J Med Primatol doi:10.1111/jmp.

12218

CASE REPORT

Transverse lie with prolapsed arm in a female red-howler

monkey (Alouatta guariba clamitans – Cabrera, 1940)

ga-Palazzo &
Edmilson R. Daneze, Beatriz L. Penna, Lucas F. Marcondes, Elzylene Le

rgia M. Magalha
Geo ~es
Faculty Dr. Francisco Maeda, Veterinary Hospital, Ituverava, S~ao Paulo, Brazil

Keywords Abstract
parturition – pathology-reproductive tract –
pregnancy – theriogenology-female – This study focuses on a case of a red-howler monkey (Alouatta guariba clami-
wildlife medicine tans) which was found with a fetus in a transverse lie position with a pro-
lapsed arm. The topic of this research is well justified as there are no data on
Correspondence this condition involving this type of non-human primate in literature. In this
Edmilson R. Daneze,
study, a red-howler monkey was observed by locals pulling at her pelvic
Faculty Dr. Francisco Maeda, Rodovia
^nimo Nunes Macedo, km 01, Bairro das
region for 3 days near a farm. On the third day, the monkey was found lying
Jero
Ac

acias, 14030-390 Ituverava, S~
ao Paulo, on the ground at which point she offered no resistance when approached.
Brazil. The environmental police took the monkey to receive medical attention. Dur-
Tel/Fax: +55 16 3729-9060; ing the physical examination, it was quickly observed that the monkey was
e-mail: eddaneze@hotmail.com pregnant; the right forelimb of the fetus was exposed from the vulva. An
ultrasound revealed a non-viable fetus, and due to the severe weakness of the
Accepted April 25, 2016.
mother, we opted for euthanasia. During the necropsy, not only was the fetus
found macerated but it was also in a transverse lie position with a prolapsed
arm and presented no external or internal injuries consistent with trauma.

birth that cannot occur by the forces of the mother

Introduction
The red-howler monkey (Alouatta guariba clamitans,
Cabrera, 1940) is found throughout the Atlantic Rain-
forest, stretching from the southern state of Bahia in
Brazil to the southern area of this biome, reaching the
Department of Misiones in northern Argentina [23, 37,
39]. It is an endangered species in which its disappear-
ance is due to habitat destruction [10, 23, 56].
Birth can be defined as the act or process of bringing
forth young from the womb [43, 84, 89]. Labor is trig-
gered by the fetus, which prompts hormonal changes in
the mother [40, 74, 84]. Any alteration from what is
expected in the normal progression of each phase of par-
turition is a sign of dystocia, including changes in fetal
presentation, absence of cervix dilation, or absence of
uterine contractions [44, 66, 67].
Dystocia is one of the most serious and frightening
conditions in veterinary obstetrics due to the maternal
and neonatal complications that are associated with this
condition [38]. Etymologically, dystocia means ‘difficult
birth’ [88], and in obstetric terms, it is used to describe a
alone [9, 88]. Dystocia can occur due to maternal or
fetal origin, several factors may contribute to its
occurrence [40, 44, 51, 57, 64].
This study reports a case of transverse lie with a pro-
lapsed arm in a red-howler monkey (Alouatta guariba
clamitans, Cabrera, 1940). The topic of this research is
well justified as no data are found in literature on this
condition involving this kind of non-human primate.
Case report
All procedures performed on the animal mentioned in
this study were in accordance with the current estab-
lished guidelines and regulations for animal welfare and
were reviewed and approved by the Ethics Committee
on Animal Use (CEUA-FAFRAM_FE), protocol
number 44/2014.
A pregnant red-howler monkey (Alouatta guariba
clamitans, Cabrera, 1940) weighing approximately
7.0 kg was rescued by the environmental police in Itu-
verava, SP near a farm in the city of Miguelopolis, SP.

