Porotic Hyperostosis: A New Perspective PATTY STUART-MACADAM Department ofdnthropology, University of Toronto, Toronto, Ontario M5S 1A1, Canada

KEY WORDS stress markers

Anemia, Cribra orbitalia, Pathogen load, Skeletal

ABSTRACT Porotic hyperostosis is a paleopathologic condition that has intrigued researchers for over a century and a half. It is now generally accepted that anemia, most probably an iron deficiency anemia, is the etiologic factor responsible for lesion production. Although there can be a number of factors involved in the development of iron deficiency anemia, a dietary explanation has often been invoked to explain the occurrence of porotic hyperostosis in past human skeletal populations. In fact, porotic hyperostosis has been referred to as a “nutritional” stress indicator. Traditionally those groups with a higher incidence of porotic hyperostosis have been considered to be less successful in adapting to their environment or more nutritionally disadvantaged than other groups. A new perspective is emerging that is challenging previous views of the role of iron in health and disease, thus having profound implications for the understanding of porotic hyperostosis. There is a new appreciation of the adaptability and flexibility of iron metabolism; as a result it has become apparent that diet plays a very minor role in the developmentof iron deficiency anemia. It is now understood that, rather than being detrimental, hypoferremia (deficiency of iron in the blood) is actually an adaptation to disease and microorganism invasion. When faced with chronic andlor heavy pathogen loads individuals become hypoferremic as part of their defense against these pathogens, thus increasing their susceptibility to iron deficiency anemia. Within the context of this new perspective porotic hyperostosis is seen not as a nutritional stress indicator, but as a indication that a population is attempting to adapt to the pathogen load in its environment. Progress in science occurs by a number of means, including the development of new techniques of investigation, the accumulation of data, and the gradual development of thought based on the work of numerous researchers. However, one of the most vital means of scientific progress is the application of new perspectives-that is, the introduction of novel frameworks, concepts, or ideas. New perspectives applied to existing data promote new insights and pave the way for new directions of thought and research. The present paper explores the development of thought with regard to a paleopathologic condition, porotic hyperostosis, and illustrates how the emergence of a new perspective can have a profound impact on the per-


ception of and understanding of this condition. Porotic hyperostosis is a paleopathologic condition that has intrigued researchers for over a century and a half. The skull vault, particularly the frontal, parietal, and occipital bones, as well as the orbital roof are affected. Macroscopically what is evident is a number of small holes of varying size and distribution that penetrate the outer compact bone of the skull. This corresponds with an increase in the middle table of bone, or diploe, and a thinning of the outer table of bone. Microscopically the spaces between bone trabeculae are enlarged and open Received July 25,1990; accepted June 20,1991,



widely onto the bone surface. Radiographically there are a number of changes: on the horizontal plates of the frontal bone (orbital roof)there is an increase in thickness seen in lateral views, and alterations of the orbital rim on anterior-posterior views, while on the skull vault thinning and/or disappearance of the outer compact bone, increased granularity, an increase in the middle table of bone, and sometimes a “hair-on-end” pattern of trabeculation are seen (Stuart-Macadam, 1982,1987). The literature pertaining to this condition abounds with views concerning etiology and terminology. Just a few of the names that have been suggested are “symmetrical osteoporosis” (Hrdlicka, 1914), “spongy hyperostosis” (Muller, 1935), and “external cribra cranii” (Koganei, 1912). Suggestions for etiology have ranged from the effects of carrying water jugs on the head (Wood-Jones, 1910), a toxic disorder (Hrdlicka, 1914), a racial trait (Welcker, 18881,or dietary problems (Williams, 1929). Owen (18591, who was one of the first to comment on the condition, said that a skull from Nepal with the lesions “is chiefly remarkable as exemplifying the rare disease of hypertrophous thickening of the parietal bones.” In 1924 Morant attributed lesions on the same skull to a “hypertrophy,osteitis, acrocephaly or a more specific but unknown pathological state.” The concensus at present favors the terms “porotichyperostosis” (after Angel, 1966) for lesions of either the vault or orbit, or “cribra orbitalia” (after Welcker, 1888)for lesions of the orbit. Researchers now feel that porotic hyperostosis is the result of an anemia and, in the majority of populations, most probably an acquired iron deficiency anemia. This is not to say that the genetic anemias such as thalassemia and sickle cell anemia did not occur in the past, but that their relatively low incidence in populations would not account for the high frequency of porotic hyperostosis seen in populations from many geographic areas and time periods (StuartMacadam, 1982,1990). Iron deficiency anemia can be defined as a reduction below normal in levels of hemoglobin and hematocrit (packed red cell volume) in blood. This can occur for a variety of reasons including blood loss, accelerated demands as a result of factors such as growth or pregnancy, inadequate absorption of iron, and nutritional deficiencies (Robinson, 1972).However, since Williams first put for-

