Assessment of fetal well-being is an area of on-going research. We are particularly interested in predicting or determining fetal stress so that treatments aimed at preventing abortion or pre-mature birth. This information would allow us to "prophylactically" applying these treatments in females speculated to be "at risk". Behavior of the Dam - The behavior of the dam must not be underemphasized. If the dam is behaving normally, eating normally, and no changes in routine have been observed, then most likely the fetus is fine. We consult with many owners about "overdue" birthing. Many of these females ultimately are found not to be pregnant. Occasionally, prolonged gestation does occur in llamas and alpacas and the causes are not well understood. Our protocol for evaluation of females that are 11.5 months or longer in gestation is to perform a complete physical examination, rectal and vaginal examination, ultrasound examination, and fetal heart rate assessment. If the dam and fetus are normal in all respects, then the pregnancy is allowed to continue undisturbed. Using this protocol, we have had excellent success with healthy neonates being born. Occasionally, an abnormal or stillborn cria is born, but these are far outnumbered by the problems caused by premature termination of pregnancy. The problem is knowing what is "normal" with these tests and how to conduct them. Rectal, and Vaginal Examination - Rectal palpation is often difficult in alpacas because of their small size, but most mature llamas can be palpated if proper pre-cautions are observed. A solid sided llama or alpaca restraint chute is important to allow easy and efficient reproductive examinations. Performing these diagnostic tools on free-standing females or females pressed against a wall are stressful for the patient, veterinarian, and owner. Sedation should be used sparingly. When needed, butorphenol tartrate (0.1 mg/kg IV or IM) provides excellent sedation with minimal to no untoward effects on the fetus or dam. Before rectal palpation, I prefer to place 60 to 100 ml of lubricant into the lumen of the rectum. In small females, 10 ml of lidocaine can be added to help relax the anal sphincter. Rectal palpation should be performed with caution because rectal tears have been reported to occur in llamas. The examiner should make the owner aware that bleeding from the anal sphincter is common when rectal palpation is performed. This is caused by over-stretching of the mucous membrane and sphincter muscle. This does not pose a risk to the animal in most cases (I have never seen a complication from mild anal sphincter bleeding). Rectal examination should be used to assess fetal movement, uterine tone, position of the broad ligaments (rule out uterine torsion), and the presence of adhesions or other periuterine masses. An interesting observation is that we have found the head and front limbs of the fetus within the pelvic canal up to 3 months before parturition. Also, we have failed to find the head and feet of the fetus within the pelvic canal as early as 3 days before parturition in llamas and alpacas to whom the cria was ultimately delivered in a normal anterior, longitudinal, dorsosacral position. Using these qualitative methods, we can say that the fetus is alive, but no definitive comment can be made concerning fetal stress. Vaginal examination will allow assessment of the cervix for inflammation, discharge, and the presence of the mucous plug. If the cervix is closed and no discharge is noted, then we can say that all appears normal, but no definitive statement can be made concerning fetal stress. Hormonal Tests - Many owners and breeders have relied upon serum progesterone concentration to assess pregnancy status. We have not found an association between fetal stress and serum progesterone status, but we have not had the opportunity to perform serial assays on "at risk" females. My opinion is that a sudden decrease in serum progesterone would be found too late for effective treatment to be initiated. No "llama or alpaca side" progesterone test has been developed to date. However, we have conducted research correlating serum progesterone assays with the commercial test kits available for canine (Target Canine Ovulation Timing Kit, BioMetallics, Princeton, NJ) and equine (Target Equine Breeding System, BioMetallics, Princeton, NJ) progesterone (Table 1). In our study, we found the equine kit was more consistently correctly interpreted, but the accuracy of the tests is broad (C2/3 range = 1 to 5 ng/ml). Ultrasonography - Ultrasonography is useful for non-invasive evaluation of the intrauterine environment and fetus. This is the mainstay of our current state-of-the-art evaluations. If the fetal thorax and heart can be seen, the fetal heart rate (FHR) can be counted. I routinely use a 5 MHZ linear transducer for evaluation of all stages of pregnancy (approximately 12 to 15 cm penetration of adequate resolution images). A 3.5 MHZ transducer can be used for deeper penetration of the abdomen (up to 20 to 23 cm), but significant loss of image resolution occurs at these depths. Most modern ultrasound machines are equipped for simultaneous B- and M-Mode ultrasonography. This allows assessment of fetal heart rate and some quantitative estimates of cardiac contractility. If the uterine fluid appears normal, then we would assume that the fetus-placenta-dam unit is normal. The placenta can be evaluated to a certain extent and premature separation of the placenta or placental edema may be found in females having had a uterine torsion. These findings suggest that a C-section may be necessary to save the life of the cria. If the FHR is normal, we would assume that the fetus is normal (adequate oxygen supply and waste removal). In our fetal stress research, we have determined that normal fetal heart rate range for alpacas and llamas is 80 to 120 (fetal heart rate ranges from 1.5 to 2.0 x maternal heart rate (MHR)). The late gestation fetus (> 6 to 7 months) is positioned in the uterus with the fetal head and thorax located near the