ANNALS OF HUMAN BIOLOCÍY, 1981, YOL. 8, NO. 6, 573-578

High-altitude haematology: Quechua-Aymara comparisons J . A R N A U D , J . C . Q U I L I C I a n d G . R I V I É R E

Centre cfHémotypologie du C.N.R.S., C.H.U. de Purpan, Toulouse, France and Instituto Boliviano de Biología de Altura, La Paz, Bolivia

Received 6 January 1981; revised 2 July 1981

Summary. Haematological studies have been carried out at various altitudes between 450 m and 4800m, on two separate human groups(Quechuas and Aymaras) living in South America. Changes in the haematological parameters do not develop linearly in relation to the altitude. The impact of chronic hypoxia on erythropoiesis is greater above 3000 m. The haemogram varies quantitatively and not qualitatively (mean corpuscular volume and mean haemoglobin concentration remain constant). The haematological study also reveáis the greater adapt-ability to high altitude of the Aymaras, an adaptability characterized by an increase in red cell count and concentration and a decrease in red cell volume. The adaptative phenomena observed in the Quechuas are reversible, whereas they persist in the Aymaras when they migrate to the lowlands (450m).

1. Introducíion Chronic hypoxia due to altitude requires a biological and individual reaction from

man, since culture does not provide him with any eííicient response to variations in ecological parameters (Bernard and Ruffié 1966, Ruffié, Quilici and Lacoste 1977; Baker 1978). Tens of millions of human beings, however, live permanently at altitudes of over 3000 m. In the biological response to high altitude, the part played by blood in the carriage of respiratory gases is crucial.

A haematological study at various altitudes between 450 and 4800 m has been carried out in Bolivia on 1885 persons of known ethnic origin (Quechuas and Aymaras) with two objects in view (a) the assessment of the adaptat ive capacity of man in response to the increasing high-altitude chronic hypoxia and (b) investigation of a possible biological diíTerentiation between the two ethnic groups. The study was part of a large haemotypological, medical and biological investigation, one object of which was to determine the influence of voluntary or controlled migrations on the Amerindian populat ions in Bolivia (Sebbag 1978).

2. Materials and methods Each blood donor was given a full medical examination including a parasitological

study in order to exelude subjeets in poor health, and an ethnological and genealogical investigation which involved obtaining information from the subjeets and checking their answers by referring to the local archives and the local authorities.

The medical and ethnological investigations were intended to select the subjeets so as to obtain samples as representative as possible of two healthy populat ions living at diíTerent altitudes (the Quechuas and the Aymaras). The mean age 29 ± 11 yearsand the distribution according to the sexes, all altitudes combined, was men 64% and women 36%. The donors had been residing for at least five years in or about the localities where the blood samples were taken.

We performed the following determinations on heparinized fresh venous blood taken from the median cubital vein: (i) the haematocrit (Ht) determined by a

<001 4460 XI 0X06 0571 02 00 < I9N1 Taslor & \ ra neis 1 tet

574 J. Arncnul e t a l .

micromethod; (ii) haemoglobin (Hb) determined by Drabkin's technique, expresscd in g/ml of whole blood and in ¿/mol/ml of RBC (taking 64458 as the haemoglobin molecular weight; Bursaux, Dubos and Poyart 1971); and (iii) the red blood cell count by dilution in BD unopettes, counting in Thomas's haematimetric cell and expressed as 10 6 red blood cells per m m 3 of whole blood. From these data we calculated the mean corpuscular volume (MCV) expressed in fx3 and the mean haemoglobin concentration of the red blood cells (MHC) expressed as percentage of the total volume.

The statistical study was carried out by means of Student's f-test for large samples (n > 30 and the degree of freedom: nx + n2 - 2 > 120).

3. Results All the results are presented in table 1 and show an obvious increase of the

haemogram with altitude. The Ht, Hb and RBC valúes plotted in figure 1 clearly show that in the Quechuas the haematological valúes increase as the altitude gets higher. Up to 2700 m the curve rises slowly (0-55% per 100 m), but over that height it gets significantly steeper (113% per 100 m between 2700 and 3600 m and 2-19% per 100 m between 3600 and 4800 m). The valúes for the Aymaras, also indicated in figure 1, are situated above the curves.

