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Set in 9.5/12.5pt STIXTwoText by Straive, Pondicherry, India
Book Dedication
This book is dedicated to my wife, Kristine, and daughters, Olivia, Pip, and Estelle, and their steadfast support of me over the years as an equine veterinarian; to Pam Wilkins, my emergency and critical care mentor and friend; to all my colleagues at the Lloyd Veterinary Medical Center (Iowa State University), Marion duPont Scott Equine Medical Center (Virginia Tech), and New Bolton Center (University of Pennsylvania) – it has been a pleasure to work together through so many foaling seasons with you; and to all the mares and foals that we have had the honor to provide veterinary care to.
David M. Wong
I would like to dedicate this book to those who came before us, the editors of the original Equine Clinical Neonatology book, Anne Koterba, Willa Drummond, and Philip Kosch, and to all our patients and dedicated veterinarians caring for them over the generations since.
Pam A. Wilkins
Contents
List of Contributors xiv
Foreword xix
Preface xx
Part I The Newborn Foal 1
Chapter 1 Postpar tum Adaptation of the Newborn Foal 3
Section I Fetal Heart Rate and Fetal ECG 3
Section II Fetal Circulation and Cardiorespiratory Transition 8
Section III Maturation of the Lung and the Surfactant System 12
Section IV Onset of Breathing 26
Section V Control of Breathing 32
Section VI Renal Transition from Fetus to Newborn 37
Section VII Newborn Physical Examination 42
Chapter 2 Principles and Theory of Cardiopulmonary Resuscitation (CPR) 51
Chapter 3 The Premature and Dysmature Neonatal Foal 64
Part II Disorders of the Neonatal Foal 79
Neonatal Respiratory System 81
Chapter 4 Embryology and Anatomy of the Respiratory System 81
Goulburn Valley Equine Hospital Congupna, Victoria, Australia
Ashlee Watts, DVM, PhD, DACVS
Associate Professor
Texas A&M University College Station, TX
Robin White, DVM, DACVR
Clinical Assistant Professor Iowa State University Ames, IA
David Whitley, DVM, MS DACVO Professor Emeritus University of Florida Gainesville, FL
Pamela A. Wilkins, DVM, MS, PhD, DACVIM, DACVECC Professor University of Illinois Urbana, IL
Edwina Wilkes, BVSc, MPHarm, FANZCVS, DVStud Lecturer in Equine Medicine
Charles Sturt University
New South Wales, Australia
Jarred Williams, DVM, PhD, DACVS, DACVECC
Associate Professor University of Georgia Athens, GA
Sharon Witonsky, DVM, PhD, DACVIM Associate Professor
Virginia Maryland College of Veterinary Medicine Blacksburg, VA
David Wong, DVM, MS, DACVIM, DACVECC Professor Iowa State University Ames, IA
Kate Wulster Bills, VMD, DACVR
Clinical Assistant Professor University of Pennsylvania Kennett Square, PA
Amanda Ziegler, DVM, PhD Research Assistant Professor North Carolina State University Raleigh, NC
Foreword
Anne Koterba, DVM, PhD
It has been quite a few years since Willa Drummond, Philip Kosch, and I published Equine Clinical Neonatology—a few decades, in fact! Back then, few hospitals or clinics had space or personnel dedicated to the care of critically ill equine neonates, and there was little advanced training available for clinicians interested in caring for these small patients. But horse owners increasingly demanded improved care and outcomes given economic factors and other considerations, such as the advances already made in human neonatology. When the book was published in 1990, it represented over 10 years of intensive clinical and basic research on the equine neonate. Our “green book” was designed to share what we had learned so that others— including clinicians, students, veterinary nurses, and horse owners—could provide better veterinary care for compromised neonatal foals.
Looking back at that time, I feel our productivity during that decade in terms of advancing the field of equine neonatology was the result of the collaboration of a large team that worked amazingly well together because we were all focused on the goal of improving outcomes for sick foals. These partners included equine organizations that provided important research funding, as well as veterinary clinicians, residents, and basic scientists who worked together in both university and private practice settings to better understand the physiology, pharmacology, and disorders of the equine neonate. A large group of medical specialists, including human neonatologists, respiratory and physical
therapists, and nutritionists, volunteered their time and provided important advice and perspectives on accurate identification of disease and treatment of neonates. Veterinary technicians, veterinary students, horse lovers, and community volunteers formed “foal teams” and provided essential around-the-clock intensive nursing care. I still feel very fortunate to have been a part of this innovative collaborative effort.
At the time, our book reflected the state of the art in equine neonatal intensive care. But in the years since, the number of veterinarians, students, and nurses caring for equine neonates has increased greatly. These individuals have expanded our knowledge of the topics we covered in our original book, and this increased understanding of the adaptive physiology from fetus through neonates—along with significant advances in diagnostics, treatments, and nursing care—has greatly improved our neonatal patients’ outcomes. Much of this work has contributed to the material covered by this new book.
I want to thank and congratulate David and Pam for taking our concept of the original book and running with it, updating older information and introducing new knowledge. There are now many hospitals and clinicians with space, equipment, and personnel both interested in and capable of delivering high-quality care to equine neonates. This book, like our original, is for the dedicated veterinarians, interested students, and nurses who support them and deliver this care.
Preface
In the year 1990, Drs. Anne Koterba, Willa Drumond, and Philip Kosch edited and published the first and only edition of Equine Clinical Neonatology. Many veterinarians refer to this small little green book as the reference text for equine neonatal care and without a doubt, over the years, this book has served as an invaluable reference and resource for countless clinicians in their quest to provide veterinary care to neonatal foals. Over the past 30 years, veterinarians and researchers have greatly advanced our understanding of physiology, disease processes, and therapeutic options as it pertains to equine neonatal medicine and critical care. Although many aspects of the foal remain to be studied, the goal of this book is to relay new discoveries and provide clear and comprehensive information on disease processes and their treatment in neonatal foals. This information on equine neonatal care is targeted to veterinary students, practicing veterinarians, and equine veterinary specialists so that we can better serve our patients and their owners.
This textbook is authored by experts in the field of equine perinatology and is organized by body systems;
within each system, subtopics such as embryology and anatomy, clinical physiology, diagnostic procedures, congenital disorders, and specific disease processes and treatment are discussed. Furthermore, one section is dedicated to general treatment principles for the equine neonate.
We are incredibly grateful for the expertise and generosity shared by the various contributors to this textbook. Their willingness to spare their time in authoring these chapters and share their individual depth of knowledge and clinical experience form the foundation of knowledge for this textbook and allows us to expand on the information provided by the original neonatal textbook published by Drs. Koterba, Drumond, and Kosch. It is our sincere hope that this text, Equine Neonatal Medicine, will prove to be a valuable resource to all those involved in the care of the neonatal foal.
