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Ultrastructure of the Lung in Chronic Hypoxia Thorax: First Published As 10.1136/Thx.49.Suppl.S27 on 1 September 1994

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Ultrastructure of the Lung in Chronic Hypoxia Thorax: First Published As 10.1136/Thx.49.Suppl.S27 on 1 September 1994 Thorax 1994;49 Supplement:S27-S32 S27 Ultrastructure of the lung in chronic hypoxia Thorax: first published as 10.1136/thx.49.Suppl.S27 on 1 September 1994. Downloaded from Paul Smith The most striking changes in the lungs in re- nations were the direct result of vasoconstrict- sponse to prolonged alveolar hypoxia occur in ion rather than the toxic effects of fulvine was the small pulmonary arteries and arterioles. shown by injecting normal rats with histamine. The influence ofchronic hypoxia on these small The immediate vasoconstriction which resulted vessels has been subjected to extensive physio- was also associated with numerous evaginations logical investigation and to pathological ex- of membranes of smooth muscle cells.2 This amination by light and electron microscopy. early report led to further investigations so that The lung parenchyma, too, may be modified, large pale evaginations of smooth muscle were but usually in response to brief severe hypoxia found to be common in the pulmonary veins as in acute decompression or high altitude of rats given monocrotaline, an alkaloid related pulmonary oedema. Chronic hypoxia induces to fulvine,3 and in pulmonary veins, arteries, subtle changes in the lung parenchyma - for and muscularised arterioles in rats subjected to example, it has been found that the thickness prolonged hypoxia.4 The latter paper was of of the alveolar capillary membrane of guinea particular interest because it showed for the pigs living at high altitude is significantly re- first time that hypoxia can induce constriction duced compared with animals living at sea of pulmonary veins as well as arteries. Hypoxia level.' This change is so subtle, however, as also promotes the formation of evaginations in to require complex morphometry of electron the pulmonary trunk of rats where they appear micrographs in order to demonstrate it. This as large "islands" of cytoplasm, with few or- review concentrates upon ultrastructural ganelles, situated beneath the endothelium.5 changes in the pulmonary arteries and ar- Fortuitous sections reveal that many of these terioles, since remodelling of these vessels by apparent "islands" are connected to smooth hypoxia is readily appreciated by qualitative muscle in the media by a narrow neck passing study and is of considerable practical import- through gaps in the internal elastic lamina. ance. Evagination ofsmooth muscle is not confined to the pulmonary circulation but has been de- scribed in the aorta of hypoxic rabbits6 and Pulmonary vasoconstriction in intestinal smooth muscle.7 Fay and Delise8 http://thorax.bmj.com/ Hypoxia is a potent constrictor of the pul- studied the morphological alterations in iso- monary vasculature but the existence of such lated smooth muscle cells from the stomach of vasoconstriction is difficult to prove by histo- Bufo marinus by scanning and transmission logical criteria. A highly crenated appearance electron microscopy. They found that in the of elastic laminae in small pulmonary arteries relaxed cell the surface was smooth and the is suggestive of constriction, but the same fold- myofilaments orientated longitudinally. On ing of the laminae may occur during collapse contraction the cell surface became covered of the lung whilst it is being processed for with bulbous prominences and the myo- on September 28, 2021 by guest. Protected copyright. histological examination or electron micro- filaments assumed a more random orientation. scopy. A specific marker for vasoconstriction These evaginations of the cell membrane oc- of the pulmonary vasculature can be seen at curred between adjacent dark attachment the ultrastructural level and was first described points for myofilaments on the cell surface. in rats given fulvine.' Fulvine is a pyrrolizidine They concluded that when the myofilaments alkaloid which produces severe pulmonary contract they exert an inwardly directed force arterial hypertension in rats associated with which squeezes out the clear cytoplasm be- advanced pulmonary vascular disease. Electron tween the attachment points to form numerous microscopy of small pulmonary blood vessels balloon-like prominences. from these rats revealed the presence of large, Although muscular evaginations are com- bulbous evaginations of the outer membrane mon in rats they are not seen in any form of vascular smooth muscle cells. They were of hypertensive pulmonary vascular disease in particularly numerous in pulmonary veins humans described so far.910 This difference where the evaginations frequently herniated between rats and humans may simply reflect through the endothelial basal lamina displacing