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Autonomic Dysfunction in Cystic Fibrosis JOURNAL OF THE ROYAL SOCIETY OF MEDICINE Supplement No. 43 Volume 96 2003 Autonomic dysfunction in cystic fibrosis AMirakhur MB MRCP MJWalshaw MD FRCP J R Soc Med 2003;96(Suppl. 43):11–17 SECTION OF PAEDIATRICS & CHILD HEALTH, 26 NOVEMBER 2002 INTRODUCTION thetic nervous system, has both pre- and postganglionic The autonomic nervous system (ANS) is a complex neural fibres. However, in general, the preganglionic fibres pass network largely responsible for the regulation of visceral uninterrupted to the organ that is to be controlled; function and maintenance of homeostasis of the internal postganglionic neurons are located in the wall of the organ.3 environment.1 This is achieved primarily through interac- The neurotransmitter for all preganglionic and para- tions with the endocrine system and via autonomic reflexes. sympathetic postganglionic fibres is acetylcholine. All The latter comprise specialized sensory receptors in the postganglionic sympathetic nerves are adrenergic except viscera which provide information regarding visceral for those fibres innervating the sweat glands which are function to higher ANS centres in the brain. At these sites cholinergic.1 sensory information is processed and integrated, and appropriate autonomic motor responses to the viscera are Higher centres relayed through the ANS efferent system. In many The supraspinal integration of ANS function is accomplished circumstances, the ANS reflexes are capable of responding by a complex interaction of many brainstem, mesencephalic very quickly to alterations in the internal environment and and cortical areas, the hypothalamus being the principal can rapidly return the system to its homeostatic baseline. higher centre for integration of ANS function. It receives sensory afferents as well as connections from the limbic GENERAL ANATOMICAL ORGANIZATION system and sensorimotor cortex, and exerts its effects via The ANS has two major divisions: the sympathetic and interactions with the endocrine system and through 2 parasympathetic nervous systems. A third division has also descending pathways to the brainstem and spinal cord. been recognized: the enteric ANS. This consists of neurons located in the wall of the gastrointestinal tract that function CLASSIFICATION OF AUTONOMIC NEUROPATHY relatively independently of the sympathetic and parasympa- Autonomic neuropathy may be primary (pure autonomic thetic systems to regulate motility and fluid and electrolyte failure, autonomic failure with multi-system atrophy, homeostasis within the gut.2 autonomic failure with Parkinson’s disease) or more commonly secondary to chronic diseases (diabetes, amyloid, Anatomy of the sympathetic nervous system chronic renal failure, chronic liver disease, nutritional disorders, malignancy).4,5 Preliminary observations suggest Sympathetic nerves originate in the spinal cord between that it also exists in cystic fibrosis (CF) (see later). segments T1 and L2 (the so-called thoracolumbar outflow), and pass from here first into the sympathetic chain, thence PATHOGENESIS OF AUTONOMIC NEUROPATHY to the tissues and organs that are stimulated by the IN CF sympathetic nerves; preganglionic fibres are short whereas the postganglionic fibres are long.1,3 Evidence that autonomic neuropathy exists in CF comes from several sources. It is known that in CF there exists a state of increased Anatomy of the parasympathetic nervous sensitivity to a-adrenergic stimulation of pupil dilatation and system increased responsiveness to cholinergic stimulation of pupil The cell bodies of the parasympathetic efferent system lie in constriction.6 In addition, the reduced cardiovascular the nuclei of cranial nerves III, VII, IX and X, and in the sensitivity to b-adrenergic stimulation in CF patients is intermediolateral cell column of the sacral spinal cord (the confirmed by a reduced leucocyte response to isoproterenol, craniosacral outflow). The parasympathetic, like the sympa- a b-receptor agonist.7 More recently, preliminary work has demonstrated the existence of autonomic neuropathy in a Adult Regional CF Unit, Cardiothoracic Centre, Thomas Drive, Liverpool L14 3PE, UK group of adult CF patients on the basis of abnormal heart 8 Correspondence to: Dr Martin Walshaw rate variability which correlates with increasing disease E-mail: [email protected] severity as determined by spirometric indices. 