Diminuição da temperatura do corpo humano nos Estados Unidos desde a Revolução Industrial
A temperatura corporal humana considerada “normal” foi estabelecida em 1851, com o trabalho do médico alemão Carl Reinhold August Wunderlich.
Ele mediu a temperatura das axilas de mais de 25 mil pessoas, e chegou ao valor de 37º C.
Médico alemão Carl Reinhold August Wunderlich, em 1851 estabelece o padrão da temperatura normal humana em 37º C.
Deste modo, o valor da temperatura humana (equivalendo a 37º C, tem sido aceito como padrão na medicina por órgãos internacionais, como a Organização Mundial da Saúde (OMS).
uma equipe de pesquisadores da Universidade Stanford/USA, discordando desse valor e argumentando que poderá estar desatualizado, delineou um experimento para mostrar essa afirmação.
Os pesquisadores analisaram então três conjuntos de dados de períodos distintos:
um amostra de soldados da Guerra Civil norte-americana (1861 a 1865),
uma amostra da década de 1970
e outra amostra dos anos 2000 e 2010.
Totalizando 677.423 amostras de pessoas diferentes (e épocas) diferentes.
A comparação entre as três medições revelou que os homens de hoje têm uma temperatura média 0,59º C menor do que a dos homens que nasceram na primeira metade do século 19. As mulheres também estão mais frias: -0,23º C, em média.
Em vez de 37º C, a nova temperatura padrão é de 36,62º C para homens, para as mulheres, o valor é ligeiramente maior.
FUNDAMENTAL PRINCIPLES.
§ 1. Two facts justify the physician in using the thermometer everywhere, tlie invariabilit}'- of the temperature in healthy persons, and its variations in disease.
§ 2. The average temperature taken at the axilla, or in any other artiticial cavity, is 98.6° F. = 37° C.=Zero- health of the medical thermometer (see second part) ; and higher by some tenth of a degree in the natural cavities. [In England the Norme is 98.4° F. ; in France, 36.9° C, where Brecliet had the glory of establishing it. Till these discrepancies shall be demonstrated to correspond, or not, to important facts of race or climate, we have no right to infirm them, but we fiave to signalize the necessity of their final verification as one of the most important objects of the future investigations on thermometry.— E. S.]
§ 3. The temperature of healthy persons is almost constantly the same ; its oscillations in the course of a day seldom exceed 1° Cent.=^° Fahr. (unusual conditions excepted). " The maintenance of a normal temperature under varying conditions, or, in other words, a constant temperature in any individual, is a proof of a sound constitution."
§ 4. A normal temperature does
not necessarily indicate health ; " but all those whose temperature either
exceeds or falls short of the normal range, are unhealthy."
§ 5 The range of temperature in
severe diseases is between 35° C.=95° F. and 42.5° C.=108.5° F., and very falls
below 33° C. = 91.4° F., or rises to 43°C.= 109.4° F., though in rare cases it
has reached 44.75° C.= X 112.55° F.
§ 6. Deviations from the normal course of temperature never occur
without causes or fixed "laws ; " that is the foundation of "
Pathological Thermometry." We sometimes fail to discover these laws,
because in disease, more than in health, the temperature of the body is the result
of mutually antagonistic factors.
§ 7. Influences which in no way disturb the temperature of the
healthy, derange that of the sick, even if tliey hardly aftect his sickness.
" Mobility of temperature under the action of external influences is,
therefore, a sign ^ of some diseased condition of the body." Therefore the
discovery of abnormal temperatures in men previously healthy is a means of
discovering or confirming the existence of a latent disease.
§ 8. Alterations of temperature may be confined to special
regions, whilst the rest of the body remains almost normal; they seldom exceed
1° C. = 1.8 — 2° F. ; but are accompanied by other obvious phenomena more
useful for the diagnosis than the local abnormality of temperature.
