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Carotid Bodies in Animal Models of Human Disease: What Do They Teach Us? S15

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Carotid Bodies in Animal Models of Human Disease: What Do They Teach Us? S15 S14 Thorax 1994;49 Supplement:S14-S18 Carotid bodies in animal models of human Thorax: first published as 10.1136/thx.49.Suppl.S14 on 1 September 1994. Downloaded from disease: what do they teach us? Gwenda Barer Animals suffer their own diseases and rarely Hypoxic carotid body in man and animal afford us accurate pictures ofhuman afflictions. "models": morphology and physiology The argument is cogent that we can only learn In 1970 Heath and colleagues published a about human problems through the study of paper describing the carotid bodies in 40 con- humans. However, had we never investigated secutive necropsies. The weight of the carotid animals there are things we certainly would body was high in patients with emphysema, never have known. I contend that we would Pickwickian syndrome, and cor pulmonale, and not have discovered the respiratory function of a significant correlation was observed between the carotid body. In anaesthetised animals we the combined weights ofthe carotid bodies and can humanely cut and record from nerves, the weight of both the right and, unexpectedly, change gas tensions, give drugs and poisons. the left ventricle.3 In 1971 a further paper Animals can be exposed to environments which confirmed these findings.4 affect humans under controlled conditions, and In the following years the Liverpool group then compared with normal animals of similar produced a series of fascinating papers on rats age, sex, and life experience. Then there is the exposed chronically to hypoxia in a hypobaric morphological problem. Animal tissues can be chamber. They showed that the carotid body taken at the moment of death or before, so that enlarged rapidly, developed vascular en- the autolytic problems which beset pathologists gorgement and cellular changes at both the do not hold. All these points apply to research light and electron microscopic levels, and re- on the carotid body, to the interaction between turned to normal rapidly in air.5 Others con- physiologists and pathologists, and the argu- firmed these findings. In collaboration with ments between them. Much has been learnt Dr Edwards from the Liverpool group our from the efforts of these two groups but few Sheffield team showed similar morphological problems are wholly settled; the disputes be- changes in rats kept in both hypobaric and tween different disciplines often point the way normobaric hypoxic chambers.6 In Prague forward to further research. In talking about Herget, in collaboration with us, found http://thorax.bmj.com/ "models" we should consider how far they enlargement of the carotid body in rats with reproduce both morphological and functional experimental silicosis and emphysema, the size features of human conditions. being proportional to the degree of hypoxia in life.7 In Sheffield we found functional changes attributable to the carotid body in our chron- ically hypoxic rats.' When removed from the chamber and given low oxygen mixtures to Historical breathe they increased their ventilation to a Study of the human carotid body gathered lesser degree than normal rats (figure). This on September 27, 2021 by guest. Protected copyright. impetus when Arias-Stella found that it was excited us because high altitude dwellers in unusually large in people in the high Andes both the Andes and the Himalayas have a who had lived all their lives in an hypoxic en- "blunted" ventilatory response to hypoxia, as vironment.' At this time Professor Heath was do children hypoxic from congenital heart dis- studying patients with chronic bronchitis and ease. The "blunting" in rats lasted only a few emphysema who were hypoxic because they days into recovery in air, but the finding has could not take in sufficient air. He found been repeated many times. About this time it changes in their pulmonary vessels similar to was shown by the group in Denver, Colorado those found in high altitude dwellers. He began that non-native residents at high altitude de- to look at their carotid bodies and found them velop "blunting" after about 12 years' res- also to be abnormally large. In Sheffield we idence.8 More recently the Denver group have were studying rats and mice made hypoxic in shown that "blunting" in women living at high a hypobaric chamber and had sent Professor altitudes in Peru is "reversible" in that a brisk Heath some slides of their lungs. He replied ventilatory response to hypoxia returns to with enthusiasm that their small lung vessels these normally blunted individuals during resembled those of his bronchitic patients. At pregnancy.9 Thus blunting may be switched on a meeting of the Pathological Society in and off. Flenley and colleagues showed that