David M. Wong
Pamela A. Wilkins
Part I
The Newborn Foal
Chapter 1 Postpar tum Adaptation of the Newborn Foal
Section I Fetal Heart Rate and Fetal ECG
Throughout the course of gestation, the maternal and fetal heart rates (FHR) are monitored as a general reflection of health. In the healthy mare, the mean maternal heart rate slowly increases, from 150 days gestation to term [1]. Maternal heart rate in late gestation is relatively constant during the last 15 days of pregnancy with a mean ± SD heart rate of 53 ± 1 beats/min prior to parturition. After parturition, heart rate significantly decreases to 42 ± 1 beats/ min (Figure 1.I.1) [2]. The fetal heart is not as easily monitored as the mare but can be measured using fetal electrocardiography (ECG) or ultrasound. Determining the FHR via ECG is a simple parameter used to monitor fetal wellbeing in the pregnant mare, but this technique has been largely supplanted by determination of FHR through transabdominal ultrasonographic visualization of the fetal heart beat and rate. Acquisition and interpretation of the fetal ECG can be hampered by the larger amplitude of the maternal ECG signal, movement of the mare, small amplitude of the fetal ECG signal, and fetal position. Despite these limitations, most clinicians familiar with fetal ECGs have little difficulty acquiring cardiac activity of the equine fetus [3]. In addition, fetal ECG can be used in a continuous fashion via telemetry, allowing detection of fetal arrhythmias as well as more prolonged monitoring of FHR trends, while the mare is maintained in a quiet stall environment. Fetal ECG can also be used through stage I of labor.
Acquisition of a maternal ECG is initiated first, using a base-apex lead configuration, to differentiate the maternal heart rate and rhythm and confirm the maternal cardiac activity as compared to the fetal cardiac activity obtained via fetal ECG lead placement. A guide to electrode placement for fetal ECG includes the following, keeping in mind that electrode placement may have to be modified based on fetal position: left arm lead on the dorsal midline of the mare in the mid-lumbar region; right arm lead on the ventral midline 10–15 cm in front of udder; and neutral lead
anywhere on the trunk of the horse (i.e. left croup) [3]. In late-pregnant mares, the right arm lead may have to be positioned on the right ventral abdomen at a level approximately at the height of the stifle [3]. Electrodes with alligator clips can be used, but electrodes with adhesive pads, reinforced with rapid-drying adhesive glue, can be used for longer or repeated use and is better tolerated by the mare. Conventional and telemetric methods can be used to acquire the ECG tracing. If conventional methods are used, recordings are performed over 10- to 20-minute periods, several times a day. Telemetry allows for continuous monitoring, with paper tracings recorded at approximately 2-hour intervals [4]. Both the maternal and fetal cardiac activity will appear blunted as compared to a maternal base apex lead (Figure 1.I.2) and the tracing can be lost in artifact or background interference. The maximum amplitude of the fetal ECG ranges from 0.05 to 0.1 mV [4].
Volumes of information are available to the obstetrician in regard to monitoring fetal health and viability in human fetuses. In comparison, a trivial amount of published information is available to the equine clinician. However, some of the pertinent information in regard to the fetal response to hypoxia and fetal ECG changes associated with fetal distress and hypoxia in the human fetus can be extrapolated to the equine species, with the disclosed fact that there may be unknown differences between species. Of note, much of the published information in reference to the human fetus’s response to hypoxia has been established via experiments performed in fetal sheep.
The clinician should recognize that transient accelerations and decelerations in FHR are present in the healthy fetus. In fact, the presence of intermittent FHR accelerations associated with fetal movement is believed to suggest adequate oxygenation to maintain normal fetal autonomic nervous system function [5]. However, persistent tachycardia or bradycardia can signal fetal distress. One must first recognize that despite the fact that the fetus has twice the
Neonatal Medicine, First Edition. Edited by David M. Wong and Pamela A. Wilkins.
David Wong
–15–10
–5–4–3–48–24 024483 45 –15–10
Days before parturition
Hours before and after parturition
Days after parturition
–5–4–3–48–240 2448 34 5
Days before birth
Hours before and after parturition
Days after birth
Figure 1.I.1 Maternal (a), fetal and newborn (b) peri-parturient hear t rates in the horse. Arrow indicates time of parturition [2].
(a)
(b)
Figure 1.I.2 Fetal and maternal ECG (a). Maternal “M” and fetal “F” signal. Fetal and maternal rates are 48 and 83 beats/min, respectively. In (b), fetal and maternal heart rates are more similar, emphasizing need for careful inspection [4].
oxygen demand as the adult, and yet far lower partial pressures of oxygen and hemoglobin saturations, the fetus has a remarkable ability to compensate for sub-normal provision of oxygen that is necessary to maintain health in the adult [6–8]. In reality, under normal conditions, the fetus has a surplus of oxygen available and is able to survive profound hypoxia for extraordinary periods of time, often without injury [6–8]. This is possible because of the combination of notable fetal anaerobic tolerance and the fetal capacity to establish a coordinated cardiovascular and metabolic defense to hypoxia [8–10]. During episodes of acute hypoxia, peripheral chemoreceptors are stimulated, resulting in a coordinated cardiovascular response designed to
sustain perfusion [6–8]. This chemoreflex response balances the severity of the hypoxic insult with the cellular tolerance of the individual [11]. In addition, once initiated, the response is titrated to the hypoxic insult, producing varied responses that are manifested clinically as variable decelerations in FHR [12].
The initial response in the near-term fetus to acute hypoxic challenge is mediated by parasympathetic pathways that result in rapid deceleration in FHR, with the degree of deceleration broadly related to the severity of hypoxia [13–15]. Shallow decelerations in FHR are associated with modest reduction in uteroplacental flow whereas more profound decelerations in FHR suggest near total or
total reduction in uteroplacental flow [15, 16]. Fetal bradycardia in response to hypoxic challenge reduces cardiac workload and is likely a defense mechanism present to preserve cardiac glycogen and reduce cardiac stress [17]. Slowing of the FHR may also allow increased exposure of the fetal blood to maternal blood, thus increasing the time for equilibration of dissolved gas from the placenta and improving oxygen content of fetal blood [4, 18, 19]. Regardless of the reduced FHR and concomitant decrease in cardiac output, the fetus maintains blood pressure and normal oxygen delivery to vital organs during moderate hypoxia by peripheral vasoconstriction [6–8, 11, 20]. If mild to moderate hypoxia is sustained, bradycardia is followed by tachycardia, a response that is mediated by increases in circulating catecholamines [21]. Tachycardia allows for ventricular output to contribute to maintaining of blood pressure while allowing peripheral vasoconstriction to abate, consequently permitting more perfusion to peripheral organs to occur [7]. This increase in heart rate does not occur if the hypoxic insult is more severe, in which case bradycardia becomes progressively more profound and is likely related to direct effects of hypoxia on the heart itself [11]. Interestingly, in fetal sheep, age-related differences in the FHR response to hypoxia were observed in that a similar hypoxic challenge that elicited bradycardia followed by tachycardia in near-term fetuses was not observed earlier in gestation; this lack of response might be related to immaturity of neurohormonal regulators and chemoreceptor function [7, 22, 23].
In horses, transcutaneous fetal ECG can be used to evaluate fetal well-being and viability in pregnant mares from approximately 150 days of gestation to parturition. As a general trend, the FHR decreases gradually from 150 days gestation to term (Table 1.I.1). Sporadic episodes of tachycardia are typically observed throughout gestation in the healthy equine fetus and may be associated with fetal movements (Table 1.I.1). Other underlying causes of
fetal tachycardia include maternal medications, maternal medical disorders, obstetric bleeding, and fetal tachyarrhythmia [5]. In contrast, fetal bradycardia is not typically observed during normal gestation and, in people, has been associated with maternal hypotension, umbilical cord prolapse, rapid fetal descent, excessive frequent uterine contractions and uterine rupture or fetal congenital heart defects [1, 5]. Thus, substantial and/or prolonged increases or decreases in fetal heart can indicate fetal distress.