§ 9. The general temperature is the " expression "
of several processes, some tending to the production of heat, others to its
exhalation. However varied is the combination of these processes, their thermal
result, or the specific heat of the body, remains the same in health ; and its variations
in disease, though not absolutely trustworthy, are yet the safest standard by
which to estimate the condition of the whole body. Variations of temperature
coincide with other functional and structural disturbances not so easy to
measure, and often appear long before other morbid alterations can be
recognized.
§ 10. The heat of the whole body may be normal.
Measurement and Evaluation of Body Temperature: Implications
for Clinical Practice
Märtha Sund-Levander
Evaluation of body temperature is one of the oldest known diagnostic methods [6, 7] and is still an important sign of health and disease, both in everyday life and in medical care. Increased body temperature is associated in the first place with infectious disease and fever [8] and the accompanying feelings of illness. In general, the individual can describe feelings of illness and discomfort, but in conditions where individuals are unable to explain themselves, the nurse has to interpret the clinical signs and rely on objective measurements. This is especially important when assessing elderly individuals [9], as atypical presentation of infection are common in this age group [10]. Before the 17th century, the humoral theory, established by Galen in the second century A.D., dominated medical thinking [7], and the interpretation of symptoms and explanations of disease were closely related to philosophy and religion [11]. Evaluation of body temperature rested on objective and subjective feelings of warmth, i.e. physicians used touch as their principal criterion for evaluating body heat [12]. The discovery of the circulation of the blood emphasised the use of natural sciences in medicine and clinicians started to use the pulse rate to diagnose fever [13]. This remained to be the most important tool even when the first thermometers were available in the late 18th century. A that time, the improved scientific knowledge of human anatomy and physiology, attributed to the introduction of autopsy [14], and new technical knowledge [9] increased the interest in objectively observing the patient [12, 15] and thus the possibility to differentiate between health and disease using biological parameters in terms of what was considered normal and abnormal. The first comprehensive report on body temperature related to normality was published in 1868 by the German physician Wunderlich [16], who established the use of thermometers in medical practice [17]. Wunderlich measured axillary temperature in patients and declared the normal body temperature to be 37.0°C with a range of 36.2°C to 37.5°C. He defined temperatures above 37.5°C as “the territory of fever” and > 38.0°C as fever [18]. Today there is a general acceptance of normal body temperature as a range rather than a fixed temperature, although there is still widespread confusion in the assessment and evaluation of body temperature in adults [19], especially in elderly individuals [20-22]. A recently performed systematic review of the literature [23] found that the range in normal body temperature was 33.2°C to 38.2°C and that few studies reported average values of body temperature equal to or above 37.0°C, i.e. the rectal temperature in six studies and the ear temperature in one study [20, 24-28].
Decreasing human body temperature in the United States since the Industrial Revolution
Myroslava Protsiv, Catherine Ley, Joanna Lankester, Trevor Hastie, Julie Parsonnet
Stanford University, School of Medicine, United States;
Jan 7, 2020
Abstract
In the US, the normal, oral temperature of adults is, on average, lower than the canonical 37°C established in the 19th century. We postulated that body temperature has decreased over time. Using measurements from three cohorts—the Union Army Veterans of the Civil War (N = 23,710; measurement years 1860–1940), the National Health and Nutrition Examination Survey I (N = 15,301; 1971–1975), and the Stanford Translational Research Integrated Database Environment (N = 150,280; 2007–2017)—we determined that mean body temperature in men and women, after adjusting for age, height, weight and, in some models date and time of day, has decreased monotonically by 0.03°C per birth decade. A similar decline within the Union Army cohort as between cohorts, makes measurement error an unlikely explanation. This substantive and continuing shift in body temperature—a marker for metabolic rate—provides a framework for understanding changes in human health and longevity over 157 years.