Table 1 also shows a quantitative and not qualitative modification of the volume and the haemoglobin contení of the red cells. Whatever the altitude, the MCV, the M H C and the Ht (expressed in /imol/ml RBC) valúes remain constant for the same ethnic group.

At high altitude (3600 m) and in comparison with the Quechuas, the Aymaras ha ve a very significantly higher number of red cells which, however, are significantly smaller and carry more haemoglobin (figure 2). At high altitude, the observed diííerence between the groups is then of both quantitative order (Ht and R BC) and of a qualitative order (MCV and MHC). The diíTerence appears principally in a much higher haemoglobin concentration in the Aymaras (5-45 /¿mol/ml R BC) than in the Quechuas (4-82//mol/ml RBC) (table 1).

Table 1. Variation of haematological data according to altitude, in Quechuas and Aymaras.

Quechuas Aymaras Altitude (m) 450 2700 3100 3600 4800 450 3600

N 127 89 144 452 190 163 720 Ht (%) X 421 47-3 46-9 50-5 63-8 41-6 52-0

S.D. 4-5 3-7 3-8 4-7 9-5 3-6 3-5 Hb (g/100mi WB) X 13-2 14-4 14 2 15-8 19-7 14-8 18 2

S.D. 2-1 1-2 1-3 1-5 2-5 1-3 1-1 R B C (10 6 m m 3 ) X 4-260 4-818 4-820 5163 6-572 4-398 5-721

S.D. 0-498 0-628 0-430 0-527 0-909 0-421 0-387 M C V (// 3) 98-8 98-2 97-2 97-8 97-0 94-6 90-9 M H C í° n ) 314 30-4 30-4 31-3 30-9 35-6 35-0 Hb (/¿mol/ml RBC) 4-86 4-72 4-70 4-85 4-79 5-52 5-43

Abbreviations: W.B., whole blood; Ht, haematocrit; Hb. haemoglobin; RBC, red blood cells; MCV. mean corpuscular volume; MHC, mean haemoglobin concentration; Metí Ib, met haemoglobin.

High-altitude haematology 575

0 4 5 0 2700 3100 3600 4800 ALTITUOT »MI

Figure 1. Haematological data according to the altitude.

Ht(%>

Hb (9/100 MI WB}

RBC (10%.m')

MCV (m3)

MHC [%)

Hb (pM/mlRBc)

N

^ = NON SIGNIFICAN! y ~ SIGNIFICAN! &\>P >0.1*

RVERY SIGNIFICANT P<0.1'

igure 2. Anthropobiological study. A comparison of haematological parameters in Aymaras with the Quechuas as a reference group.

576 J. Armuci e t a l .

4. Discussion High-altitmle Iwematology

It has been known for a long time that a moderate adaptat ive polycythaemia appears in chronic high altitude hypoxia (Monge 1930); so far, however, most studies have dealt more with acclimatization than with the adapta t ion mechanisms.

Our results do not agree with those of Moulin (1971), who noted a linear variation of the haemogram according to the altitude in the Quechuas . We obtain a curve with a slope that gets steeper as the altitude increases. There seems to be, at about 3000 m, a critical threshold between médium and high altitude (mean barometric pressure 525 mm Hg; mean partial oxygen pre£?ure: l l O m m Hg).

Under the conditions of médium altitude ( < 3 0 0 0 m ) , the physiological and haematological adjustments are sufficiently well coordinated. They remain within the safety limits compatible with a normally functioning circulatory system (Coudert, Durand, Lokhart , Marc-Vergnes and Mart ineau 1972).

The increased viscosity due to the increase in the number of red cells remains within reasonable limits (Geigy 1963). Too fast an increase of the vifccosity is likely to cause cardiovascular disturbances, so the organism calis on another adaptat ive mechanism situated at the level of intra-erythrocyte metabolism to improve the supply of oxygen to the tissues. The erythropoietic response, which depends on the degree of hypoxia, is still strong (figure 1) but nevertheless weaker than that required if there had not been any biochemical adapta t ion of the red cell (Arnaud 1979).