The definition of fetal bradycardia and tachycardia remains obscure in the horse with normal FHR ranging from 65 to 115 beats/min in the last months of gestation [4]. During the last weeks of gestation, the baseline FHR ranges from 60 to 75 beats/min with the lower range being 40 to 75 beats/min. In one study, the lowest measured FHR was <70 beats/min in 80% of fetuses evaluated, <60 beats/min in 55%, and <50 beats/min in 14%. In contrast, the highest FHR measured were in the range of 83–250 beats/min, with 86% of fetuses having a FHR >100 beats/min, >120 beats/min in 50% and >200 beats/min in 20% [24]. Thus, if the FHR is <60 or >120 beats/min over a prolonged period of time, repeated evaluation is indicated. One source suggests persistent fetal tachycardia as a heart rate over 200 beats/min at 120–220 days gestation and greater than 110 beats/min from 280 days gestation to parturition; bradycardia is defined as a FHR <60 beats/min at any stage of gestation [25].
Persistent fetal bradycardia usually coincides with late gestation asphyxia, whereas persistent tachycardia may represent early effects of hypoxia, maternal pyrexia, or a prolonged acceleration pattern in a healthy fetus [26]. The fetus is dependent on the placenta for oxygen supply, and a reduction in fetal cardiac activity is the only means to reduce cardiac oxygen consumption. Thus, the primary response to fetal hypoxia is a reduction in heart rate and absence of episodic heart rate increases. Subsequently, persistent tachycardia followed by bradycardia and cardiac
Table 1.I.1 Heart rate, beat-to-beat (RR) interval, and number and duration of accelerations and decelerations in heart rate acquired via equine fetal ECG evaluation at various stages of gestation [3].
arrest occur as fetal decompensation occurs through the loss of central nervous system control mechanisms [3]. In one report, fetal bradycardia was recorded in an equine fetus 48 hours prior to abortion and reached a nadir of 38 beats/min at 10 minutes prior to abortion [1].
During the last 10–14 days prior to parturition, FHR remains fairly stable, although one report noted increases in FHR 5 days prior to parturition to 5 days after birth [2, 3]. Similar to other studies, the mean ± SD FHR within 24 hours of parturition was 79 ± 3 beats/min and was significantly lower than the heart rate at 48 (96 ± 3 beats/min) and 120 hours of age (102 ± 6 beats/min) in healthy neonatal foals [2]. Unfortunately, FHR and R-R interval do not allow prediction of impending parturition in the horse [3]. In a review of FHR during stage I of labor, a decrease in FHR was observed prior to rupture of the chorioallantois [27]. After rupture of the chorioallantois, 82% (37/45 fetal ECGs) of fetuses demonstrated a gradual decrease or maintenance of the same FHR, whereas 18% had an increase in FHR during stage II [1, 3, 27, 28]. Decelerations in FHR have been associated with brief periods of decreased uteroplacental blood flow during uterine contractions
References
1 Colles, C.M. and Parkes, R.D. (1978). Foetal electrocardiography in the mare. Equine Vet. J. 10: 32–37.
2 Nagel, C., Erber, R., Bergmaier, C. et al. (2012). Cortisol and progestin release, heart rate and heart rate variability in the pregnant and postpartum mare, fetus and newborn foal. Theriogenology 78: 759–767.
3 Nagel, C., Aurich, J., and Aurich, C. (2010). Determination of heart rate and heart rate variability in the equine fetus by fetomaternal electrocardiography. Theriogenology 73: 973–983.
4 Wilkins, P.A. (2003). Monitoring the pregnant mare in the ICU. Clin. Tech. Equine Pract. 2: 212–219.
5 Walton, J.R. and Peaceman, A.M. (2012). Identification, assessment and management of fetal compromise. Clin. Perinatol. 39: 753–768.
6 Martin, C.B. (2008). Normal fetal physiology and behavior, and adaptive responses with hypoxemia. Semin. Perinatol. 32: 239–242.
7 Bennet, L. and Gunn, A.J. (2009). The fetal heart rate response to hypoxia: insights from animal models. Clin. Perinatol. 36: 655–672.
8 Bennet, L., Westgate, J., Gluckman, P.D. et al. (2003). Fetal responses to asphyxia. In: Fetal and Neonatal Brain Injury: Mechanisms, Management, and the Risks of Practice, 2e (ed. D.K. Stevenson and P. Sunshine), 83–110. Cambridge: Cambridge University Press.
associated with labor in people [5]; however, this has not been directly examined in the horse. Additionally, fetal arrhythmias were detected during stage I of labor in a small number (4/39 fetuses, 10%) of fetal ECGs and included sinus arrhythmia and atrial premature contraction. One fetus with atrial premature contractions was later observed to have atrial fibrillation as a neonatal foal; however, fetal ECG could not be used to predict the presence of neonatal arrhythmias.
Beat-to-beat (R-R interval) variability is another parameter that can be measured when evaluating the fetal ECG. The R-R interval ranges from 0.5 to 4 mm in the equine fetus, with most in the range of 1 mm [4]. The R-R interval variability arises from an intact fetal central nervous system and appropriate functioning of the parasympathetic and sympathetic nervous systems. If there is an absence of variation in R-R interval, loss of the function of the fetal CNS may be present and indicates close observation. Of note, the R-R interval should be measured when the FHR is not accelerating or decelerating and the clinician should be cognizant of the fact that maternal drugs (i.e. sedation) can affect the RR interval [4].
9 Gunn, A.J., Quaedackers, J.S., Guan, J. et al. (2001). The premature fetus: not as defenseless as we thought, but still paradoxically vulnerable? Dev. Neurosci. 23: 175–189.
10 Gunn, A.J. and Bennet, L. (2008). Timing of injury in the fetus and neonate. Curr. Opin. Obstet. Gynecol. 20: 175–181.
11 Bennet, L., Peebles, D.M., Edwards, A.D. et al. (1998). The cerebral hemodynamic response to asphyxia and hypoxia in the near-term fetal sheep as measured by near infrared spectroscopy. Pediatr. Res. 44: 951–957.
12 Sameshima, H., Ikenoue, T., Ikeda, T. et al. (2004). Unselected low-risk pregnancies and the effect of continuous intrapartum fetal heart rate monitoring on umbilical blood gases and cerebral palsy. Am. J. Obstet. Gynecol. 190: 118–123.
13 Cohn, H.E., Sacks, E.J., Heymann, M.A. et al. (1974). Cardiovascular responses to hypoxemia and academia in fetal lambs. Am. J. Obstet. Gynecol. 120: 817–824.
14 Giussani, D.A., Spencer, J.A., Moore, P.J. et al. (1993). Afferent and efferent components of the cardiovascular reflex responses to acute hypoxia in term fetal sheep. J. Physiol. 461: 431–449.
15 Itskovitx, J. and Rudolph, A.M. (1982). Denervation of arterial chemoreceptors and baroreceptors in fetal lambs in utero. Am. J. Phys 242: H916–H920.
16 Baan, J., Boekkooi, P.F., Teitel, D.F. et al. (1993). Heart rate fall during acute hypoxemia: a measure of chemoreceptor response in fetal sheep. J. Dev. Physiol. 19: 105–111.
17 Fletcher, A.J., Gardner, D.S., Edwards, M. et al. (2006). Development of the ovine fetal cardiovascular defense to hypoxemia towards term. Am. J. Physiol. Heart Circ. Physiol. 291: H3023–H3034.