species differences. It is possible, however, that the endothelial cells into the lumen.2 the pulmonary arteries of humans constrict to Muscular evaginations were also found in small a lesser extent than those of the rat. A major pulmonary arteries, but in this class of vessel component of the increased pulmonary vas- they were largely confined to the adventitial cular resistance associated with plexogenic pul- border, herniating through gaps in the external monary arteriopathy is therefore due to vascular elastic lamina. Presumably the almost con- occlusion by myofibroblasts rather than to vaso- Department of constriction.91' 12 Furthermore, chronic hyp- Pathology, University tinuous internal elastic lamina of the rat pul- of Liverpool, Liverpool monary artery prevented muscular evaginations oxia in humans is associated with a modest L69 3BX, UK from passing through it. That these evagi- increase in pulmonary arterial blood pressure P Smith with mean values at rest of 29 mm Hg in natives S28 Smith of Morococha at an altitude of 4540 m.'3 This most smooth muscle cells have this immature is in sharp contrast to a right ventricular mean appearance, but the quantity of myofilaments Thorax: first published as 10.1136/thx.49.Suppl.S27 on 1 September 1994. Downloaded from pressure of 30-55 mm Hg recorded in rats sub- has increased. In addition, small clumps of jected to a pressure of 380 mm Hg in a de- elastin are deposited in the endothelial basal compression chamber for 4-5 weeks.'4 lamina. Between three and five weeks there is a progressive increase in the proportion of the cytoplasm of smooth muscle cells occupied by Muscularisation of pulmonary arterioles myofilaments with a corresponding reduction Animal species which are indigenous to high in secretory organelles. These cells now re- altitude, such as the llama, alpaca, mountain semble mature smooth muscle. They are also viscacha, and the yak, show no changes in their encountered more frequently, suggesting either heart or pulmonary blood vessels in response that new muscle has migrated from proximal to the hypobaric hypoxia oftheir environment. 15 vessels or that existing cells have undergone They are considered to be genetically adapted division. By five weeks there is an almost con- to life at high altitude. Animals which ac- tinuous layer of elastin beneath the endo- climatise to hypoxia have been little studied at thelium forming a new internal elastic lamina. natural high altitude except for the cow which The origin of the new smooth muscle in responds with intense vasoconstriction and hy- muscularised arterioles is far from certain. Elec- pertrophy ofits pulmonary arterioles.'5 Instead, tron microscopy of normal arterioles reveals common laboratory animals such as rats and that they contain sparsely distributed, highly rabbits have mostly been studied in hypoxic attenuated smooth muscle cells immediately chambers simulating altitudes as high as beneath the endothelium.2" These cells have 5500 m. This extreme hypoxia leads to severe also been referred to as pericytes and in- pulmonary arterial hypertension, right vent- termediate cells24 but, whatever one cares to ricular hypertrophy, and pronounced mus- call them, they have a muscular pedigree and cularisation of pulmonary arterioles.'4 1"17 presumably hypertrophy to form the immature Humans, too, have to acclimatise to high al- smooth muscle during the first two weeks of titude and commonly showhypoxic remodelling hypoxia. It is likely that they can also divide of the pulmonary vasculature. Arias-Stella and since mitotic figures in pulmonary arterioles Saldaia'8 were the first to note that pulmonary have been reported after 7-10 days ofhypoxia,24 arterioles consisted ofa thick media ofcircularly and there is uptake of tritiated thymidine by orientated smooth muscle sandwiched between the newly formed smooth muscle.25 two elastic laminae in Quechua Indians from At the light microscopical level muscularised Cerro de Pasco at an altitude of 4330 m in the arterioles have a similar appearance irrespective Peruvian Andes. This observation was later of whether they have been induced by hypoxia confirmed in Aymara Indians and mestizos or other agents. It is generally assumed, there- from La Paz at an average altitude of 3800 m, fore, that there is but a single type of mus- http://thorax.bmj.com/ although only a proportion of them showed cularised arteriole. This assumption was tested muscularised arterioles. 1 20 Pulmonary vascular recently by comparing the ultrastructure of remodelling in citizens of La Paz may also these vessels in rats which had been hypoxic involve the development oflongitudinal muscle from birth with those from young rats given in the intima of small pulmonary arteries and the pyrrolizidine alkaloid monocrotaline.26 arterioles and occasionally the formation of Both groups of animals showed extensive mus- muscular tubes.20 Similar
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