CirculhationFEBRUARYVOL. XXXIII

AN OFFICIAL JOURNAL of0the AMERICAN HEART ASSOCIATION

Editorial

The Preterminal Arterioles in the PulmonaryCirculation of High-Altitude Natives

NOTABLE advances in knowledge of re-

spiratory physiology and pulmonaryhemodynamics have resulted from the appli-cation of newer technics. Special attentionhas been given to the alterations producedby hypoxia in the pulmonary circulatory sys-

tem. In 1940 Von Euler and Liljestrandshowed that the pulmonary arterial pressure

in cats increased when they were maintainedin low-pressure chambers.1 Investigations per-

formed on the inhabitants in high-altituderegions of the Peruvian Andes have shownsome of the characteristics of the pulmonarycirculation and respiratory function in theseindividuals.2 4 The anatomic studies per-

formed in this field have provided the basisfor further understanding of the functionalchanges observed. Close correlation has beenfound between the hemodynamic alterationsand the histologic structural features in pul-monary vasculature.5The vascular channels designated "pre-

terminal arterioles,"6 ("capillary arterial col-laterals"7) an important component of the pul-monary vascular tree, have been assigned little

From the Department of Pathology, Facultad deMedicina, Universidad Peruana de Ciencias Medicasy Biologicas, Lima, Peru.

Supported by Grant H-7000-03, the National Insti-tutes of Health, U. S. Public Health Service.

Dr. Recavarren's present address is Department ofPathology, University of Cincinnati, Cincinnati, Ohio.

Circulation, Volume XXXIII, February 1966

functional significance. Some of the hemody-namics and oxygen blood saturation changesappearing in high-altitude natives during ex-

ercise, as well as in subjects suffering fromacute pulmonary edema at high altitude, are

better understood when the role played bythese vessels is appreciated.The "preterminal arterioles" are vessels

whose walls consist of a single elastic layerand a few subintimal smooth-muscle fibers.They do not belong to the end branchings ofthe pulmonary vascular tree. They arise fromsmall and medium-sized muscular arteries,from which they emerge at right angles andopen directly into the venous side of the al-veolar septal capillaries, forming a bypassbetween the arterial and venous circulationof the lungs (fig. 1). In some instances a

neuromuscular apparatus can be demonstrat-ed at the arterial stoma.7

These vessels carry unoxygenated blood andthey cannot participate in gaseous exchangebecause they are thick walled and are notlocated in the alveolar septal walls. Arias-Stella6 designated these vessels "preterminalarterioles," when studying the histologic char-acteristics of the lung in primary pulmonaryhypertension. Costero and associates7 verifiedthe existence of these communications in nor-

mal subjects. More recently, Heard and Reid,8using India ink injection, clearly demonstratedthe existence of the same structures.

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Figure 1

High-altitude adult native: panoramic view of a pre-terminal arteriole. The collateral channel has itsorigin in a medium-sized muscular pulmonary arterialbranch.

The physiologic role attributable to thepreterminal arterioles in the pulmonary cir-culation may be presumed from (a) thehemodynamics of the lungs in the high-alti-tude subject during exercise and (b) the fea-tures of acute high-altitude pulmonary edema.

Preterminal Arterioles and PulmonaryHemodynamics in the High-Altitude

Native during Exercise

The existence of a mild degree of pulmo-nary arterial hypertension has been clearlydemonstrated in natives at high altitudes.34Anatomic studies in these subjects have re-

vealed that the basic structural feature as-

sociated with this hemodynamic state is a

persistence of the fetal pulmonary vascularpattern.5 Another pertinent observation isthat individuals born and living at high alti-tudes exhibit arterial blood desaturation atrest.9

Cruz9 in Morococha (14,900 feet above sea

level) has shown that pulmonary arterialpressure and arterial blood desaturation in-crease significantly during exercise in relationto levels at rest. West and associates'0 andVogel and associates" have obtained similarresults.