18 Cohn, H.E., Piasecki, G.J., and Jackson, B.T. (1980). The effect of fetal heart rate on cardiovascular function during hypoxia. Am. J. Obstet. Gynecol. 138: 1190–1199.
19 Jensen, A., Garnier, Y., and Berger, R. (1999). Dynamics of fetal circulatory responses to hypoxia and asphyxia. Eur. J. Obstet. Gynecol. Reprod. Biol. 84: 155–172.
20 Richardson, B.S., Carmichael, L., Homan, J. et al. (1993). Cerebral oxidative metabolism in fetal sheep with prolonged and graded hypoxemia. J. Dev. Physiol. 19: 77–83.
21 Hanson, M.A. (1997). Do we now understand the control of the fetal circulation? Eur. J. Obstet. Gynecol. Reprod. Biol. 75: 55–61.
22 Iwamoto, H.S., Kaufman, T., Keil, L.C. et al. (1989). Responses to acute hypoxemia in fetal sheep at 0.6–0.7 gestation. Am. J. Phys. 256 (3 Pt 2): H613–H620.
23 Matsuda, Y., Patrick, J., and Carmichael, L. (1992). Effects of sustained hypoxemia on the sheep fetus at midgestation: endocrine, cardiovascular, and biophysical responses. Am. J. Obstet. Gynecol. 167: 531–540.
24 Palmer, J.E. (2000). Fetal monitoring. Proceedings of the Equine Symposium and Annual Conference, San Antonio, TX, 39–43. http://nicuvet.com/nicuvet/Equine-Perinatoloy/ Reprints/Fetal%20monitoring%20-%20SFT.htm.
25 Knottenbelt, D.C. (2004). Risk category of the foal. In: Equine Neonatology Medicine and Surgery (ed. D.C. Knottenbelt, N. Hodstock, and J. Madigan), 29–60. Edinburgh: Sunders.
26 Steer, P.J. (2008). Has electronic fetal heart rate monitoring made a difference? Semin. Fetal Neonatal Med. 13: 2–7.
27 Yamamoto, K., Yasuda, J., and Too, K. (1992). Arrhythmias in newborn Thoroughbred foals. Equine Vet. J. 24: 169–173.
28 Too, K., Kanagawa, H., and Kawata, K. (1967). Fetal and maternal electrocardiograms during parturition in a mare. Jpn. J. Vet. Res. 15: 5–14.
Section II Fetal Circulation and Cardiorespiratory Transition
Fetal Circulation
Fetal circulation is notably different from what is present in the neonate and adult horse in order to maximize efficiency of blood flow and oxygen delivery during fetal development. Understanding fetal circulation is important to comprehending hemodynamics in utero as well as congenital diseases, but for the clinician, this knowledge is also important in the evaluation of severely ill or premature foals that fail to make the normal transition to extrauterine life. In the fetus, vascular shunts such as the ductus venosus and foramen ovale exists to deliver oxygenated blood from the placenta to the left atrium, while another shunt brings deoxygenated blood to the descending aorta (ductus arteriosus). The critical characteristic of fetal circulation is that gas exchange occurs at the placental interface and not the fetal lungs [1]. Compared to other veterinary species, the difference in partial pressure of oxygen (PO2) between the uterine vein and umbilical vein is low (0–4 mmHg), resulting in a high umbilical vein oxygen content (48–54 mmHg) [2, 3]. Likewise, the gradients for carbon dioxide (PCO2) are very low (0–1 mmHg) in the horse, reflecting the greater diffusability of CO2 compared to O2 [3]. Umbilical vein oxygenation in the equine fetus is more sensitive to changes in maternal arterial pressure of oxygen (PaO2) than in other species. This has been postulated to account for the frequent incidence of perinatal asphyxia in the foal. On the other hand, when maternal PaO2 is increased with inhaled oxygen, oxygen concentration in the umbilical vein increases more than in the uterine vein; this characteristic can be used therapeutically in fetal foals with suspected hypoxemia [2].
In other species, a portion of oxygenated blood in the umbilical vein travels to the right atrium through the ductus venosus and caudal vena cava allowing approximately 50% of blood in the umbilical vein to bypass the liver [1]. One theory in regard to the purpose of the ductus venosus
is to direct highly oxygenated blood derived from the ductus venosus in such a way that it passes preferentially through the foramen ovale, therefore allowing distribution to the upper body (heart and brain) [4]. A unique feature of the equine fetus is that this species lacks the ductus venosus [3, 5]. The cause for this is uncertain, but one theory put forth is that equine fetal arterial blood has relatively high oxygen tensions and that preferential distribution of umbilical blood contributing to enhanced supply of oxygen to the heart and brain is not necessary [4]. Regardless of the reason, oxygenated blood is preferentially shunted to the left atrium via the valve of the foramen ovale (septum primum). Blood is shunted as higher pressure in the right atrium (due to high volume venous return) keeps the valve over the foramen ovale open, thus allowing blood to flow from right to left atrium [1]. A small amount of blood from the pulmonary veins joins the blood shunted through the foramen ovale; the blood then enters the left ventricle and is ejected and into the aorta to the systemic circulation [6]. Deoxygenated blood that returns to the right atrium from the systemic circulation flows through the tricuspid valve into the right ventricle and is ejected into the pulmonary artery. Due to the high pulmonary vascular resistance of the fetal lungs, most of the right ventricular output is shunted into the descending aorta through the ductus arteriosus. A small part (10–25%) perfuses the lungs to support metabolic needs. The ductus arteriosus connects the pulmonary artery and aorta at the level of the origin of the left subclavian artery and the pulmonary artery bifurcation. For this reason, the brain, heart, and cranial portion of the body receive blood with higher oxygen content during fetal life. For this same reason, selective cyanosis of the caudal extremities is seen in neonates with a patent ductus arteriosus (PDA) and Eisenmenger syndrome. In this situation, the left-to-right shunt causes pulmonary hypertension as blood travels through the ductus arteriosus, eventually reversing the blood flow right-to-left, thereby resulting in
Cristobal Navas de Solis
301–320>320
Figure 1.II.1 Mean values of (a) arterial blood pressure and (b) heart rate from fetal ponies at different gestational ages (term ~335 days). N = 4–9 individual fetuses at each gestational age. Source: Adapted from Fowden et al. [5].
cyanosis. Further details of the physiology and clinical consequences of PDA are explained in Chapter 12. Blood in the descending aorta perfuses the abdominal organs and lower limbs of the fetus, subsequently flowing to the umbilical arteries for gas exchange and transfer of waste products in the placenta [1, 7].
Similar to other species, fetal blood pressure (BP) increases with gestational age in the equine fetus (Figure 1.II.1). The mean BP rises from 30–35 mmHg at 150 days of gestation to 80–90 mmHg at term and is associated with a decline in heart rate from 120 to 80 beats/min [5]. These changes in blood pressure and heart rate occur gradually between 150 and 300 days of gestation and then accelerate as the fetus approaches parturition, with further decreases in heart rate in the last 30 minutes before birth.
Cardiorespiratory Transition
The placenta is a low-resistance vascular bed and the fetal pulmonary circulation is a high-resistance circuit. This is one of the keys to understanding fetal circulation and the changes that occur at birth. It is important to remember, and is intuitive, that different factors can affect gas exchange in the placenta and therefore fetal wellbeing. Maternal diseases such as respiratory disease (resulting in hypoxemia), cardiac diseases (causing low cardiac output and perfusion), nutritional deficiencies, placentitis or placental insufficiency are examples. Congenital diseases, disease in the neonatal period or even cardiovascular dysfunction later in life have been linked to problems in placental circulation [1].