A Ititucie anthropobiology The two human groups studied here are of the same origin (Vellard 1973) but have

been living for thousands of years in diíTerent surroundings, the Aymaras inhabiting the northern zone of the Andean Altiplano and the Quechuas irregularly scattered from the Altiplano to the Andean Valleys. The two groups show diíTerent adaptat ive patterns.The adaptat ive polycythaemia observed seems to be an acquired and irreversible adaptat ive character in the Aymaras, as it persists under normal environmental living conditions (return to lowlands, figure 2). Our observations do not agree with those of Moulin (1971), who noted that all the haematological data were higher for the Quechuas than for the Aymaras. If such is the case for the acclimatization phenomena (though it seems diíTicult to consider an acclimatization to high altitude of the Aymaras already adapted to such conditions), it does not appear as obvious for the adaptat ion phenomena. The reason for this is probably that throughout our study, we selected persons who had been residing permanently at altitude for a time longer than that required for acclimatization (Baker and Little 1976). The advantages that the Aymaras draw from this situation are (¿/) an increase in gas-carrying capacity in the blood (RBC and Hb; figure 2) without excessive polycythaemia (Whittembury, Lozano, Torres and Monge 1968) (b) better buíTer capacity within the red cells due to the increase in the haemoglobin level (Lefrangois, Gautier, Pasquies, Cevaer and Hellot 1970), so that the red cells are better adapted to control any possible variation in the pH caused either directly by hypoxia or indirectly by the physiological response to hypoxia (hyperventilation) (Lefrangois, Pasquies and Gautier 1976). and (c) an increase in the quanti ty of inactive H b kept in store (metHb) which is increased at altitude (Arnaud, Quilici, Gutierrez, Beard and Vergnes 1979, Arnaud 1979).

The Quechuas, owing to their mobility and henee to the large geographical zone and the ecological diversity of their habitat , have not been able to acquire the

High-altitude haematology 577

adaptat ive characters favourable to life in conditions of chronic hypoxia at high altitude. The more sedentary Aymaras, when transplanted to lowlands (450 m), keep some of the adaptat ive characters, as we have observed, though the hypoxic stress has completely disappeared. If the environment is responsible for the development of adaptat ive characters, the "climat social" (Bernard and Ruffié 1966) has played an important part in their selection. In the course of millenia an ethnical hierarchy separated the two groups, and the Aymaras withdrew to higher and more inhospitable zones than those peopled by the Quechuas .

References ARNAUD, J . , 1979, Fonction respiratoire de lerythrocyte humain en haute altitude. Anthropobiologie

moléculaire de Tadaptation á la haute altitude. Thése d'Etat de Sciences no. 881, Université Paul Sabatier, Toulouse.

ARNAUD, J . , QUILICI, J . C . , GUTIERREZ, N . , BHARD, J . , and VFRGNES, H . , 1979, Methaemoglobin and erythrocyte reducing systems in high altitude natives. Annals of Human Biology, 6, 585 592.

BAKER, P . T . , 1978, The Biology of High Altitude Peoples, International Biological Programme 14, (Cambridge: Cambridge University Press).

BAKI R, P. T., and LMTI.E, M. A., 1976, Man in the Andes. A multidisciplinary study ofhigh altitude Quechua. (Stroudsburg, PA: Dowden, Hutchinson and Ross).

BERNARD, J . . and RÜFUÉ, J., 1966, Hématologie Géographigue (Paris: Masson). BI RSAI E. , D I IU>s, C . , and POYAR I, C . F., 1971, Pouvoir oxyphorique et P50 du sang humain. Bulletin de