It has been widely held that pulmonaryarteriolar constriction and increased pulmo-nary blood flow during exercise are funda-mental contributory factors in the rise of pul-

monary arterial pressure. On the other hand,several interpretations have been offered toexplain the significant increase in peripheralblood desaturation exhibited by high-altitudenatives when performing exercise. Cruz9 sug-gested that the supine position assumed bythe experimental subject causes a deficientgaseous exchange in the posterior portion ofthe lungs. West and collaborators'0 thoughtthat the permeability of the capillary alve-olar membrane underwent alteration. Vo-gel and associates," considering the reductionof the respiratory equivalent, have recentlytaken the stand that at high altitude, exerciseproduces a condition of relative hypoven-tilation.Knowledge of the vascular structure in the

"high-altitude lung" aids in interpretation ofthe results obtained from hemodynamic stud-ies performed in the exercising high-altitudesubject. The increase of arteriolar smoothmuscle5 suggests that these vessels are capableof an intense degree of contraction. Thiscould thus be a basis for the marked rise inpulmonary arterial pressure noted during ex-ercise.Two factors appear to indicate that "pre-

terminal arterioles" are involved in the pro-duction of blood desaturation in the high-altitude native performing exercise. The firstrelates to the occurrence of pulmonary ar-terial hypertension in the high-altitude subjectduring exercise, which could be a determiningfactor in the opening of a large number ofthese channels connecting the arterial andvenous side of the capillary bed. Such by-passes would greatly reduce the transit timefor gaseous exchange in venous capillaries,partially in view of the increased bloodstream velocity resulting from pulmonary ar-terial hypertension. By this mechanism a con-siderable volume of unoxygenated blood mayenter pulmonary veins and ultimately thesystemic circulation, thereby increasing thedesaturation of peripheral arterial blood. Theopening of the preterminal arterioles wouldserve as a compensatory safety valve to re-duce the pulmonary hypertension.The patency of the collateral channels may

Circulation, Volume XXXIII, Pebruary 1966

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L+ lINormal pulmonory pressure |++++| Pulmonary hypertension

i.P.A. Medium sized branch ofthe pulmonary artery

a Pulmonary orteriole

P. A. Preterminal arteriole

P. V. Pulmonary venule

Art. Cp. Arterial capillaryV.Cp. Venous capillary

Cp.Bed Capillary bed-3. Cam,PiS

Figure 2Blood pressure at branch of the pulmonary artery, preterminal arteriole and capillary bed, atrest and at exercise.

have further significance; the elevated pres-sure in the pulmonary arterial system maybe transferred unaltered into capillary net-work (fig. 2). The existence of pulmonarycapillary hypertension during exercise9 pro-vides a second point of support for our hy-pothesis. In catheterization experiments inexercising high-altitude natives, 17 of 35 sub-jects showed increases of capillary pressure,some of them registering rises of over 100 percent.

High-Altitude Pulmonary Edema andthe Preterminal Arterioles

High-altitude pulmonary edema appears inyoung people native to or residing at high al-titudes for long periods of time when theseindividuals return to high altitudes after abrief period in the lowlands.'2 HemodynamicCirculation, Volume XXXIII, February 1966

studies performed in these individuals haveshown higher pulmonary arterial pressure lev-els than in ordinary high-altitude subjects;there are increased desaturation of the periph-eral arterial blood and an apparently normalpulmonary capillary pressure.13The degree of pulmonary arteriolar mus-

cularization'2 that these patients exhibitedcorrelates closely with the level of pulmonaryhypertension that appeared during the attackof pulmonary edema.

It appears also that the hypertension issufficient to open the preterminal arteriolesand thus permit the pulmonary arterial hy-pertension to be transmitted into the exten-sive pulmonary capillary bed. The resultingincrement in capillary hydrostatic pressureand the increased capillary permeability, sec-

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ondary to hypoxia, are the fundamental fac-tors in the production of edema. It is interest-ing to note that hemodynamic measurementsindicating normal capillary pressure in peopleaffected by high-altitude pulmonary edemawere actually taken after the edema existed.It would then appear that the passage of fluidfrom the vascular space to the alveoli had al-ready occurred and, therefore, a fall in capil-lary hydrostatic pressure would be antici-pated.