Transition to extrauterine circulation is driven by changes in pulmonary and systemic pressures, oxygenation of pulmonary blood, and prostaglandin metabolism.
This transition involves the closure of the aforementioned fetal shunts over the first 1 to 2 weeks of life [6]. At birth the foal is hypoxemic and hypercapnic; this stimulates the first gasping breaths. Compression of the thorax through the birth canal drives fluid out of the airway and the lungs start to inflate [8, 9]. Lung inflation causes a drop in pulmonary resistance, which consequently increases pulmonary blood flow. As pulmonary artery pressure falls below aortic pressure, blood in the pulmonary artery is directed into the lungs rather than the ductus arteriosus, as noted during fetal development. Some blood is shunted from the relatively high aortic pressure into the pulmonary artery, typically lasting 48–72 hours. The shunt created by the ductus arteriosus can often be heard in the neonate as a continuous murmur over the heart base (point of maximal intensity over the pulmonic/aortic valve or somewhat more dorsal under the triceps muscle) but a clinically relevant PDA is rare in the foal [10]. Continuous murmurs should prompt further evaluation in the presence of signs of cardiovascular or respiratory diseases, but benign neglect is acceptable in the first few days of life if the neonatal foal appears clinically healthy. The ductus arteriosus closes progressively under the influence of increased oxygen content in the blood and decreased prostaglandin concentrations. As flow though the ductus arteriosus ceases, a sharp increase in pulmonary circulation increases pulmonary venous return to the left atrium, functionally closing the foramen ovale. Pharmacological closure of selected PDAs, mainly in preterm infants, is often cited in the human literature. Briefly, non-steroidal antiinflammatory drugs (NSAIDs) or acetaminophen are given to counteract the vascular smooth muscle relaxation induced by PGE2 on vascular smooth muscle relaxation [11]. Pharmacological therapy has been shown to increase the odds of PDA closure but not change the odds
of death, necrotizing enterocolitis, or intraventricular hemorrhage, raising the question of whether this therapy necessarily improves clinical outcomes [12]. The safety, indications, dosages, or efficacy of pharmacological therapy to aid closure of PDAs in neonatal foals has not been explored.
High prostaglandin concentrations, low pulmonary oxygenation, and immaturity of the wall of the ductus arteriosus can predispose to delayed ductal closure in premature neonates. At birth the umbilical cord is severed, which blocks access of peripheral blood to the low-pressure placental bed; thus, systemic vascular resistance rapidly increases. In the majority of neonates, pulmonary vascular resistance drops below systemic vascular resistance within minutes to hours after birth and the arterial ductal shunt becomes left-to-right if the ductus arteriosus remains patent. This means pulmonary hyperperfusion and systemic hypoperfusion, but not cyanosis, are the initial consequences of a PDA [1]. In individuals with severe pulmonary overcirculation, pulmonary vascular remodeling and endothelial damage leads to pulmonary hypertension and shunt reversal (right to left shunt). This is known as Eisenmenger syndrome. Reversed PDA results in poor oxygenation as blood bypasses the lungs and polycythemia develops [13]. Hypoxemia, hypothermia, and acidosis can cause, or contribute to, increased pulmonary pressure and cause reversal to fetal circulation and right-to-left shunting by reopening the foramen ovale and ductus arteriosus. The shunting worsens hypoxemia, which furthers the pulmonary hypertension [14]. Persistent fetal circulation (also called persistent pulmonary hypertension of the newborn) is defined as postnatal persistence of right-to-left ductal or arterial shunting, or both in the presence of elevated right ventricular pressure.
Heart Rate, Rhythm, and Blood Pressure in the Newborn and Neonatal Foal
The heart rate of the healthy equine neonate is approximately 80–100 beats per minute (BPM) [15]. However, heart rate varies considerably in the first hours of life, and different reference intervals can be used for specific time points. The average fetal heart rate decreases progressively during the hour prior to birth from an average of approximately 70 BPM to approximately 60 BPM. Immediately after birth, the average heart rate suddenly increases to approximately 80 BPM, then decreases to approximately 65 BPM after 2 minutes. The heart rate then increases to normal neonatal values of 80–100 BPM over the following 10 minutes [16]. The ranges in heart rate are, however, wide, and ranges of 30–90, 60–200, and 72–133 BPM have been described in the first 1–5 minutes, 6–60 minutes, and
Table 1.II.1 Normal values of hear t rate and respiratory rate in equine neonates [20].
Age Heart rate (/min) Respiratory rate (/min) Reference
Birth 70–80Gasping to 70/min [10]
1–5 min30–90 [17]
2–30 min120–14050 [10]
6–60 min60–200 [17]
1–12 h140–15040 [10]
12–24 h110–12035 [10]
12–24 h80–12030–40 [14]
9–43 h 72–133 [17]
24–48 h90–10030 [10]
24–48 h80–100 [14]
48–72 h 60–8020 [10]
7 d 89–118 [19]
7 d 93–129 [18]
30 d 73–89 [19]
30 d 89–117 [18]
60 d 68–86 [18]
90 d 52–65 [19]
90 d 58–76 [18]
200 d 45–63 [19]
Adult 45–49 [20]
9–43 hours after birth, respectively, in Thoroughbred foals [17]. The difference in rates reported between various studies may be due to breed variation or specific situations of the examination [16–19].
Heart rate is highly dependent on the degree of excitement. It is advisable to obtain the rate when the foal is quiet or sleeping. Reported heart rates for foals in the peripartum period and during the few months of growth are reported in Table 1.II.1. The rhythm is most commonly regular [15] with the exception of the first 15 minutes of life in which there are frequent arrhythmias [21].
Blood pressure (Blood pressure = Cardiac output/ Systemic vascular resistance) is often monitored in foals as a surrogate of blood flow. It is important to note that blood pressure does not equate to blood flow or perfusion. Different BP monitors can be used in foals, but oscillometric monitors with the cuff placed over the coccygeal artery are most often used. Positioning the cuff over the metatarsal or median artery can produce analogous measurements, but with some devices this location can produce a less accurate reading [22]. The precision of these devices needs to be assessed in a device-specific manner. Table 1.II.2 provides values in growing ponies using an ultrasonic device [18].
Table 1.II.2 Noninvasive blood pressure values in growing foals.
90
Source: Adapted from Lombard et al. [18].
References
1 Finnemore, A. and Groves, A. (2015). Physiology of the fetal and transitional circulation. Semin. Fetal Neonatal Med. 20 (4): 210–216.
2 Palmer, J. (n.d.). Perinatology. New Bolton Center, University of Pennsylvania http://nicuvet.com/nicuvet/ Learn/Perinatology%20Handout.pdf.
3 Silver, M. (1984). Some aspects of equine placental exchange and foetal physiology. Equine Vet. J. 16: 227–233.
4 Barnes, R.J. (1997). Perinatal carbohydrate metabolism and the blood flow of the fetal liver. Equine Vet. J. Suppl. 24: 26–31.
5 Fowden, A.L., Giussani, D.A., and Forhead, A.J. (2020). Physiological development of the equine fetus during late gestation. Equine Vet. J. 52: 165–173.
6 Sidhu, P.S. and Lui, F. (2020). Embryology, Ductus Venosus. In: StatPearls. Treasure Island, FL: StatPearls Publishing https://www.ncbi.nlm.nih.gov/books/NBK547759/https:// www.ncbi.nlm.nih.gov/books/NBK547759.