Physio-Pathologie Respiratoire, 7, 7 2 9 - 7 4 2 . COUDERT, J . , DÜRAND, J . , LOCKHART, A. , M A R O VIRGNES, J . P., and MARTINEAUD, J . P., 1972, Les réponses

circulatoires provoquées par le séjour permanent ou passager en altitude. C.N.R.S., RCP 87. GIIGY, 1963, Tahles Scienti fiques, 6th edition. Département Pharmaceutique, Geigy, p. 563. LI I R \N(,()is, R . , G A I I II R, H . , PASQUES, P., CEVAER, A . M . , and H I L L O I , M . , 1970, Pouvoir tampon du sang

humain á haute et basse altitude. Journal de Physiologie, 62, 4 0 1 - 4 0 2 . LFFRAN^OIS, R. , PASQUIS, P., and G A U I I I R , H . , 1976, Mecanisme de Tadaptation respiratoire a la haute

altitude. In Anthropologie des Populations Andines. Les colloques de L ' I N S E R M , vol. 63 , pp. 2 5 9 2 7 0 . MONGE, M . C„ 1930, Les erythrémies iV altitudes (Paris: Masson). MOULIN. J „ 1971, Hématimétrie et cytologie en milieu tropical de TAmérique du Sud: variations raciales et

¿cologiques. Thése, Université Paul Sabatier, Toulouse. Rui FIÉ, J., 1976, De la Biologie ¿i la Culture (Paris: Flammarion). RUFFIÉ, J . , QUILIC I, J. C., and LACOSTE, M . C., 1976, Anthropologie Jes Populations Andines, Colloque

I N S E R M , n o . 6 3 . SEBBAG, R., 1978,Contribution a le tudedeszonesdeco lon i sa t ion en basses terres boliviennes. Uneenquéte

bio-médicale á Yapacani. Thése de Médecine, Université Paul Sabatier, Toulouse. VELLARD, J . A. , 1973, Etudes sur les populations indigenes de la Bolivie. Populations du Piémont Andin.

Monographie du C N R S (Paris: C N R S ) . WHITTEMBURY, J . , LOZANO, R. , TORRES, C . , MONGE, C . , 1968, Blood viscosity in high altitude polycythemia.

Acta physiologica latino americana, 18, 355- 359. Address correspondence to: Mr. J. Arnaud, Centre dTlémotypologie du C.N.R.S., C.H.U. de Purpan,

Avenue de Grande Bretagne, 31300 Toulouse, France.

Zusammenfassung. Hamatologische Untersuchungen wurden in verschiedenen Hóhen zwischen 450 und 4800 Metern bei zwei getrennten, südamerikanischen Gruppen (Quechuas and Aymaras) durchgeführt. Die Veránderungen der hámatologischen Parameter entwickeln sich nicht in einer linearen Funktion im Verháltnis zur Hóhe. Die Wirkung der chronischen Hypoxie auf die Erythropoese ist über 3000 Meter grótter. Das Hámogramm variiert quantitativ und nicht qualitativ (MCV und M H C bleiben konstant). Die hamatologische Untersuchung zeigt auch eine gróBere Anpassungsíahigkeit der Aymaras an groBe Hóhe, eine Anpassungsfahigkeit, die gekennzeichnet ist durch eine Zunahme der Zahl der roten Blutkorperchen und der Hamoglobinkonzentration und einer Abnahme des Volumens der roten Blutkorperchen. Die adaptiven Erscheinungen, die bei den Quechuas beobachtet wurden, sind reversibel, wohingegen sie bei den Aymaras bestehen bleiben, wenn sie in das Tielland (450 Meter) wandern.

Resume. Des etudes hematologiques ont ete menees a di verses altitudes de 450 m a 4K00 m sur deu \ groupcs humains diííerents (Quechuas el Aymaras) vi\ant en Amérique du Sud. Les changements des parámetros hematologiques ne se íont pas selon une fonction lineaire de l'altitude. L'impacl de l'hypoxie chronique sur l'er>thropoiese est plus marque au-dessus de 3000m. L'hemogramme varié quantitati \ement et non

578 Hiyh-altitude haematology

qualitativement (les MCV et MHC restent constants). L etude hematologique revele aussi la plus grande adaptabilite des Aymaras á la haute altitude, une adaptabilité caracterisée par une augmentation du compte de globules rouges et de la concentration d'hémoglobine et une diminution du volume de globules rouges. Les phenomenes adaptatifs observés chez les Quechuas sont reversibles tandis qu'ils persistent chez les Aymaras quand ils migrent en región basse (450 m).