ward the suggestion in 1929 anthropologists have emphasized a dietary explanation for the occurrence of porotic hyperostosis (hence anemia) in the archaeological record. In fact, porotic hyperostosis has often been referred to as a nutritional stress indicator (Armelagos, 1990; Goodman et al., 1988; Huss-Ashmore et al., 1982; Mensforth et al., 1978; Martin et al., 1985). It is true that the term nutrition encompasses more than just diet; the problem is that this has not been made explicit in discussions of porotic hyperostosis and as a result the assumption has often been made that diet is of paramount importance. However, it is easily understood how porotic hyperostosis could be interpreted in this manner. For example, there appears to be a strong correlation between the occurrence of porotic hyperostosis and both the introduction of ‘cereal grains in the Neolithic (Cohen and Armelagos, 1984), and subsistence on cereal grains, particularly maize. Cereal grains contain phytates, which can inhibit the absorption of dietary iron by the intestine. El-Najjar (1976), El-Najjar and Robertson, (19761, and El-Najjar and colleagues (1975, 1976, 1982) popularized the “maize dependency” hypothesis, which stressed that porotic hyperostosis was most common in groups that had a high proportion of maize in their diet. Since that time there has been a greater appreciation of the complexity of the story (Lallo et al., 1977; Mensforth et al., 1978; etc.), but diet is still invoked as a factor in almost every discussion of porotic hyperostosis (exceptions are Kent, 1986; StuartMacadam, 1988,1989,1990). The dietary hypothesis fit the data well enough in the past, but now new data, and more importantly a new perspective, have emerged which shed a different light on porotic hyperostosis. The new perspective involves a reappraisal of the role of iron in health and disease. There is a greater appreciation of the flexibility and complexity of iron absorption by the intestine and a new understanding of the adaptive features of iron metabolism. It is now known that iron plays an important role in the defense system of the human body. Two important points have emerged as a result: 1. Except in cases of outright malnutrition, diet plays a minor role, if any, in the development of iron deficiency anemia. 2. Mild iron deficiency, or hypoferremia, is



1988; Strauss, 1978) have written on the mechanism of iron withholding and its advantages in the face of micro-organism invasion. Many micro-organisms require iron for The data to support these contentions their own replication, yet lack their own have accumulated in the medical literature stores. They rely on supplies of iron that they over a number of years. Wadsworth (see can obtain from the host with their own 1975 review) was one of the first researchers manufactured iron-chelators. The human to deemphasize the importance of diet in the body is able to minimize the iron available to development of iron deficiency anemia. He micro-organisms by decreasing serum iron, noted that many studies showed absolutely which is more readily available t o microno correlation between dietary intake of iron organisms, and decreasing absorption of diand presence or absence of iron deficiency etary iron by the intestinal mucosa. Serum anemia. Davidson et al. (1933) also noted iron is decreased by binding the available that in a large population of individuals from iron to the transport protein, transferrin, or Aberdeen there were no obvious differences sending it into storage in the reticuloendoin iron consumption between those who de- thelial system. A short-term reduction in veloped iron deficiency anemia and those absorption of dietary iron does not comprowho did not. Arthur and Isbister (1987) state mise iron metabolism because there is still that “even if iron intake was reduced to nil, ample iron available from the destruction of which is virtually impossible even with the old red blood cells. In fact, iron metabolism is most frugal diets, it would still take at least almost a closed system with as much as 90% two to three years to develop iron deficiency of the iron required for the production of new anemia, and probably even longer because red blood cells being obtained by the turnlosses would decline as levels declined.” In over of senescent red blood cells. There are in vivo, in vitro, and population addition, as iron levels in the diet decrease, the proportion absorbed increases (Wads- studies that support the concept that being iron deficient is an advantage during expoworth, 1990). The fact is that the intestine is capable of a sure to many disease organisms, including a wide range of levels of absorption of iron number of bacteria, fungi, and parasites. In from the same diet, depending on factors the past thirty years, several hundred studsuch as age, sex, physiological status, and ies on animals and a number on humans disease status. Studies have shown that iron have shown that hosts whose iron withholdabsorption from an adequate diet can vary ing system is compromised are at increased from a fraction of a milligram to as much as 3 risk of infection (Weinberg, 1990). Several or 4 milligrams a day, depending on body dozen reports have shown that strengtheniron content. For example, hyperferremia, or ing the iron withholding system results in iron overload, is associated with a decrease decreased risk of infection (see reviews in in absorption of iron from the diet. When an Weinberg, 1974,1978,1984). Iron withholdincreased supply of iron is needed by the ing is also associated with conditions such as body, the levels of intestinal absorption can inflammation and neoplasia, and seems to increase concomitantly. This is particularly be a generalized stress response. The data the case with women and children, who have are not always clear-cut, and the concept is much greater physiological needs for iron still controversial, but the evidence increasthan men. Studies have shown that 5-10% of ingly supports the concept of iron withholddietary iron is absorbed by healthy Western ing as a positive, adaptive response to invadadult males, whereas as much as 25% is ing micro-organisms. Data from the anthropological literature absorbed by iron deficient adults (Arthur and Isbister, 1987). The same flexibility oc- can also provide support for the concepts of curs with iron loss; normal males lose ap- diet being a minor factor in the development proximately .9 milligrams per day and hy- of iron deficiency anemia and the occurrence perferremic males lose about 2 milligrams of iron deficiency being a defense against micro-organisms. If the occurrence of porotic per day (Finch, 1989). Weinberg (1974, 1977, 1978, 1984, 1990) hyperostosis is examined through time and and others (Bullen and Griffiths, 1987;Crosa, space three major trends are apparent: tem1987;Griffiths and Bullen, 1987; Kluger and poral, geographic, and ecological (StuartBullen, 1987; Martinez et al., 1990; Payne, Macadam, 1990). Porotic hyperostosis is

not necessarily a negative condition; in fact it is one of the body’s defenses against disease.