In1851, the German physician Carl Reinhold August Wunderlich obtained millions of axillary temperatures from 25,000 patients in Leipzig, thereby establishing the standard for normal human body temperature of 37°C or 98.6 °F (range: 36.2–37.5°C [97.2- 99.5 °F]) (
Mackowiak, 1997;
Wunderlich and Sequin, 1871). A compilation of 27 modern studies, however (
Sund-Levander et al., 2002), reported mean temperature to be uniformly lower than Wunderlich’s estimate. Recently, an analysis of more than 35,000 British patients with almost 250,000 temperature measurements, found mean oral temperature to be 36.6°C, confirming this lower value (
Obermeyer et al., 2017). Remaining unanswered is whether the observed difference between Wunderlich’s and modern averages represents true change or bias from either the method of obtaining temperature (axillary by Wunderlich vs. oral today) or the quality of thermometers and their calibration (
Mackowiak, 1997). Wunderlich obtained his measurements in an era when life expectancy was 38 years and untreated chronic infections such as tuberculosis, syphilis, and periodontitis afflicted large proportions of the population (
Murray et al., 2015;
Tampa et al., 2014;
Richmond, 2014). These infectious diseases and other causes of chronic inflammation may well have influenced the ‘normal’ body temperature of that era.
The question of whether mean body temperature is changing over time is not merely a matter of idle curiosity. Human body temperature is a crude surrogate for basal metabolic rate which, in turn, has been linked to both longevity (higher metabolic rate, shorter life span) and body size (lower metabolism, greater body mass). We speculated that the differences observed in temperature between the 19th century and today are real and that the change over time provides important physiologic clues to alterations in human health and longevity since the Industrial Revolution.
The question of whether mean body temperature is changing over time is not merely a matter of idle curiosity. Human body temperature is a crude surrogate for basal metabolic rate which, in turn, has been linked to both longevity (higher metabolic rate, shorter life span) and body size (lower metabolism, greater body mass). We speculated that the differences observed in temperature between the 19th century and today are real and that the change over time provides important physiologic clues to alterations in human health and longevity since the Industrial Revolution.
In men, we analyzed: a) 83,900 measurements from the Union Army Veterans of the Civil War cohort (UAVCW) obtained between 1862 and 1930, b) 5998 measurements from the National Health and Nutrition Examination Survey I cohort (NHANES) obtained between 1971 and 1975, and c) 230,261 measurements from the Stanford Translational Research Integrated Database Environment cohort (STRIDE) obtained between 2007 and 2017 (
Table 1). We also compared temperature measurements in women within the two later time periods (NHANES, 9303 measurements; and STRIDE, 348,006 measurements).
Fig. 1
Body temperature measurements by age as observed in three different time periods: 1860–1940 (UAVCW), 1971–1975 (NHANES 1), and 2007–2017 (STRIDE).
(A) Unadjusted data (local regression) for temperature measurements, showing a decrease in temperature across age in white men, black men, white women, and black women, in the three cohorts. (B) Coefficients and standard errors from multivariate linear regression models for each cohort including age, weight, height, ethnicity group and time of day as available. Yellow cells are statistically significant at a p value of < 0.01, orange cells are of borderline significance (p0.05), and remaining uncolored cells are not statistically significant. (C) Expected body temperature for 30 year old men and women with weight 70 kg and height 170 cm in each time period/cohort.
In both STRIDE and a one-third subsample of NHANES, we confirmed the known relationship between later hour of the day and higher temperature: temperature increased 0.02°C per hour of the day in STRIDE compared to 0.01°C in NHANES. The month of the year had a relatively small, though statistically significant, effect on temperature in all three cohorts, but no consistent pattern emerged. Using approximated ambient temperature for the date and geographic location of the examination in UAVCW and STRIDE, a rise in ambient temperature of one degree Celsius correlated with 0.001 degree (p
We explored whether chronic infectious diseases—even in the absence of a diagnosis of fever—might raise temperature in the UAVCW cohort, by assessing the temperatures of men reporting a history of malaria (N = 2,203), syphilis (N = 465), or hepatitis (N = 24), or with active tuberculosis (N = 738), pneumonia (N = 277) or cystitis (N = 1,301). Only those currently diagnosed with tuberculosis or pneumonia had elevated temperatures compared to the remainder of the UAVCW population [37.22°C (95% CI: 37.20–37.24°C) and 37.06°C (95% CI: 37.03–37.09°C), respectively compared to 37.02 (95% CI: 36.52–37.53)].
