Variation in epinephrine and cortisol excretion rates associated with behavior in an Australian...

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Variation in Epinephrine and Cortisol Excretion Rates Associated With Behavior in an Australian Aboriginal Community LINCOLN H. SCHMITT, 1 * G.A. HARRISON, 2 AND R.M. SPARGO 3 1 Department of Anatomy and Human Biology, The University of Western Australia, Nedlands, Western Australia 6907, Australia 2 Institute of Biological Anthropology, University of Oxford, Oxford OX2 6QS, United Kingdom 3 Health Department of Western Australia, Derby, Western Australia 6728, Australia KEY WORDS stress hormones; blood pressure; lifestyle; gambling ABSTRACT Urinary epinephrine and cortisol hormone output in a re- mote Australian Aboriginal community was on average about twice as high in those individuals measured on a Thursday or Friday as those measured at the beginning of the next week (Monday or Tuesday). Diastolic blood pressure was about 6 mm Hg higher in the Thursday–Friday group, but the difference in mean systolic blood pressure between the day groups does not reach statisti- cal significance. These physiological differences are associated with a marked dichotomy in behavior in the two time periods: on the first 2 days, virtually all adults were involved in intense gambling activity for large stakes, but this was not a feature of the latter period. This behavior pattern occurs on a regular weekly basis. If substantiated by longitudinal studies, this phenom- enon may provide an additional link between human behavior and a poor health profile mediated via the physiological consequences of high stress hormone output. Am J Phys Anthropol 106:249–253, 1998. r 1998 Wiley-Liss, Inc. Epinephrine and cortisol are central ele- ments in the maintenance of homeostasis and the stress response, but chronically high levels have been implicated in the etiology of some of the so-called lifestyle diseases, in- cluding hypertension, coronary heart dis- ease, and non–insulin dependent diabetes mellitus (e.g., Steptoe, 1981; Kenyon and Fraser, 1992; Bjo ¨rntorp, 1996). Experimen- tal studies have revealed a plethora of nox- ious stimuli that elevate stress hormone excretion rates. More carefully controlled experiments have revealed that many of these responses are due to the cognitive appraisal of the stimulus, and it has been suggested that everyday living experiences are a major determinant of endocrine hor- mone output variation (Mason, 1971; Mason et al., 1976). Anthropological studies that have revealed an association between life- style and hormone excretion include com- parisons of migrant groups (e.g., Brown 1982; Pearson et al., 1990) and the level of self-reported stress and busyness (e.g., Pol- lard et al., 1992). A recent study revealed exceptionally high urinary cortisol excretion rates in three Aus- tralian Aboriginal communities in the Kim- berley region that are undergoing rapid sociocultural change. Epinephrine excretion was also high in the same groups by world standards (Schmitt et al., 1995). The factors responsible for these high populational lev- els and for the variation within communities are difficult to determine. In this paper we describe in more detail urinary stress hor- mone excretion rates found in one of those communities and note its association with a marked change in the behavior of most *Correspondence to: Lincoln H. Schmitt, Department of Anatomy and Human Biology, The University of Western Austra- lia, Nedlands, WA 6907, Australia. E-mail: [email protected] Received 2 September 1997; accepted 25 February 1998. AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 106:249–253 (1998) r 1998 WILEY-LISS, INC.

Transcript of Variation in epinephrine and cortisol excretion rates associated with behavior in an Australian...

Variation in Epinephrine and Cortisol Excretion Rates AssociatedWith Behavior in an Australian Aboriginal Community

LINCOLN H. SCHMITT,1* G.A. HARRISON,2 AND R.M. SPARGO3

1Department of Anatomy and Human Biology, The University of WesternAustralia, Nedlands, Western Australia 6907, Australia2Institute of Biological Anthropology, University of Oxford,Oxford OX2 6QS, United Kingdom3Health Department of Western Australia, Derby,Western Australia 6728, Australia

