Survey of Veterinarians Using a Novel Physical Compression Squeeze Procedure in the Management of Neonatal Maladjustment Syndrome in Foals

Abstract

Horses are a precocious species that must accomplish several milestones that are critical to survival in the immediate post-birth period for their survival. One essential milestone is the successful transition from the intrauterine unconsciousness to an extrauterine state of consciousness or awareness. This transition involves a complex withdrawal of consciousness inhibitors and an increase in neuroactivating factors that support awareness. This process involves neuroactive hormones as well as inputs related to factors such as cold, visual, olfactory, and auditory stimuli. One factor not previously considered in this birth transition is a yet unreported direct neural reflex response to labor-induced physical compression of the fetus in the birth canal (squeezing). Neonatal maladjustment syndrome (NMS) is a disorder of the newborn foal characterized by altered behavior, low affinity for the mare, poor awareness of the environment, failure to bond to the mother, abnormal sucking, and other neurologically-based abnormalities. This syndrome has been associated with altered events during birth, and was believed to be caused exclusively by hypoxia and ischemia. However, recent findings revealed an association of the NMS syndrome with the persistence of high concentrations of in utero neuromodulating hormones (neurosteroids) in the postnatal period. Anecdotal evidence demonstrated that a novel physical compression (squeeze) method that applies 20 min of sustained pressure to the thorax of some neonatal foals with this syndrome might rapidly hasten recovery. This survey provides information about outcomes and time frames to recovery comparing neonatal foals that were given this squeeze treatment to foals treated with routine medical therapy alone. Results revealed that the squeeze procedure, when applied for 20 min, resulted in a faster full recovery of some foals diagnosed with NMS. The adjunctive use of a non-invasive squeeze method may improve animal welfare by hastening recovery and foal-mare interactions that minimize health problems. This would also avoid or reduce costs arising from hospitalization associated with veterinary and nursing care that sometimes leads owners to elect for euthanasia.

Keywords: birth; consciousness; equine; hypoxia; neurosteroids; perinatal; survey.

Figure 1

Neonatal foal being received and evaluated in an intensive care referral veterinary hospital. NMS foals may need a controlled environment with minimal pathogens and ideal temperature, often with accommodations for the mare nearby. The mare may need to be milked and the foal tube fed frequently when the foal lacks a suck reflex. Continuous care and observation by trained personnel may be required, including intravenous fluid and medication administration. Critical care facilities have access to laboratory measurements required for direct supportive care. Recumbent foals may require physical therapy and body position support. Methods that can be used in the field setting that result in the foal more rapidly sucking the mare may prevent secondary complication and the need for referral to critical care facilities.

Figure 2

Illustration of the proposed influences associated with the transition of consciousness from intrauterine to extrauterine life. While in utero, the fetal foal remains in a sleep-like state of consciousness, which acts to protect the mare from movements of long limbs of foals weighing 80–120 lbs (37.2–54.4 kg) at birth. This neuroinhibited state is maintained in mammals through high circulating and cerebral concentrations of adenosine, progesterone and its related neuroactive steroids allopregnanolone and pregnanolone, as well as prostaglandin D2 and a placental neuroinhibitory peptide, all acting together with warmth, buoyancy, and cushioned tactile stimulation [2,3,4,5,6]. At the onset of stage-1 labor the fetus comes under the stimulation of 17β-estradiol, which continues through stages 2 and 3 affecting the locus coeruleus. The locus coeruleus produces large amounts of norepinephrine, which causes the transition to consciousness at birth. During stage-2 labor, the arousal stimulation is overridden by thoracic pressure that induces squeeze-induced somnolence and immobility while in the narrow birth canal. When the fetus exits the birth canal, the squeeze pressure is released and full stimulation from the priming of 17β-estradiol occurs. The foal transitions to full consciousness and mobility shortly after delivery, which is essential for survival as a prey animal.

Figure 3

Illustration of the factors associated with the squeeze induced transition of consciousness in a foal with neonatal maladjustment syndrome. A persistent elevation of neurosteroids is observed in foals 24 h post-birth [12]. When the foal is subject to the 20-min squeeze procedure, a reflex neuroinhibition occurs with onset of somnolence; slow wave sleep; immobilization; and reduction in pain, body temperature, and heart rate [15]. Endocrine changes occurring during the squeeze include increased ACTH, androstenedione, and DHEA [15]. Release of the squeeze pressure produces arousal and transition to normal consciousness in some foals with onset of sucking the mare. In other mammals, onset of consciousness is associated with 17β-estradiol stimulation, which affects the locus coeruleus that, in turn, produces large amounts of norepinephrine, creating the transition to consciousness at birth [2,3,4,5,6].

Figure 4

Illustration of the proposed influences associated with states of consciousness, physiological functions, and physical factors affecting the fetal foal in utero, stage 2 labor, and immediately post-birth. In utero, neuroinhibitory factors cause inhibition of movement and consciousness. At this stage, the fetus receives oxygen and nutrition from the placenta, and organs such as the gut and lungs are quiescent. During stage 2 labor, birth canal pressure produces immobility and further neuroinhibition associated with mild hypoxemia and hypercapnia. Immediately upon exiting the birth canal, thoracic squeeze pressure is reduced, releasing neuroinhibition. Physical factors such as skin sensation, olfactory, auditory, and visual stimuli contribute to arousal, ultimately leading to bonding with the mare.

Figure 5

Synthesis and pathways of neurosteroids in the brain [27]. Neurosteroids can have potent effects on both neurodevelopment and consciousness [12]. Progesterone and its related derivatives have been reported to affect gene transcription important for neurodevelopment. Additionally, progesterone and deoxycorticosterone serve as precursors for the endogenous neurosteroid allopregnanolone, which acts on the GABA receptor to rapidly alter consciousness. Levels of neurosteroids in the blood, central nervous system, and spinal fluid are distinct, and may be influenced by levels of precursor steroids shown here. Elevated blood levels of progesterone, pregnenolone, androstenedione, dehydroepiandrosterone, and epitestosterone have been reported in foals with NMS, and are possibly associated with behavioral and conscious state alterations [12].