maternal xiphoid bone just to the right of midline. Thus, the hair may need to be clipped to allow ultrasonography of the fetal heart. Most owners do not object to having this done because this region of hair removal is not seen and is not economically important. Occasionally the fetal heart can not be found because of fetal positioning (fetal backbone or maternal viscera obstruction of ultrasound waves, positioning too deep in the abdomen for viewing, etc). Also, we have seen fetal ultrasound examinations where there was no apparent heart beat, but the fetus was alive and was normal at birth. Thus, fetal heart ultrasound images must be interpreted with caution. Fetal ECG - In our early research to establish a tool for assessment of fetal stress, we attempted to perform fetal ECG. This technique has been used successfully in horses to assess fetal heart rate and rhythm. We used several models of ECG machines including a physiograph with high sensitivity leads and were unable to consistently record fetal ECG patterns. In the llamas and alpacas we tested, the fetal complexes were only intermittently recorded and were usually buried within maternal complexes such that they were unrecognizable. Rarely, we could obtain a clear ECG complex, but we were not able to determine rate or rythm in any fetus. We concluded that fetal ECG's are seldom successful because of the size of the abdomen, position of the fetus, low magnitude of fetal complexes, and the overwhelming ECG of the dam. To date, we have not been able to record any diagnostic fetal ECG segment. Fetal Cardiotocography - Recently, we have been investigating the use of fetal Doppler ultrasound for assessment of fetal well-being (Fetal Monitor 155, Corometrics Medical Systems, Inc, Wallingford, Conn, USA). The Fetal Heart Monitor records fetal heart rate and heart rate variability (external Doppler probe), and uterine contractions (external probe with pressure sensor). Jonker has published a text on cardiotocography in cattle. This text is recommended reading for those interested in developing skills in fetal heart monitoring. Rabello and Lapidus published a text on electronic fetal monitoring in humans and this text is highly recommended for knowledge of techniques for assessment of fetal stress. The Corometrics unit has the ability to record FHR and uterine activity pressure waves in humans. To date, we have not been able to successfully record diagnostic uterine activity tracings because of interference by forestomach motility, maternal movement, fetal movement, and the maternal abdomen geometry. However, we have been able to consistently and reliably record fetal heart tracings to assess rate and variability. Based on Doppler ultrasound recordings of fetal heart rate, we determined that FHR is expected to be between 80 and 120 (roughly 1.5 to 2 times the MHR). However, the normal fetal heart rate is not consistent from moment to moment. We have identified three fetal heart rate patterns: 1) low frequency undulation, 2) sudden acceleration followed by deceleration, 3) no undulation. Based on our clinical research, low frequency undulations are the normal pattern for gestating fetuses of llamas and alpacas. At this time, we are not certain about the significance of rapid accelerations and decelerations or the absence of undulation. I feel that the absence of undulation may represent periods of fetal quiescence and are not abnormal unless they are associated with low heart rate (FHR < 60). The only FHR's that we have seen that were consistently below 60 were in dams with severe illness and the cria ultimately were delivered by C-section or were aborted. Rapid acceleration and deceleration have been reported to occur in cattle, but were uncommon. These periods may be associated with sudden fetal movement, maternal excitation, uterine contraction, or unknown stimuli. We have observed this pattern in only one alpaca and the recording was obtained 2 days after non-surgical correction of a uterine torsion. In that alpaca, we elected to perform a C-section because of concerns for fetal stress. At surgery, premature separation of the placenta seemed to have occurred but a live male cria was delivered. This episode of sudden FHR acceleration was thought to have occurred because of developing fetal hypoxia. REFERENCES: Jonker FH. Cardiotocographic monitoring of the bovine fetus. University of Utrecht (ISBN 90-393-0425-4) 1993 (171 pages). Rabello YA, Lapidus MR. Fundamentals of electronic fetal monitoring. Corometrics Medical Systems, Inc, Wallingford, Conn. 1988 (162 pages). Deans AC, Steer PJ. The use of the fetal electrocardiogram in labor. Br J Obstetrics and Gynecology. 1994;101:9-17. Jonker FH, van Oord HA, van Geijn HP, et al. Feasibility of continuous recording of fetal heart rate in the near term bovine fetus by means of transabdominal Doppler. Vet Quarterly 1994;16:165-168. Jonker FH, van Geijn HP, Chan WW, et al. Characteristics of fetal heart rate changes during the expulsive stage of bovine parturition in relation to fetal outcome. Am J Vet Res 1996;57:1373-1381. Cohen S, Mulder JH, van Oord HA, et al. Noninvasive monitoring of fetal heart rate during the last ten days of gestation in sows. Am J Vet Res 1997;58:1285-1290. Table 1. Serum progesterone concentration study comparing results of laboratory RID with that of canine-side and equine-side test kits. Camelid
Laboratory Assay
Canine Kit
Equine Kit 1
1.5
C3*
C2 2
1.42
C2
C2 3
1.4
C2
C2 4
0.33
C2*
C1 5
0.09
C2*
C1 6
0.04
C2*
C1 Target Equine Breeding System: C1 = 0 - 1 ng/ml; C2/3 = 1- 5 ng/ml;
C4 = 5 ng/ml Target Canine Ovulation Timing Kit: C1 = 0 - 1 ng/ml;
C2 = 1 - 2.5 ng/ml; C3 = 2.5 - 5 ng/ml;
C4 = 5 ng/ml * indicates false positive test result David E Anderson, DVM, MS
Head and Associate Professor of Farm Animal Surgery
Director, International Camelid Initiative
601 Vernon L Tharp Street
College of Veterinary Medicine
The Ohio State University
Columbus, Ohio 43210
Anderson.670@osu.edu
Phone: 614-292-6661 Fax: 614-292-3530
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