7 Huff, T., Chaudhry, R., and Mahajan, K. (2020). Anatomy, thorax, heart ductus arteriosus. In: StatPearls. Treasure Island, FL: StatPearls Publishing https://www.ncbi.nlm. nih.gov/books/NBK470160.
9 Saadi, A., Dalir-Naghadeh, B., Hashemi Asl, S.M. et al. (2020). Right to left patent ductus arteriosus, acute bronchointerstitial pneumonia, pulmonary hypertension and cor pulmonale in a foal. Equine Vet. Educ. 9: 152–158.
10 Knottenbelt, D.C. et al. (ed.) (2004). Perinatal review. In: Equine Neonatal Medicine and Surgery E-Book: Medicine and Surgery, 1–28. Elsevier Health Sciences.
11 Bardanzellu, F., Neroni, P., Dessì, A. et al. (2017). Paracetamol in patent ductus arteriosus treatment: efficacious and safe? Biomed. Res. Int. 2017: 1438038.
12 Mitra, S., Florez, I.D., Tamayo, M.E. et al. (2018). Association of Placebo, indomethacin, ibuprofen, and acetaminophen with closure of hemodynamically significant patent ductus arteriosus in preterm infants: a systematic review and meta-analysis. JAMA 319: 1221–1238.
13 Navas De Solis, C. and Wesselowski, S. (2020). Equine congenital heart disease and respiratory disease interactions. Equine Vet. Educ. 9: 460–464.
15 Marr, C.M. (2015). The equine neonatal cardiovascular system in health and disease. Vet. Clin. North Am. Equine Pract. 31: 545–565.
16 Yamamoto, K., Yasuda, J., and Too, K. (1991). Electrocardiographic findings during parturition and blood gas tensions immediately after birth in thoroughbred foals. Jpn. J. Vet. Res. 39: 143–157.
17 Rossdale, P.D. (1993). Clinical view of disturbances in equine foetal maturation. Equine Vet. J. Suppl. 14: 3–7.
18 Lombard, C.W., Evans, M., Martin, L. et al. (1984). Blood pressure, electrocardiogram and echocardiogram measurements in the growing pony foal. Equine Vet. J. 16: 342–347.
19 Ohmura, H. and Jones, J.H. (2017). Changes in heart rate and heart rate variability as a function of age in Thoroughbred horses. J. Equine Sci. 28: 99–103.
20 Wong, D.M. and Wilkins, P.A. (2015). Defining the systemic inflammatory response syndrome in equine neonates. Vet. Clin. Equine 31: 463–481.
21 Yamamoto, K., Yasuda, J., and Too, K. (1992). Arrhythmias in newborn thoroughbred foals. Equine Vet. J. 24: 169–173.
22 Giguère, S., Knowles, H.A. Jr., Valverde, A. et al. (2005). Accuracy of indirect measurement of blood pressure in neonatal foals. J. Vet. Intern. Med. 19: 571–576.
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and handicraft on Bokharan territory that are sanctioned by the law of Sharigat. Bokharan subjects shall have a similar right to practise all such occupations on Russian territory as are sanctioned by the law of Russia.
(12) Russian subjects shall have the right to acquire gardens, cultivate lands, and own every species of real property in the Khanate. Such property shall be subject to the same land tax as Bokharan property. The same right shall be enjoyed by Bokharan subjects in the whole territory of the Russian Empire.
(13) Russian subjects shall have the right to enter Bokharan territory when furnished with permits, signed by the Russian authorities. They shall have the right of free passage throughout the Khanate, and shall enjoy the special protection of the Bokharan authorities.
(14) The Bokharan Government shall not in any case admit on to Bokharan territory any foreigners, of whatever nationality, arriving from Russian territory, unless they be furnished with special permits signed by the Russian authorities. If a criminal, being a Russian subject, takes refuge on Bokharan territory, he shall be arrested by the Bokharan authorities and delivered over to the nearest Russian authorities.
(15) In order to maintain direct and uninterrupted relations with the supreme Russian authorities in Central Asia, the Amir of Bokhara shall appoint one of his intimate counsellors to be his resident envoy and plenipotentiary at Tashkent. Such envoy shall reside at Tashkent in a house belonging to the Amir and at the expense of the latter.
(16) The Russian Government shall in like manner have the right to appoint a permanent representative at Bokhara, attached to the person of his Highness the Amir. He shall reside in a house belonging to the Russian Government and at the expense of the latter.
(17) In conformity with the desire of the Emperor of All the Russias, and in order to enhance the glory of his Imperial Majesty, his Highness the Amir Seid Mozaffur has determined as follows: The traffic in human beings, being contrary to the law which commands man to love his neighbour, is abolished for ever in the territory of Bokhara. In accordance with this resolve, the strictest injunctions shall immediately be given by the Amir to all his Begs to enforce the new law and special orders shall be sent to all the frontier towns of Bokhara to which slaves are brought for sale from neighbouring countries, that should any such slave be brought thither, they shall be taken from their owners and shall be set at liberty without loss of time.
(18) His Highness the Amir Seid Mozaffur, being sincerely desirous of strengthening and developing the amicable relations which have subsisted for five years to the benefit of Bokhara, approves and accepts for his guidance the above seventeen articles composing a treaty of friendship between Russia and Bokhara. This treaty shall consist of two copies, each copy being written in the two languages, in the Russian and in the Turki language.
In token of the confirmation of this treaty and of its acceptance for the guidance of himself and of his successors, the Amir Seid Mozaffur has affixed thereto his seal. Done at Shaar on the 10th day of October 1873, being the 19th day of the month Shayban of the year 1290.
Translations of letters[46] from A -G K , G -G T , to the A A .
T , June 1878.
To the A W A , S A K .
“Be it known to you that our relations with the British Government are of great importance to Afghanistan and its dependencies. As I am unable to see you, I have deputed my trustworthy (official) General Stolietoff to you. The General is an old friend of mine, and during the late Russo-Turkish war earned the favour of the Emperor by his spirit and bravery. He has become well known to the Emperor This trustworthy person will communicate to you what he thinks best. I hope you will pay attention to what he says, and repose as much confidence in his words as if they were my own; and that you will give your answer in this matter through him. In the meantime, be it known to you that if a friendly treaty will be of benefit to us, it will be of far greater benefit to yourself.”
Received through G S , August 9, 1878.
“Be it known to you that in these days the relations between the British Government and ours with regard to your kingdom require deep consideration. As I am unable to communicate my opinion verbally to you, I have deputed my agent, Major-General Stolietoff. This gentleman is a near friend of mine, and performed excellent services in the late Russo-Turkish war, by which he earned favour of the Emperor. The Emperor has always had a regard for him. He will inform you of all that is hidden in my mind. I hope you will pay great attention to what he says, and believe him as you would myself, and, after due consideration, you will give him your reply. Meanwhile, be it known to you that your union and friendship with the Russian Government will be beneficial to the latter, and still more so to you. The advantages of a close
alliance with the Russian Government will be permanently evident.”