KEY WORDS stress hormones; blood pressure; lifestyle; gambling

ABSTRACT Urinary epinephrine and cortisol hormone output in a re-mote Australian Aboriginal community was on average about twice as high inthose individuals measured on a Thursday or Friday as those measured at thebeginning of the next week (Monday or Tuesday). Diastolic blood pressure wasabout 6 mm Hg higher in the Thursday–Friday group, but the difference inmean systolic blood pressure between the day groups does not reach statisti-cal significance. These physiological differences are associated with a markeddichotomy in behavior in the two time periods: on the first 2 days, virtually alladults were involved in intense gambling activity for large stakes, but thiswas not a feature of the latter period. This behavior pattern occurs on aregular weekly basis. If substantiated by longitudinal studies, this phenom-enon may provide an additional link between human behavior and a poorhealth profile mediated via the physiological consequences of high stresshormone output. Am J Phys Anthropol 106:249–253, 1998. r 1998 Wiley-Liss, Inc.

Epinephrine and cortisol are central ele-ments in the maintenance of homeostasisand the stress response, but chronically highlevels have been implicated in the etiology ofsome of the so-called lifestyle diseases, in-cluding hypertension, coronary heart dis-ease, and non–insulin dependent diabetesmellitus (e.g., Steptoe, 1981; Kenyon andFraser, 1992; Bjorntorp, 1996). Experimen-tal studies have revealed a plethora of nox-ious stimuli that elevate stress hormoneexcretion rates. More carefully controlledexperiments have revealed that many ofthese responses are due to the cognitiveappraisal of the stimulus, and it has beensuggested that everyday living experiencesare a major determinant of endocrine hor-mone output variation (Mason, 1971; Masonet al., 1976). Anthropological studies thathave revealed an association between life-style and hormone excretion include com-parisons of migrant groups (e.g., Brown

1982; Pearson et al., 1990) and the level ofself-reported stress and busyness (e.g., Pol-lard et al., 1992).

A recent study revealed exceptionally highurinary cortisol excretion rates in three Aus-tralian Aboriginal communities in the Kim-berley region that are undergoing rapidsociocultural change. Epinephrine excretionwas also high in the same groups by worldstandards (Schmitt et al., 1995). The factorsresponsible for these high populational lev-els and for the variation within communitiesare difficult to determine. In this paper wedescribe in more detail urinary stress hor-mone excretion rates found in one of thosecommunities and note its association with amarked change in the behavior of most

*Correspondence to: Lincoln H. Schmitt, Department ofAnatomy and Human Biology, The University of Western Austra-lia, Nedlands, WA6907,Australia. E-mail: [email protected]

Received 2 September 1997; accepted 25 February 1998.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 106:249–253 (1998)

r 1998 WILEY-LISS, INC.

members of the community during the courseof the sampling period. In this community,the behavioral change occurs on a regularweekly basis.

SUBJECTS AND METHODS

A urine specimen was collected from 62adult volunteers aged 19–67 years as part ofan investigation of stress hormone output inKimberley Aboriginal people (Schmitt et al.,1995). The subjects live in a community ofabout 350 people in a tropical environmentand about 600 km from the nearest town.Virtually all individuals in this communityshare some genetic relationship. Subjectscame to the local health clinic, a central sitein the community, at about 3 PM, when theyvoided their bladder, and weight, stature,and blood pressure (assessed with an elec-tronic digital sphygmomanometer) were re-corded. They then resumed their usual activi-ties until around 5 PM, when they returnedand voided their bladder, and the urine wascollected. Epinephrine and cortisol were as-sayed by high pressure liquid chromatogra-phy (Jenner et al., 1981; Jenner and Rich-ards, 1985).

For the analyses described here, eachsample was allocated to one of two daygroups according to the day of urine collec-tion, either Thursday–Friday or Monday–Tuesday. Each individual contributed onesample only. Many people received wages orsocial benefits on Thursday around midday,when work ceased and almost all membersof the community became involved in cardgambling for large stakes over the next 2days. While gambling continued during theMonday and Tuesday collections, it involvedfar fewer individuals, and the stakes hadbecome trivial.