One possible reason for the lower temperature estimates today than in the past is the difference in thermometers or methods of obtaining temperature. To minimize these biases, we examined changes in body temperature by birth decade within each cohort under the assumption that the method of thermometry would not be biased on birth year. Within the UAVCW, we observed a significant birth cohort effect, with temperatures in earlier birth decades consistently higher than those in later cohorts (
Figure 2). With each birth decade, temperature decreased by −0.02°C. We then assessed change in temperature over the 197 birth-year span covered by the three cohorts. We observed a steady decrease in body temperature by birth cohort for both men (−0.59°C between birth decades from 1800 to 1997; −0.030°C per decade) and women (−0.32°C between 1890 and 1997; −0.029°C per decade). Black and white men and women demonstrated similar trends over time (
Figure 3).
Fig. 2
Temperature trends within birth cohorts of the UAVCW, 1860–1940 (black and white men).
(A) Smoothed unadjusted data (local regression) for temperature measurement trends within birth cohorts. The different colors represent different birth cohorts (green: 1820s, blue: 1830s, orange: 1840s). (B) Coefficients (and standard errors) from multivariate linear regression including age, body weight, height and decade of birth (1820–1840) (these coefficients do not correspond to the graph as here the trajectories are approximated by linear functions). Only the three birth cohorts with more than 8000 members are included. * and ** indicate significance at the 90%, and 99% level, respectively. (C) Expected body temperature (and associated 95% confidence interval) for 30 year old men with body weight 70 kg and height 170 cm in each birth cohort. These values derive from the regression models presented in B.
Fig. 3
Modeled body temperature over time in three cohorts by birth year (black and white ethnicity groups).
(A) Body temperature decreases by birth year in white and black men and women. No data for women were available for the birth years from 1800 to 1890. (B) Coefficients (and standard errors) used for the graph from multivariate linear regression including age, body weight, height and birth year. All cells are significant at greater than 99% significance level.
DISCUSSION
In this study, we analyzed 677,423 human body temperature measurements from three different cohort populations spanning 157 years of measurement and 197 birth years. We found that men born in the early 19th century had temperatures 0.59°C higher than men today, with a monotonic decrease of −0.03°C per birth decade. Temperature has also decreased in women by −0.32°C since the 1890s with a similar rate of decline (−0.029°C per birth decade). Although one might posit that the differences among cohorts reflect systematic measurement bias due to the varied thermometers and methods used to obtain temperatures, we believe this explanation to be unlikely. We observed similar temporal change within the UAVCW cohort—in which measurement were presumably obtained irrespective of the subject's birth decade—as we did between cohorts. Additionally, we saw a comparable magnitude of difference in temperature between two modern cohorts using thermometers that would be expected to be similarly calibrated. Moreover, biases introduced by the method of thermometry (axillary presumed in a subset of UAVCW vs. oral for other cohorts) would tend to underestimate change over time since axillary values typically average one degree Celsius lower than oral temperatures (
Sund-Levander et al., 2002;
Niven et al., 2015). Thus, we believe the observed drop in temperature reflects physiologic differences rather than measurement bias. Other findings in our study—for example increased temperature at younger ages, in women, with increased body mass and with later time of day—support a wealth of other studies dating back to the time of Wunderlich (
Wunderlich and Sequin, 1871;
Waalen and Buxbaum, 2011).