J Med Primatol 45 (2016) 156–162

156 © 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Daneze et al.
She was taken to the Veterinary Hospital at the College
of Dr. Francisco Maeda (FAFRAM/FE) for medical
assistance.
According to the environmental police, the animal
had been observed by locals for 3 days, and when
approached, it would flee. The locals from the area
claimed that the female was pulling at something that
appeared to be stuck near her pelvic region. On the third
day, the animal was found on the ground next to a tree
and offered no resistance upon approach.
During the physical examination, the animal was
observed as being debilitated and very weak. She also
presented tachycardia, tachypnea, and pulmonary
crackles were heard using a stethoscope. Increased pale-
ness in mucous membranes was observed, and she had a
capillary refill time (CPT) of 4 s and presented
hypothermia (36.3°C). The vulva presented a brownish
discharge with a foul odor and insinuated fetus, expos-
ing the right forelimb. The exposed fetal limb was dark
red in color with blackened edges and disjointed bones,
when handled, it was confirmed that it was still attached
(Fig. 1A).
A hematology and serum biochemical analysis was
not made due to the difficulty of cannulating the periph-
eral vein to collect a blood sample. Fetal evaluation was
difficult to determine with an ultrasound due to the
large amount of intrauterine gases; however, it was pos-
sible to confirm the absence of vital signs.
Upon confirmation of fetal death combined with the
mother’s severe level of weakness and having a poor
prognosis for surgery, we opted for euthanasia. Due to
(A)
(C)
Fig. 1 (A) Lateral–medial view of the fore-
limb of the red-howler monkey, lightened
fetus in the vulva during dystocic labor (ar-
row). (B) The pregnant uterus of the red-
howler monkey, during autopsy, observe the
exposed forelimb (arrow). (C) Fetus with
consequent distortion of the features caused
by the mothers attempt to remove it. (D)
The usual formation of the head and face of
the fetus. FAFRAM/FE. Ituverava-SP, 2012.
J Med Primatol 45 (2016) 156–162
© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Transverse lie position in red-howler monkey
the difficulty in cannulating the peripheral veins, we
opted for venous access through the brachiocephalic
vein, near the brachial plexus. The euthanasia protocol
consisted of fixed anesthesia with propofol (5.0 mg/kg)
followed by an intravenous injection of potassium chlo-
ride (100 mg/kg) [90].
During the necropsy, no external or internal injuries
were found that would be consistent with trauma. How-
ever, foam was observed in the distal portion of the tra-
chea and pulmonary bronchi, indicating swelling, there
were also food contents in the stomach and feces in the
intestines, indicating that the animal was feeding nor-
mally. The liver had two longitudinal fibrous lines in the
left medial lobe, indicating old injuries that had already
healed, and also presented a mild pale yellow pigmenta-
tion on the external surface, compatible with steatosis.
There were no significant changes in the other organs.
The uterus was isolated (Fig. 1B) and in the external
evaluation it was observed that it presented no punc-
tures or lacerations, it was tight and distended, it was
predominantly pale with some reddish areas, compatible
with tissue hemorrhage. After a longitudinal incision, it
was observed that the tissue was thin and had discreet
mucosal swelling, the inner face had reddened and
blackened areas compatible with tissue bleeding as well
as a brownish discharge with a foul odor.
The fetus had no vital signs, was swollen, emphyse-
matous and presented a foul odor, which suggests that it
had been dead for some time and was in the process of
maceration. It was in a flexed breech position with the
head bent forward and the left thoracic and pelvic limbs
(B)
(D)
157
Transverse lie position in red-howler monkey
bent, and the right shoulder was in the right acromion–
iliac position, noting to be in a transverse lie position
with a prolapsed arm (Fig. 1C). Irregularities were
observed in the face which suspected malformation, but
after further handling, it was obvious that this malfor-
mation was due to the mothers attempt to remove the
infant from her uterus (Fig. 1C and D).
Discussion
For the development of this report, we searched for
studies that could help in understanding the population
dynamics, reproductive aspects, and diseases of
A. g. clamitans primates that inhabit the Miguelopolis,
SP region in Brazil. However, no studies with informa-
tion on this colony in particular were found, as well as
in colonies of these primates in other forest remnants
[2, 5, 24, 35, 50].
According to the Environment Ministry of Brazil [12],
there are only a few long-term studies that provide data
on the A. g. clamitans; there is a huge gap in its biodi-
versity, social aspects, and health of this population.
This is because the primates of the genus Alouatta
(Lac
epede, 1979), despite being widely distributed
throughout Central and South America, have great abil-
ity to survive in highly fragmented environments [26, 56,
76, 79], as the Atlantic Rainforest in Brazil [47, 52],
inhabiting areas ranging anywhere from 4 to 41 hectares
[2]. Furthermore, studies indicate that the landscape
fragmentation can modify aspects of the biology of
these species, for example, the mode of use of space and
the migration pattern [20, 21, 25, 31, 60], enabling the
formation of groups which can vary widely among spe-
cies and less within species [14].
Dystocia can occur in all domestic females [85]. It is
considered relatively common in non-human primates
[32, 81]. When searching different available databases,
few reports were found on cases of dystocia in non-
human primates [29, 72, 75, 80, 82], and none of which
made reference to the condition that was present in this
particular red-howler monkey (A. g. clamitans).
The basic causes for the occurrence of dystocia in
female animals can be hereditary, nutritional, handling,
infection related, trauma, or even due to combined
causes [57, 66]. In female monkeys, the predisposing fac-
tors include size, presentation, and position of the fetus
as well as maternal pelvic abnormalities [15, 32], or can
be associated with the age and parity of the female mon-
key [80]. Algovik et al., 2010 [4] report that dystocia in
women may be linked to the chromosome 12p12 and
five additional loci; however, it is suggested that broader
studies be carried out.
158
Daneze et al.
The gestation period in female red-howler monkeys
(A. g. clamitans) is approximately 185 days [68].
Uncomplicated labor usually lasts 1–4 hours with the
vast majority of infants delivered head first [32]. The
delivery usually occurs at night [11, 32, 40]; however,
there have been reports of births occurring during the
day [16, 30, 63], which facilitates the detection of possi-
ble dystocia [11]. In this case, it was not possible to esti-
mate the onset of the female monkey’s labor because it
was a free living animal.
According to [11, 32], New World primates are sus-
ceptible to dystocia due to the fetal size in relation to the
size of the mother.
Locals from the area reported that they had been
watching the female monkey for 3 days and that the pri-
mate was pulling at something that seemed to be stuck
near her pelvic region, which happened to be the fetus.
It is understood that during the physiological process of
expelling the fetus and due to the transverse position
and the infant’s right forelimb being exposed first, it was
impossible for the rest of the infant’s body to pass
through the birth canal due to anatomical limitations of
the pelvis [18] and abnormal fetal presentation. With the
discomfort and pain characteristic of labor [3, 45] and
with the associated pain with unfinished labor, the par-
turient mother must have attempted to remove the
infant which caused the displacement of the limb bones
that was observed.
In this case, it is very likely that the death of the fetus
was due to acute fetal distress [78] as a result of
intrauterine asphyxia [22, 71]. According to [62], during
labor, uterine contractions decrease uteroplacental
blood flow, causing a temporary or permanent reduc-
tion of the oxygen supply to the fetus, favoring the
occurrence of fetal hypoxia, hypercapnia, and acidosis
with consequent death. According to [8], a period of
cerebral hypoxia for more than minutes can cause fetal
death.
When there is fetal death with an open cervix in early
pregnancies and fetuses are not eliminated from the
uterus by abortion, they evolve to macerated fetuses
[33, 41]. Maceration is a destructive aseptic process of
disintegration of a retained fetus in the uterus, which
softens and liquifies the fetal tissue leaving only the
skeleton [1, 13, 85]. In addition to characterizing the
presence of gas in the uterus and purulent vulvar dis-
charge presenting a foul odor [41, 54, 59], this putrefac-
tive process usually determines the development of
toxemia in the female [1, 19, 41, 70] or brings the onset
of excessive hemostasis, with a risk of disseminated
intravascular coagulation (DIC) and multiple organ
failure [77].
J Med Primatol 45 (2016) 156–162
© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Daneze et al. Transverse lie position in red-howler monkey