a Sheffield in 1970 he gave a paper on human proportion of patients with chronic hypoxic carotid bodies and we gave one on pulmonary lung disease have a poor ventilatory response vessels in our hypoxic mice.2 We met and both to hypoxia.'0 To this point human and animal Department of decided to look at carotid bodies in animals studies concurred, but more detailed mor- Medicine, Royal in a low oxygen environment - in "animal phological investigations led to a divergence. Hallamshire Hospital, kept Sheffield S10 2JF, UK models of hypoxic lung disease". Thus began In rats chronically exposed to hypoxia with G Barer a long friendship and collaboration. or without hypercapnia morphometric analysis Carotid bodies in animal models of human disease: what do they teach us? S15 175- A - Normoxic appearance was found by Habeck in some of + zC} Chronically hypoxic his hypoxic patients.15 The question was raised Thorax: first published as 10.1136/thx.49.Suppl.S14 on 1 September 1994. Downloaded from E 150 as to whether this appearance was related to the advanced age ofmany ofthe patients compared E 125 with the youth of the rats. A study of changes + + in the human carotid body with age showed 0o 100 _ + that this was not so, although sustentacular r- > became more common as life ad- w <+ proliferation 75 + + vanced.'6 Nonetheless one cannot compare the + carotid body of a human coming to necropsy 50 after a lifetime of repeated illnesses and 2 5 5 0 7 5 10 0 12 5 15.0 17 5 20 0 experiences with that of a rat dying after Pao2 (kPa) a sheltered healthy life and brief hypoxic This is unresolved. 125 B 4111~- Normotensive exposure. problem 12-+ Hypertensive Do chronically hypoxic rats, therefore, more 100 O closely resemble high altitude dwellers than .E ++ hypoxic patients? This may be so. Arias-Stella + + and found that the carotid body of 757 Valcarcel'7 0 + Quechua Indians contained larger and more C,) 50 e i numerous lobules than that of plain dwellers, 0 i0 due to proliferation of "chief cells" with thin uw 25 intervening fibrous tissue. Recently Professor Heath's group have looked at carotid bodies of 0 four high altitude dwellers from Ladhak in the 2 5 5 0 7 5 10 0 12 5 15-0 17 5 20.0 Karacorams.'8 The carotid body was ab- Pao2 (kPa) normally heavy in the two oldest subjects. In Re lation between ventilationIlOOg body weight and three cases there were numerous clusters of arterial Po2. Values are means (SE.) (A) Chronically chief cells with many of the "dark" variety, hylpoxic rats increase ventilation less than control rats with which have been found both in young and old increasing hypoxia. (B) Hypertensive rats ventilate more thcin normotensive rats over a wide range of Po2 but the cases of hypoxaemia. Only a 52 year old man increase in ventilation with increasing hypoxia is similar. had sustentacular cell proliferation. We must Dcita derived from refs 21 and 29. look at rats after repeated or very long hypoxic exposures to see if they develop sustentacular hyperplasia. It may eventually be proved, how- showed that the enlargement of the carotid ever, that rats and humans are fundamentally bc,dy was partly due to vascular engorgement different. but also to proliferation of type 1 (often called http://thorax.bmj.com/ chief) cells and connective tissue cells; there was also angiogenesis." The dense-cored ves- Biochemical changes in the hypoxic icles in type 1 cells, which contain dopamine, carotid body: functional consequences were changed morphologically and the number In the 1970s and 1980s electrochemical ana- per carotid body was greatly increased. The lyses showed that the catecholamine content of proliferation of type 1 cells was at first disputed the carotid body in rats altered during hypoxia. since they were thought to be neural in origin; During chronic hypoxia the noradrenaline and hyperplasia was proved conclusively when mi- dopamine contents increased dramatically, on September 27, 2021 by guest. Protected copyright. toses were found after arrest of cell division and returned slowly to normal during recov- with vincristine.'2 Autoradiographs taken after ery in air.'9 The turnover of dopamine also administration of tritiated thymidine showed increased.20 Dopamine inhibits the response of numerous cell divisions 1-4 days into hypoxic the carotid body to hypoxia; it diminishes both exposure.13 No change was detected in the type the frequency of impulses travelling up the 2 cells which normally envelop the nests of type carotid nerve and the subsequent increase in 1 cells. The carotid body therefore appeared to ventilation. We wondered ifthe "blunting" seen be hyperplastic and active as one might expect in our rats could be due to the high content of under chronic stimulation. dopamine in their carotid bodies. We found, By contrast, in the enlarged carotid body indeed, that a dopamine inhibitor, dom- of patients
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