Resting metabolic rate is the largest component of a typical modern human’s energy expenditure, comprising around 65% of daily energy expenditure for a sedentary individual (
Heymsfield et al., 2006). Heat is a byproduct of metabolic processes, the reason nearly all warm-blooded animals have temperatures within a narrow range despite drastic differences in environmental conditions. Over several decades, studies examining whether metabolism is related to body surface area or body weight (
Du Bois, 1936;
Kleiber, 1972), ultimately, converged on weight-dependent models (
Mifflin et al., 1990;
Schofield, 1985;
Nelson et al., 1992). Since US residents have increased in mass since the mid-19th century, we should have correspondingly expected increased body temperature. Thus, we interpret our finding of a decrease in body temperature as indicative of a decrease in metabolic rate independent of changes in anthropometrics. A decline in metabolic rate in recent years is supported in the literature when comparing modern experimental data to those from 1919 (
Frankenfield et al., 2005).
Although there are many factors that influence resting metabolic rate, change in the population-level of inflammation seems the most plausible explanation for the observed decrease in temperature over time. Economic development, improved standards of living and sanitation, decreased chronic infections from war injuries, improved dental hygiene, the waning of tuberculosis and malaria infections, and the dawn of the antibiotic age together are likely to have decreased chronic inflammation since the 19th century. For example, in the mid-19th century, 2–3% of the population would have been living with active tuberculosis (
Tiemersma et al., 2011). This figure is consistent with the UAVCW Surgeons' Certificates that reported 737 cases of active tuberculosis among 23,757 subjects (3.1%). That UAVCW veterans who reported either current tuberculosis or pneumonia had a higher temperature (0.19°C and 0.03°C respectively) than those without infectious conditions supports this theory (
Supplementary file 1). Although we would have liked to have compared our modern results to those from a location with a continued high risk of chronic infection, we could identify no such database that included temperature measurements. However, a small study of healthy volunteers from Pakistan—a country with a continued high incidence of tuberculosis and other chronic infections—confirms temperatures more closely approximating the values reported by Wunderlich (mean, median and mode, respectively, of 36.89°C, 36.94°C, and 37°C) (
Adhi et al., 2008).
Reduction in inflammation may also explain the continued drop in temperature observed between the two more modern cohorts: NHANES and STRIDE. Although many chronic infections had been conquered before the NHANES study, some—periodontitis as one example (
Capilouto and Douglass, 1988)— continued to decrease over this short period. Moreover, the use of anti-inflammatory drugs including aspirin (
Luepker et al., 2015), statins (
Salami et al., 2017) and non-steroidal anti-inflammatory drugs (NSAIDs) (
Lamont and Dias, 2008) increased over this interval, potentially reducing inflammation. NSAIDs have been specifically linked to blunting of body temperature, even in normal volunteers (
Murphy et al., 1996). In support of declining inflammation in the modern era, a study of NHANES participants demonstrated a 5% decrease in abnormal C-reactive protein levels between 1999 and 2010 (
Ong et al., 2013).
Changes in ambient temperature may also explain some of the observed change in body temperature over time. Maintaining constant body temperature despite fluctuations in ambient temperature consumes up to 50–70% of daily energy intake (
Levine, 2007). Resting metabolic rate (RMR), for which body temperature is a crude proxy, increases when the ambient temperature decreases below or rises above the thermoneutral zone, that is the temperature of the environment at which humans can maintain normal temperature with minimum energy expenditure (
Erikson et al., 1956). In the 19th century, homes in the US were irregularly and inconsistently heated and never cooled. By the 1920s, however, heating systems reached a broad segment of the population with mean night-time temperature continuing to increase even in the modern era (
Mavrogianni et al., 2013). Air conditioning is now found in more than 85% of US homes (
US Energy Information Administration, 2011). Thus, the amount of time the population has spent at thermoneutral zones has markedly increased, potentially causing a decrease in RMR, and, by analogy, body temperature.