Because the data design is unbalanced,multiple regression was used to assess therelationship between hormone output (asresponse variables) and day group, sex, age,urine flow rate, stature, and weight (asexplanatory variables), with day group andsex coded as dummy variables. Both forwardand backward selection methods were used,the latter beginning with all the three-wayinteraction terms involving sex and daygroup and each of the metric features. Ex-

cept where noted, these two selection meth-ods produced the same results. These mul-tiple regression analyses are equivalent toextended forms of analysis of covariance forunbalanced data, with the added advantagethat the assumptions of parallel slopes wereassessed through the testing of interactionsbetween discrete and continuous variables.Similar analyses of diastolic and systolicblood pressure as response variables werealso undertaken. Hormone output, weight,and urine flow rate were log10 transformedbefore all analyses, and reported means areback-transformed values. Genstat (Genstat5 Committee, 1993) was used for all statisti-cal analyses.

RESULTS

The samples of the two day groups, Thurs-day–Friday and Monday–Tuesday, do notdiffer in sex ratio (x2 5 0.26, P 5 0.61) or themeans of age, stature, or weight (Table 1).Urine flow rate is significantly higher in theMonday–Tuesday group, and cortisol andepinephrine excretion rates are significantlyhigher in the Thursday–Friday group. Bothsystolic and diastolic blood pressure are alsohigher in the Thursday–Friday group, butthese differences do not quite reach statisti-cal significance.

For epinephrine, multiple regressions re-vealed two statistically significant effects: apositive association with urine flow rate(P 5 0.008) and a higher mean in theThursday–Friday group (P 5 0.004). Thesexes were not significantly different in epi-nephrine excretion rates in this sample (P 50.318), although the male mean was signifi-cantly greater than the female mean in thetotal regional sample (Schmitt et al., 1995).Correcting epinephrine output for urine flowrate revealed a pattern between the two daygroups (Fig. 1) that was similar to theuncorrected values (Table 1).

Forward selection multiple regression withcortisol as the response variable revealedthe Thursday–Friday group has a highermean (P 5 0.027), and this is the onlysignificant effect. Backward elimination indi-cated two significant interactions: betweenage and sex and between stature and daygroup. The interactions arise because the

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regression of cortisol on age is different formales and females, and the regression onstature is different for the two day groups.These interaction effects are possibly a con-sequence of overfitting the regression model.Nonetheless, using the regression estimatesto adjust statistically for these effects to themean of age and stature (Fig. 2) reveals daygroup differences that are similar to theuncorrected data (Table 1). Adding urineflow rate to any of the models tested did notappreciably alter the results.

Multiple regression of diastolic blood pres-sure reveals significant associations with

weight (P , 0.001), sex (P 5 0.006), and daygroup (P 5 0.043). Diastolic blood pressureis about 6 mm Hg higher in the Thursday–Friday group than the Monday–Tuesdaygroup (Table 2). Systolic blood pressure issignificantly associated with age (P , 0.001)and sex (P 5 0.001), but the two day groupsare not different (P 5 0.13).

DISCUSSION

The community that forms the subject ofthis study experiences a regular weeklybehavioral cycle which is directly related tothe receipt of income. Most individuals re-ceive their major cash income through fort-nightly employment payments or govern-ment social payments, and these two formsare paid out on alternating weeks. At thetime of this study, the payments occurred onthe first day of urine collection, a Thursdayaround midday, and it immediately led tointense card gambling activity, involvingsubstantial portions of the payment. Virtu-ally all the adults in the community wereinvolved either as players or spectators witha strong vested interest in the outcome. Thisintense gambling continued on the Fridaybut declined rapidly over the weekend, andby the Monday only a small proportion of the

Fig. 1. Regression-corrected mean epinephrine (61 standard error).

TABLE 1. Samples sizes (N), mean values for daygroups, and probability values (P ) for tests of

significance of the equality of the two day groups

Thursday–Friday

Monday–Tuesday P

N males 13 18N females 15 16Age (years) 37.3 32.4 0.11Stature (mm) 1694 1715 0.31Weight (kg) 76.4 72.7 0.38Urine flow rate (ml/h) 47.8 76.8 0.033Epinephrine output (µg/h) 0.737 0.433 0.032Cortisol output (µg/hr) 2.57 1.26 0.027Diastolic blood pressure

(mm Hg) 80.2 73.9 0.056Systolic blood pressure

(mm Hg) 129.8 119.5 0.054

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community participated in gambling, andthe stakes were trivial. Although the exactdetails are not known for this particularweek, in general the decline in high-stakegambling seems to be a consequence of theone or few winners of substantial sums towithdraw the money from the community.This behavioral phenomenon occurs on aregular weekly cycle in this and probablyother Kimberley Aboriginal communities.