Authors [27, 46, 48, 81] explain that a difficult delivery
rarely results in maternal death, making it prudent to ini-
tiate fluid therapy and supportive care to stabilize the
patient prior to performing surgery. However, in many
cases, the mother can die as a direct consequence of the
long and difficult labor associated with physical exhaus-
tion, uterine hemorrhage, uterine atony, sepsis, or shock
[81]. Therefore, considering the clinical conditions of the
female in this report, it was clear that she would not last
long and would most likely die from sepsis or shock
within a few hours or while under anesthesia. Further-
more, when it has been established that an animal is in
moribund condition, meaning that it is near death or in
the process of dying [34], it should be euthanized as soon
as possible to prevent further distress or suffering [6, 58].
In humans, the obstetric conduct in cases of fetal
death is to induce vaginal delivery [7, 55, 73], in some
cases a cesarean delivery is also an option [69]. When
dealing with animals, there are several ways to intervene
in cases of obstructed labor which varies according to
species and may or may not enable vaginal labor [64].
As for female monkeys in instances where there are clin-
ical indications of dystocia, the treatments can vary. If
the fetus is lodged in the vaginal canal manual extrac-
tion can be an option, however for non-human pri-
mates, cesarian section is more common [15] and is the
recommend procedure in cases of dystocia in female
monkeys [40, 65].
For an elective cesarean section, it is vital to time
the operation to make sure that the fetus has matured
enough for extrauterine survival [15]. In recent years,
obstetric ultrasound examinations have become rou-
tine, making it easier to anticipate the diagnosis of any
form of fetal compromise, including information
regarding fetal position and presentation, as well as
morphology and viability [36, 53]. In veterinary medi-
cine, due to pregnancy variations within the same ani-
mal species, there are no protocols of prenatal tests.
However, numerous studies have been developed in
this context to better understand and assess the gesta-
tional period and fetal biometric morphology [17, 28,
42] as well as female structures involved in delivery
[61, 83, 86], including female monkeys [49, 87]. As the
female monkey in this case was a free living animal,
the use of ultrasound only enabled confirmation of
fetal death [81], dystocia was visible through fetus
exposure from the vulva.
Conclusions
It is concluded that the case discussed in this report
reveals dystocia caused by changes in fetal presentation
followed by mummification and a likelihood of tox-
emia. Behavioral changes were the first symptoms
observed in the free living animal. The time between
this observation and medical intervention in cases of
dystocia is noted to be critical to the survival of both
mother and infant.
Conflict of interest
The authors declare no potential conflict of interests.

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