G S sent the following letter, on his return to Tashkent from Kabul, to the Foreign Minister, W S M K , dated September 21, 1878:
“Thank God, I reached Tashkent safely, and at an auspicious moment paid my respect to the Viceroy (Yaroni Padishah means ‘half king’). I am trying day and night to gain our objects, and hope I shall be successful. I am starting to see the Emperor to-day, in order to inform his Majesty personally of our affairs. If God pleases, everything that is necessary will be done and affirmed. I hope that those who want to enter the gate of Kabul from the east will see that the door is closed; then, please God, they will tremble. I hope you will give my respects to his Highness the Amir. May God make his life long and increase his wealth! May you remain in good health, and know that the protection of God will arrange our affairs!
“(Signed) G S .”
From G K to the A A , dated Tashkent, October 22, 1878.
“Be it known to you that your letter, dated 12th Shawal, reached me at Tashkent on the 16th October, i.e., 3rd Zekada, and I understood its contents. I have telegraphed an abstract of your letter to the address of the Emperor, and have sent the letter itself, as also that addressed to General Stolietoff, by post to Livadia, where the Emperor now is. I am informed on good authority that the English want to come to terms with you; and, as a friend, I advise you to make peace with them if they offer it.”
From G S to W S M K , dated October 8, 1878.
“First of all, I hope you will be kind enough to give my respects to the Amir. May God make his life long and increase his wealth! I shall always remember his royal hospitality. I am busy day and night in his affairs, and, thank God, my labours have not been without result. The great Emperor is a true friend of the Amir’s and of Afghanistan, and his Majesty will do whatever he may think necessary. Of course, you have not forgotten what I told you, that the affairs of kingdoms are like a country which has many mountains, valleys, and rivers. One who sits on a high mountain can see things well. By the power and order of God, there is no empire equal to that of our great Emperor. May God make his life long! Therefore, whatever our Government advises you, you should give ear to it. I tell you the truth that our Government is wise as a serpent and harmless as a dove. There are many things which you cannot understand, but our Government understands them well. It often happens that a thing which is unpleasant at first is regarded as a blessing afterwards. Now, my kind friend, I inform you that the enemy of your famous religion wants to make peace with you through the Kaisar (Sultan) of Turkey. Therefore, you should look to your brothers who live on the other side of the river. If God stirs them up, and gives the sword of fight into their hands, then go on in the name of God (Bismilla), otherwise you should be as a serpent; make peace openly, and in secret prepare for war, and when God reveals His order to you, declare yourself. It will be well, when the Envoy of your enemy wants to enter the country, if you send an able emissary, possessing the tongue of a serpent and full of deceit, to the enemy’s country, so that he may with sweet words perplex the enemy’s mind, and induce him to give up the intention of fighting with you.
“My kind friend, I entrust you to the protection of God. May God be the protector of the Amir’s kingdom, and may trembling fall upon the limbs of your enemies! Amen.
“Write to me soon, and send the letter to the capital. Please write in Arabic characters, so that I may be able to read your letter.”
From G K to the A A , dated November 26, 1878.
“I was much pleased to receive your letter, dated 24th Zekada, 1295 (November 18, 1878), and to hear of your good health. I have also received a copy of the letter which you sent to the Governor-General. May God be pleased with you. The British Ministers have given a pledge to our Ambassador in London that they will not interfere with the independence of Afghanistan. I am directed by his Majesty the Emperor to communicate this news to you, and then, after forming friendship, to go to his Majesty. I intend to go to the Russian capital after I have arranged the affairs of this country (Turkestan). As I do not consider it advisable to keep your trusted officials, whom you are in want of, here any more, I send Mahommed Hassan Khan, Kamuah (Deputy-Governor), and Gholam Haidar Khan, with two officers, back to you. I hope you will consider me a well-wisher of your kingdom, and write to me now and then. I have given instructions that, until my return, every letter of yours which they receive at Turkestan should be forwarded to the capital. Your good fortune is a cause of happiness to me, and if any troubles come upon you, I also shall be grieved. Some presents have been sent by me through Mirza Mahommed Hassan, Kamuah; perhaps they may be accepted.”
Translation of a letter from G K to G V , dated December, 1878.
“The Amir knows perfectly well that it is impossible for me to assist him with troops in winter. Therefore, it is necessary that war should not be commenced at this unseasonable time. If the English, in spite of the Amir’s exertions to avoid the war, commence it, you must then take leave of the Amir and start for Tashkent, because your presence in Afghanistan in winter is useless. Moreover, at such a juncture as the commencement of war in Afghanistan, you ought to come here and explain the whole thing to me, so that I may communicate it to the Emperor. This will be of great benefit to Afghanistan and to Russia.”
From G K to the A A , dated December 25, 1878.
“Your letter, dated 27th Zel Hijja (November 20, 1878), has reached me. I was pleased to hear tidings of your good health. The Emperor has caused the British Government to agree to the continuance of Afghan independence. The English Ministers have promised this. I earnestly request you not to leave your kingdom. As far as possible, consider your own interests, and do not lose your independence. For the present come to terms with the British Government. If you do not want to go back to Kabul for this purpose, you can write to your son, Mahommed Yakub Khan, to make peace with the English as you may direct him. Do not leave the soil of Afghanistan at this time, because it will be of benefit to you. My words are not without truth, because your arrival in Russian territory will make things worse.”
From G K to the A A , received at Mazar-i-Sharif on January 17, 1879.
“I have received your friendly letter, dated 13th Zel Hijja (December 8, 1878). In that letter you asked me to send as many troops as could be got ready. I have written to you a letter to the effect that the Emperor, on account of your troubles, had communicated with the British Government, and that the Russian Ambassador at London had obtained a promise from the British Ministers to the effect that they would not injure the independence of Afghanistan. Perhaps you sent your letter before you got mine. Now, I have heard that you have appointed your son, Mahommed Yakub, as your Regent, and have come out of Kabul with some troops. I have received an order from the Emperor to the effect that it is impossible to assist you with troops now. I hope you will be fortunate. It all depends on the decree of God. Believe me, that the friendship which I made with you will be perpetual. It is necessary to send back General Vozgonoff and his companions. You can keep Dr. Yuralski with you if you please. No doubt the doctor will be of use to you and to your dependents. I hope our friendship will continue to be strengthened, and that intercourse will be carried on between us.”
From G K to the A S A , dated December 29, 1878.
“The Foreign Minister, General Gortchakow, has informed me by telegraph that the Emperor has directed me to trouble you to come to Tashkent for the present. I therefore communicate this news to you with great pleasure; at the same time, I may mention that I have received no instructions about your journey to St. Petersburg. My personal interview with you will increase our friendship greatly.”
Letter from M -G I , Governor of Zerafshan, to the Heir-Apparent, M M K , and others
“On the 26th of Rabi-ul-Awul, at an auspicious moment, I received your letter which you sent me, and understood its contents. I was very much pleased, and at once communicated it to General Kauffman, the Governor-General. With regard to what you wrote about the friendly relations between the Russian and Afghan Governments, and your own desire for friendship, I have the honour to state that we are also desirous of being friends. The friendship between the two Governments existed in the time of the late Amir, and I hope that it will be increased and strengthened by Amir Mahommed Yakub Khan.
“May God change the wars in your country to happiness; may peace reign in it; and may your Government be strengthened! I have been forwarding all your letters to the Governor-General, General Kauffman. May God keep you safe!
“The Zerafshan Province Governor, “M -G I .”
Written and sealed by the General.
Written on March 29, 1879.
Treaty between the Russian Government and Amir Shir Ali Khan, written from memory by Mirza Mahommed Nabbi.
(1) The Russian Government engages that the friendship of the Russian Government with the Government of Amir Shir Ali Khan, Amir of All Afghanistan, will be a permanent and perpetual one.