Frankenhaeuser’s (1989) biopsychosocialmodel of hormone determinants ascribesmental effort as the primary determinant ofepinephrine output and negative affect asthe major determinant of cortisol levels. It isclear that gambling could lead to high men-tal effort, both on the part of gamblers and

those watching with strong vested interests,and this may explain the higher levels ofepinephrine on the Thursday and Friday.Intense gambling almost certainly involvesmuch emotion, and for most this will benegative and might therefore be expected tolead to increased cortisol output in the groupas a whole. Hunter and Spargo (1988) notedthat the observer often experiences moreintense negative emotion than the player.

There are several possible confoundingfactors in this cross-sectional study, and theeffects described here may not be a direct oreven indirect consequence of the behavioralobservations noted. The results could be aconsequence of unforeseen physical environ-mental factors, but obvious parameters suchas daily temperature fluctuations are smallin this tropical environment. In the labora-tory, samples were analyzed in a randomorder and without any knowledge of the fieldconditions. It is possible that bias self-selection of volunteers led average differ-ences between the two day groups, but whatis apparent to the casual observer is that theintense interest in gambling or its outcomeis ubiquitous in this community. The valid-ity of the results reported here and theirinterpretation await more thorough studies

TABLE 2. Mean diastolic and systolic blood pressure(6 standard error) corrected for significant covariates

Thursday–Friday

Monday–Tuesday

Diastolic blood pressure(mm Hg)

Male 84.0 6 2.54 78.3 6 2.21Female 76.2 6 2.35 70.5 6 2.37

Systolic blood pressure(mm Hg)

Male 134.4 6 3.45 128.6 6 3.03Female 121.3 6 3.24 115.5 6 3.21

Fig. 2. Regression-corrected mean cortisol (61 standard error).

252 L.H. SCHMITT ET AL.

of the activities of community members andlongitudinal measures of hormone output.

There are several possible causes of differ-ential urine flow rates in the two day groups,including, for example, differences in physi-cal activity or liquid intake which may them-selves be direct or indirect consequences ofbehavioral differences. In the total Kimber-ley sample, urine flow rate was generallypositively associated with epinephrine andcortisol output, with the exception of cortisolexcretion in males (Schmitt et al., 1995).Here we observe the opposite effect, withhigh flow rates on Monday–Tuesday whenepinephrine and cortisol outputs are rela-tively low. Hence, it is unlikely that thehormone differences between the day groupsare mediated through urine flow rates, andthis is confirmed by the statistical correc-tions for flow rate that have been employedand lead to no substantive changes in thepatterns.

Studies of people experiencing rapid socio-cultural change report high stress hormonelevels, and this change is often associatedwith a poor health profile. These conditionsare features of Kimberley Aborigines. Gam-bling has been implicated as a factor in thisweb of cultural change phenomena. Hunterand Spargo (1988) have argued that gam-bling has widespread and deleterious public-health consequences, affecting nutrition,parenting, and the ability to utilize re-sources over an extended time frame. Fur-thermore, they report that the effect of los-ing money is less anxiety-provoking thanthe subsequent but immediate desire to getmore money to continue playing. Therefore,gambling may act as a factor in diseasethrough the physiological consequence ofhigh stress hormone output. Cortisol in par-ticular is known to increase blood pressure(Kenyon and Fraser, 1992), which is associ-ated with cardiovascular disease, and toinfluence centripetal fat deposition, which isassociated with non–insulin dependent dia-betes mellitus. In the Kimberley communitythat was the focus of this study and someother Australian Aboriginal groups, the inci-dence of these two diseases is several times

the Australian average (Gracey and Spargo,1987; Thomson, 1991).

ACKNOWLEDGMENTS

We particularly thank the Aboriginal vol-unteers and health workers who made thestudy possible, Giles Ungpakorn for thelaboratory hormone assays, and Tessa Pol-lard, Sue Hisheh, and Michael Gracey forassistance with the manuscript.

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