbirth rates for various species of macaques ranged from 4% to 39%.^19,28,32,45 At SNPRC, stillbirths accounted for 7.7% of rhesus births and 13.5% of cynomolgus births. In one previous study, an additional 6% of the spontaneous births in rhesus macaques were premature,²⁸ but we were unable to determine the frequency of premature birth in the SNPRC colony. Twinning is rare in Old World NHP^10,44 but occurs routinely in some New World species.^10,44 In our experience, the rare twinning events in Old World species often were coupled with the retention of both placentas.

Prior cesarean section and premature delivery are among the known risk factors for retained placenta in humans,^{3,29,32,35,40} and these associations are similar to the findings of the current study, most notably for baboons. Many baboons had undergone at least 1 prior cesarean section due to previous research demands, and the incidence of retained placenta in animals with a prior cesarean section was high in this colony (36.1%). In contrast, few cesarean sections were performed in either of the macaque colonies, and the incidence of subsequent retained placentas was relatively low as well (4.7% in cynomolgus macaques and 0% in rhesus macaques). Premature delivery likely causes an abnormal cascade in the hormonal and mechanical events that initiate parturition, thus leading to the retention of the placenta, and premature delivery showed likely association with retained placenta in baboons (9.5%); the incidence of premature delivery was not determined for cynomolgus and rhesus macaques. Due to their prominent perineal swelling, gestational age is readily calculated in baboons, thus simplifying the recognition of premature deliveries in these species. Visual determination of gestational age is difficult in macaques, so we were unable to accurately determine the association between retained placenta and premature delivery in these colonies.

Additional potential complicating factors that may have contributed to the occurrence of retained placenta include gestational diabetes and bacterial infections. Women with gestational diabetes are closely monitored for potential complications throughout pregnancy. Blood values were not routinely collected or readily available for most of the animals in the current study, regardless of species. For those NHP with retained placenta, gestational diabetes was noted in the records of 3 baboons, according to their blood and urine glucose and ketone levels. Another 7 baboons were noted to have bacterial infections of the uterus postpartum. Because cultures and bloodwork were not performed for all animals in the current study, the significance of these complications is unknown. Overall, according to previous and current findings, retained placentas occur in only a small percentage of NHP after delivery, with an incidence similar to that in humans and other animal species. Concurrent tears of the vagina, indicative of a difficult delivery, were noted in several of the NHP cases of retained placenta. On examination, the fetus likewise may show evidence of the difficult delivery as bruising and redness, especially to the face in nonbreech births, which also has been noted as a sign of dystocia in pigtail macaques.⁴¹

In the SNPRC colonies, retained placenta was the most common cause of admission with regard to reproductive complications during the 15-y period (August 1999 through August 2014) that we retrospectively examined. We considered that resolution of retained placenta had occurred when all placental remnants had been evacuated from the uterus. The time to resolution ranged from immediate to 2 mo but was typically complete within 1 wk (Table 1). In all 3 colonies, most NHP were able to breed again successfully after experiencing a retained placenta. However, some dams were removed from breeding, either because of repeated reproductive problems or for unrelated reasons, and a few animals were euthanized due to complications or sequellae from the retained placenta (Table 1). Most infants that were born alive survived and experienced no adverse consequences. Some infants were raised by foster animals or in a nursery, but the majority of progeny were reared by their dams. In addition, retained placenta was often seen in conjunction with other reproductive complications, including stillbirth, premature delivery, and a history of prior cesarean section. In a few NHP, parturition was induced after a traumatic event inflicted by conspecific cage-mates. Twinning is uncommon in baboons and cynomolgus and rhesus macaques, but when it occurred in conjunction with retained placenta, both placentas were retained. After resolution of the retained placenta, followed by a recovery period of reproductive rest, many NHP were able to return to breeding. After experiencing and recovering from retained placenta, some NHP were able to give birth with no complications, others again retained the placenta, and still others never became pregnant again despite being housed with a fertile male.

Advances in the reproductive management of NHP will benefit from comparisons driven by data collection strategies oriented to all members of a reproductive breeding group prior to reproductive complications. Data meriting universal collection are gestational diabetic status, the presence of tears to the vagina, bacterial infection, gestational day at birth, parity, birth weight, and body condition score of the dams. Overall, the range of contributing physiologic differences across primate species warrants further examination.