11 JOURNAL OF THE ROYAL SOCIETY OF MEDICINE Supplement No. 43 Volume 96 2003 Possible mechanisms for the pathogenesis of autonomic supine blood pressure, fall in blood pressure on standing neuropathy in CF are: and impaired thermoregulation; increased energy intake is associated with the opposite changes.26 Many CF patients . metabolic are malnourished, as a result of a high metabolic rate, . nutritional malabsorption, and general ill health. immunological. Vitamin E deficiency Metabolic causes Malabsorption of fat-soluble vitamins in CF may result in 27 Diabetes mellitus vitamin E deficiency. Several authors have reported that this may cause neurological deficits in this patient group.28,29 In classic diabetes, several metabolic mechanisms have been However, the presence of autonomic neuropathy was not proposed to explain the relationship between the extent and specifically investigated. Nevertheless, vitamin E is known severity of hyperglycaemia and the development of to contribute to the development of autonomic neuropathy autonomic neuropathy. For example, activation of the in non-CF patients30 and may be improved with vitamin E polyol pathway by glucose via aldose reductase which administration; certainly in diabetes vitamin E improves the results in sorbitol and fructose accumulation, myo-inositol ratio of cardiac sympathetic to parasympathetic tone as depletion and slowing of nerve conduction by alteration of assessed by analysis of heart rate variability.31 neural Na/K ATPase activity.9–12 Other mechanisms include local ischaemia resulting in lipid peroxidation of nerve membranes leading to nerve Immunological factors fibre death,13–15 decreased nitric oxide production with The identification of autoantibodies to b2-adrenergic receptors impaired endothelium dependent vasodilatation and Na/K in the serum of three patients with allergic respiratory disease ATPase activity,16 increased homocysteine levels17 and was described by Venter et al.32 These autoantibodies inhibited abnormal amino acid metabolism and protein glycation.9 adrenergic ligand binding to the receptor, providing a Approximately 20% of adult CF patients have difficulty in molecular basis for b-adrenergic hyporesponsiveness. A handling glucose, a condition labelled CF related diabetes potential role for these autoantibodies has also been mellitus.18 demonstrated in a CF patient with autonomic dysfunction.33 A positive correlation between high levels of antibodies Chronic liver disease specific for nicotinic acetylcholine receptors in autonomic Autonomic dysfunction also exists in chronic liver disease19 ganglia and the severity of autonomic dysfunction has been and is independent of aetiology.20 It is implicated in the reported in subjects with idiopathic autonomic neuro- development of portal hypertension.21 Impairment of pathy.34 A similar relationship exists between complement- axoplasmic transport, thiamine and pyridoxine deficiencies, fixing sympathetic ganglia autoantibodies and defective enhanced lipid peroxidation of nerve membranes and cardiac innervation in type I diabetes.35 circulating immune complexes are important pathogenic Antibodies against nerve growth factor have also been mechanisms.22 Chronic liver disease, in the form of identified.36 Nerve growth factor is essential for the secondary biliary cirrhosis, occurs as a sequel to altered development and maintenance of autonomic nerves.37 bile mucus in CF patients, with diffuse hepatic nodularity Deficiency of this leads to autonomic neuropathy.38 developing in only 2–5% of patients, although fatty changes are much more common.23 SYSTEMS REVIEW Uraemia Autonomic nerves innervate virtually every body system, and so the symptoms of autonomic dysfunction are quite Widespread autonomic dysfunction has been demonstrated varied. These include orthostatic hypotension, abnormal in chronic uraemic patients using a battery of six sweating, gastroparesis, impotence and bladder and bowel cardiovascular tests.24 CF patients who receive repeated dysfunction.39 The significant associated mortality and courses of nephrotoxic antibiotics may develop renal morbidity due to silent myocardial ischaemia,40 sudden disease.25 cardiac death,41 which may be related to a prolonged QT interval,42 and anaesthetic complications43 emphasize the Nutritional factors need for accurate, sensitive and specific tests of autonomic Malnutrition function. The systems which lend themselves most easily to In general, an alteration in nutritional status with examination are cardiovascular, gastrointestinal, ophthalmic subsequent reduced energy intake is accompanied by and urinary and these will now be discussed in more 12 evidence of reduced sympathetic activity and decreased detail. JOURNAL OF THE ROYAL SOCIETY OF MEDICINE Supplement No. 43 Volume 96 2003 CARDIOVASCULAR SYSTEM An alternative to this classification of severity is to give Autonomic fibres innervate the atria, ventricles, coronary each individual test a score of 0, 1, or 2, depending on arteries and resistance vessels of the peripheral circulation.44 whether it is normal, borderline or abnormal, respectively. Essentially, sympathetic activity increases heart rate and An overall
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