(2) The Russian Government engages that, as Sirdar Abdulla Khan, son of the Amir, is dead, the friendship of the Russian Government with any person whom the Amir may appoint Heir-Apparent to the throne of Afghanistan, and with the heir of the Heir-Apparent, will remain firm and perpetual.
(3) The Russian Government engages that if any foreign enemy attacks Afghanistan, and the Amir is unable to drive him out, and asks the assistance of the Russian Government, the Russian Government will repel the enemy, either by means of advice or by such other means as it may consider proper.
(4) The Amir of Afghanistan will not wage war with any foreign Power without consulting the Russian Government, and without its permission.
(5) The Amir of Afghanistan engages that he will always report in a friendly manner to the Russian Government what goes on in his kingdom.
(6) The Amir of Afghanistan will communicate every wish and important affair of his to General Kauffman, GovernorGeneral of Turkestan, and the Governor-General will be authorised by the Russian Government to fulfil the wishes of the Amir.
(7) The Russian Government engages that the Afghan merchants who may trade and sojourn in Russian territory will be safe from wrong, and that they will be allowed to carry away their profits.
(8) The Amir of Afghanistan will have the power to send his servants to Russia to learn arts and trades, and the Russian officers will treat them with consideration and respect as men of rank.
(9) (Does not remember.)
(10) I, Major-General Stolietoff Nicholas, being a trusted Agent of the Russian Government, have made the abovementioned Articles between the Russian Government and the Government of Amir Shir Ali Khan, and have put my seal to them.
Correspondence between the B and R G
Respecting the Exclusion of A from the R sphere of influence, and settling the Russo-Afghan Frontier of 1872 and 1887.
From time to time the Russian Government has given a series of assurances that whatever its action in other respects may have been, it regarded Afghanistan as entirely beyond its sphere of action.
In March 1869, the Earl of Clarendon, then Secretary of State for Foreign Affairs, informed the British Ambassador at St. Petersburg that he had received communication of a despatch addressed by the Russian Chancellor, Prince Gortchakow, to the Russian Ambassador in London, containing the following declaration:
“You may repeat to her Britannic Majesty’s Principal Secretary of State the positive assurance that his Imperial Majesty looks upon Afghanistan as completely outside the sphere within which Russia may be called upon to exercise her influence. No intervention or interference whatever, opposed to the independence of that State, enters into his intentions.”
On October 17, 1872, Earl Granville addressed to Lord Loftus, Ambassador at St. Petersburg, the following letter upon the RussoAfghan frontier.
“Her Majesty’s Government I have not yet received from the Cabinet of St. Petersburg communication of the report which General Kauffman was long since instructed to draw up on the countries south of the Oxus, which are claimed by the ruler of Afghanistan as his hereditary possessions. Her Majesty’s Government have awaited this communication in full confidence that impartial inquiries instituted by that distinguished officer would confirm the views they themselves take of this matter, and so enable the two Governments to come to a prompt and definitive decision on the question that has been so long in discussion between them. But as the
expected communication has not reached them, and as they consider it of importance, both for the maintenance of peace and tranquillity in Central Asia, and for removing all causes of misunderstanding between the Imperial Government and themselves, I will no longer delay making known, through your Excellency, to the Imperial Government the conclusion at which her Majesty’s Government have arrived, after carefully weighing all the evidence before them. In the opinion, then, of her Majesty’s Government, the right of the Amir of Kabul (Shir Ali) to the possession of the territories up to the Oxus as far down as Khoja Saleh is fully established, and they believe, and have so stated to him through the Indian Government, that he would have a right to defend these territories if invaded. On the other hand, her Majesty’s authorities in India have declared their determination to remonstrate strongly with the Amir should he evince any disposition to overstep these limits of his kingdom. Hitherto the Amir has proved most amenable to the advice offered to him by the Indian Government, and has cordially accepted the peaceful policy which they have recommended him to adopt, because the Indian Government have been able to accompany their advice with an assurance that the territorial integrity of Afghanistan would in like manner be respected by those Powers beyond his frontiers which are amenable to the influence of Russia. The policy thus happily inaugurated has produced the most beneficial results in the establishment of peace in the countries where it has long been unknown. Her Majesty’s Government believe that it is now in the power of the Russian Government, by an explicit recognition of the right of the Amir of Kabul to these territories which he now claims, which Bokhara herself admits to be his, and which all evidence as yet produced shows to be in his actual and effectual possession, to assist the British Government in perpetuating, so far as it is in human power to do so, the peace and prosperity of those regions, and in removing for ever by such means all cause of uneasiness and jealousy
between England and Russia in regard to their respective policies in Asia.
“For your Excellency’s more complete information I state the territories and boundaries which her Majesty’s Government consider as fully belonging to the Amir of Kabul, viz.:
“(1) Badakshan, with its dependent district of Wakhan, from the Sarikal (Wood’s Lake) on the east, to the junction of the Kokcha river with the Oxus (or Penjah), forming the northern boundary of this Afghan province throughout its entire extent.
“(2) Afghan Turkestan, comprising the districts of Kunduz, Khulm, and Balkh, the northern boundary of which would be the line of the Oxus from the junction of the Kokcha river to the post of the Khoja Saleh, inclusive, on the high road from Bokhara to Balkh. Nothing to be claimed by the Afghan Amir on the left bank of the Oxus below Khoja Saleh.
“(3) The internal districts of Aksha, Saripool, Maimana, Shibherfan, and Andkoi, the latter of which would be the extreme Afghan frontier possession to the north-west, the desert beyond belonging to independent tribes of Turcomans.
“(4) The western Afghan frontier between the dependencies of Herat and those of the Persian province of Khorassan is well known and need not here be defined. Your Excellency will give a copy of this despatch to the Russian Minister for Foreign Affairs.
“I am, etc., “G .”
(R )
P G to C B (communicated to E G by C B , February 5, 1873).
“S . P , “January 31, 1873.
“M. C ,—Lord Augustus Loftus has communicated to me the reply of her Britannic Majesty’s principal Secretary of State to our despatch on Central Asia of the 19th December.
“I enclose a copy of his document.
“We see with satisfaction that the English Cabinet continues to pursue in those parts the same object as ourselves, that of ensuring to them peace, and as far as possible, tranquillity. The divergence which existed in our views was with regard to the frontiers assigned to the dominions of Shir Ali. The English Cabinet includes within them Badakshan and Wakhan, which, according to our views, enjoyed a certain independence. Considering the difficulty experienced in establishing the facts in all their details in those distant parts, considering the greater facilities which the British Government possesses for collecting precise data, and, above all, considering our wish not to give to this question of detail greater importance than is due to it, we do not refuse to accept the line of boundary laid down by England. We are the more inclined to this act of courtesy as the English Government engages to use all her influence with Shir Ali in order to induce him to maintain a peaceful attitude, as well as to insist on his giving up all measures of aggression or further conquests. This influence is indisputable. It is based not only on the material and moral ascendency of England, but also on the subsidies for which Shir Ali is indebted to her. Such being the case, we see in his assurance a real guarantee for the maintenance of peace.
Your Excellency will have the goodness to make this declaration to her Britannic Majesty’s principal Secretary of State, and to give him a copy of this despatch. We are convinced that Lord Granville will perceive in it a fresh proof of the value which our august master attaches to the maintenance and consolidation of the most friendly relations with the Government of her Majesty Queen Victoria.