Some factors known to influence body temperature were not included in our final model due to missing data (ambient temperature and time of day) or complete lack of information (dew point)(
Obermeyer et al., 2017). Adjusting for ambient temperature, however, would likely have amplified the changes over time due to lack of heating and cooling in the earlier cohorts. Time of day at which measurement was conducted had a more significant effect on temperature (
Figure 1—figure supplement 4). Based on the distribution of times of day for temperature measurement available to us in STRIDE and NHANES, we estimate that even in the worst case scenario, that is the UAVCW measurements were all were obtained late in the afternoon, adjustment for time of day would have only a small influence (
In summary, normal body temperature is assumed by many, including a great preponderance of physicians, to be 37°C. Those who have shown this value to be too high have concluded that Wunderlich’s 19th century measurements were simply flawed (
Mackowiak, 1997;
Sund-Levander et al., 2002). Our investigation indicates that humans in high-income countries have changed physiologically over the last 200 birth years with a mean body temperature 1.6% lower than in the pre-industrial era. The role that this physiologic ‘evolution’ plays in human anthropometrics and longevity is unknown.
OTHERS
A temperatura do corpo humano está esfriando?
Um novo estudo constata que a temperatura caiu, em média, nos últimos 150 anos.
Karen Weintraub on January 17, 2020
For the eLife study, she and her colleagues compared temperatures from three different data sets: a total of 83,900 measurements from the Union Army Veterans of the Civil War (UAVCW) cohort, collected between 1862 and 1930; 15,301 measurements from the National Health and Nutrition Examination Survey I (NHANES I), collected between 1971 and 1975; and 578,222 measurements from the Stanford Translational Research Integrated Database Environment (STRIDE), collected between 2007 and 2017. Figures for women were not available from the earliest data set but were collected from the two later cohorts, and the research showed that body temperature for men and women decreased steadily across the time periods.
Philip Mackowiak, an emeritus professor of medicine at the University of Maryland School of Medicine, who was not involved in the new study, says data from as far back as the Civil War is inherently suspect. “That’s not to say that what [the new study] found is not valid. It could be, but you just don’t know,” he says, because there are so many variables that could not be controlled for in the data set, such as whether soldiers and veterans were healthy when tested, where the thermometer was placed and what kind of instrument was used.
Even Wunderlich’s established 1851 result is questionable, Mackowiak says, because although he had a large database of patients, it is hard to know whether he measured temperature consistently or how he analyzed such a volume of information long before the invention of computers. And “the body is composed of a whole host of temperatures,” Mackowiak adds. The liver is the hottest part, and the surface of the skin is the coldest. Plus, he says, “there’s no ‘normal’ temperature;
there’s a range of temperatures,” with people running hotter later in the day than they do in the morning. Women also have higher temperatures on average than men, in part because they rise with ovulation.
Parsonnet agrees that the Civil War data set has some limitations, such as where caregivers took the temperatures and whether they were careful or simply filled in 98.6 degrees F because that’s what they knew normal temperature was supposed to be. Those concerns were tempered, she says, by the fact that she and her team found a similar annual drop in temperature between the 1970s cohort and the current one. The effect was still present when examined by the soldiers’ and veterans’ year of birth rather than when the temperature was obtained, suggesting that the type of thermometer or the caregiver’s attitude could not explain the change. And within the data set, the researchers found the expected variation by age, weight and height, suggesting that the values were not random.
Even with the data’s limitations, the findings are compelling, according to Frank Rühli, founding chair and director of the Institute of Evolutionary Medicine at the University of Zurich, who says he reviewed the paper for eLife but was not involved in the research. “Human body temperature data going back that far—roughly 150 years—is very interesting,” he says. “It allows us to see short-term alterations of physiological traits in humans, which is quite rare.”
All the experts agree on one thing:
a fever is still a fever. Lowering the average for normal body temperature does not mean that the standard for a fever—generally considered more than 100 degrees F for adults—should be changed, Mackowiak says. “Temperature can be helpful in determining whether or not you’re ill and, based on its level, how ill you might be,” he says. For patients, a bacterial infection plus a lower than normal temperature could be an even more ominous sign than a higher than normal one, he says. Following a rise or fall in temperature can also indicate whether you are getting better or how you are responding to medication, he adds, though “how you feel is the most important thing.”
The new study probably should not change the definition of fever, Rühli says. “But the variety of what is looked at as being normal should probably be adjusted.”