SIXTO RECAVAPREN, M.D.

References1. VON EULER, U. S., AND LILJESTRAND, G.: Ob-

servations on the pulmonary arterial bloodpressure in the cat. Acta physiol. scandinav.,12: 301, 1940.

2. VELASQUEZ, T.: Maximal diffusing capacity of thelungs at high altitudes. School of AviationMedicine. USAF, Randolph Field. Report No.56-108, Nov. 1958.

3. ROTTA, A., CANEPA, A., HURTADO, A., VELAs-QUEZ, T., AND CHAVEZ, R.: Pulmonary cir-culation at sea level and at high altitudes. J.Appl. Physiol. 9: 328, 1956.

4. PENALOZA, D., SIME, F., BANCHERO, N., GAM-BOA, R., CRUZ J., AND MARTICORENA, E.:Pulmonary hypertension in healthy men bornand living at high altitudes. Am. J. Cardiol.11: 143, 1963.

5. ARIAS-STELLA, J., AND SALDANA, M.: The termi-nal portion of the pulmonary arterial tree in

people native to high altitudes. Circulation28: 915, 1963.

6. ARIAS-STELLA, J.: Hipertension pulmonar pri-maria. Segundo Congreso Latinoamericano deAnatomia-Patologica, Sao Paulo, Brasil, Seti-embre, 1958.

7. COSTERO, I., BARROSO, MONGUEL, R., CONTRERAS,R., CHAvEz, A., MONROY, G., AND Qumoz, A.:Colaterales vasculares del pulmon. Rev. Lat.Amer. de Anat. Pat. 4: 5, 1960.

8. HEARD, B. E., AND REID, A.: Preliminary Studiesof the Pulmonary Capillaries by India Ink In-jection. Fifth Annual Conference on Researchin Emphysema. Aspen, Colorado, June 13-16,1962.

9. CRTUZ, J.: Efecto del ejercicio sobre el corazon yla circulacion pulmonar en el nativo de lasgrandes alturas. Thesis de Bachiller, Fac. Med.Lima, Peru, 1963.

10. WEsT, J. B., LAHIRI, S., GILL, M. B., MILL-EDGE, J. S., PUGH, C. G. C. E., AND WARD,M. P.: Arterial oxygen saturation during ex-ercise at high altitude. J. Appl. Physiol. 17:617, 1962.

11. VOGEL, J. H. K., WEAVER, W. F., ROSE, R. L.,BLOUNT, S. G., JR., AND GROVER, R. F.: Pul-monary hypertension on exertion in normalman living at 10,150 feet (Leadville, Colo-rado). Medicine Thoracalis 19 (5), 1963.

12. ARIAS-STELLA, J., AND KRUGER, H.: Pathologyof high altitude pulmonary edema. Arch.Path. 76: 43, 1963.

13. HULTGREN, H. N., LOPEZ, C., LUNDBERG, E.,AND MILLER, H.: Physiologic studies of pul-monary edema at high altitude. Circulation29: 393, 1964.

Servetus and the Lesser CirculationThe most important physiological contributions of Michael Servetus are these:

first, the passage of blood through the lungs, its mixing there with air, and its changein color; second, his emphasis on the size of the pulmonary artery, from which he de-duced that it must serve some purpose other than transporting blood for the nourishmentof the lungs; and third, his twice-repeated statement that there is no communicationallowing blood to move through the interventricular septum.-ANDRE' COURNAND, M.D.Circulation of the Blood. Edited by Alfred P. Fishman, M.D., and Dickinson W. Rich-ards, M.D. New York, Oxford University Press, 1964, p. 23.

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SIXTO RECAVARRENNatives

The Preterminal Arterioles in the Pulmonary Circulation of High-Altitude

Print ISSN: 0009-7322. Online ISSN: 1524-4539 Copyright © 1966 American Heart Association, Inc. All rights reserved.

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