very uncommon before the Neolithic period (Angel, 1978; Meiklejohn et al., 1984; Kennedy, 1984). The frequency then increases during the Neolithic (Angel, 1978)or with the adoption of agriculture (Lallo et al., 1977; Cohen and Armelagos, 1984). Although the picture becomes very complex, there does appear to be a general reduction in prevalence towards the 20th century (Angel, 1978; Hengen, 1971; Henschen, 1961). Porotic hyperostosis occurs in skeletal collections from every country and continent, but Hengen’s analysis of over 5,000 skulls shows that the closer the country of origin is to the equator, the greater the incidence of porotic hyperostosis. Porotic hyperostosis occurs more frequently in individuals from lowland or coastal sites than those from highland sites. This has been observed by a number of researchers including HrdliEka (1914), ElNajjar et al. (19761, Ubelaker (19841, and Angel (1972). What clues do these trends provide about the picture of anemia in the past? First, it is unlikely that dietary differences alone could account for these broad trends in time, space, and ecology. Even though the prevalence of porotic hyperostosis does increase with the introduction of agriculture, closer analysis of the data shows that groups with a heavy reliance on agriculture (hence cereal grains) have a varying prevalence of porotic hyperostosis, as do groups that are known to rely more heavily on animal protein food sources. For example, Ubelaker (1984) found little porotic hyperostosis in an Ecuador highland site where there was intensive agriculture, and in some areas in North America where maize and cereal grains were intensely cultivated, porotic hyperostosis has been found in only a few individuals (Larsen, 1987). However, Walker (1986)found a high prevalence of porotic hyperostosis in a group from the Santa Barbara Channel Islands having an iron-rich marine diet. The data also show that both proximity to the equator and altitude correlate with incidence of porotic hyperostosis regardless of subsistence base. If diet is not the major etiological factor in porotic hyperostosis, then what is? Consideration of the trends in occurrence of porotic hyperostosis and the new perspective suggests that a different factor, pathogen load, is much more critical in the development of anemia in past populations. Pathogen load refers to the total number of micro-organisms in the local environment, including fungi, viruses, bacteria, and parasites. This,

in turn, is dependent on innumerable factors such as climate, geography, topography, population size and density, hygiene, food resources, seasonality, customs, and subsistence patterns. Pathogen load can have both direct and indirect effects on the iron status of individuals. The direct effects are evident when an individual develops anemia as a result of pathogens that are responsible for blood loss or the destruction of red blood cells. For example,the malarial parasite invades the red blood cell and causes its premature destruction. The hookworm parasite (either Ancylostoma duodenale or Necator americanus)attaches directly onto the small intestine and can result in anemia through chronic blood loss. The indirect effects are evident when an individual contracts either an acute or chronic disease. In the case of many acute diseases, the body becomes temporarily hypoferremic as part of its defense system. In this case, iron absorption from the diet is decreased, serum iron is bound to the iron-transporting protein, transferrin, and excess iron is taken into storage. With chronic diseases there is often an associated anemia; again this is probably associated with attempts on the part of the body to defend itself against pathogens. Anemia of chronic disease is one of the most common forms of anemia, and is associated with a number of diseases that would have affected past populations, such as chronic mycotic infections, tuberculosis, and osteomyelitis. Pathogen load being a major factor in the development of porotic hyperostosis satisfactorily explains the observed trends through time and space. The increase in porotic hyperostosis during the Neolithic and with agriculture is a function not of iron-poor diets, but of increased sedentism, aggregation, and population density which resulted in greater exposure to pathogens. A decrease in porotic hyperostosis towards the 20th century could be explained by improvements in sanitation and hygiene. The increase in porotic hyperostosis with increasing proximity to the equator reflects the increased viability of many micro-organisms with warm, humid conditions. A decrease with altitude is associated with less favorable conditions for pathogens. New data from anthropological studies also support the concepts that diet does not play a major role in the incidence of porotic hyperostosis and that pathogen load is a critical factor in the story of anemia in the past. Reinhard (1990) analyzed coprolites


from some of the same Southwest Anazasi Indian sites that El-Najjar et al. (1976) used to generate their “maize dependency” hypothesis. On the basis of that data Reinhard could find no relationship between maize consumption and the occurrence of porotic hyperostosis. He did, however, find a very high correlation between pinworm prevalence in coprolites and porotic hyperostosis, which he felt provided evidence for a relationship with microparasitism (protozoal, bacterial, and viral infection). Ubelaker (1990) has obtained data on a range of sites in Ecuador within a broad, complex culturaltemporal framework that includes coastal and highland sites spanning nearly 8,000 years. He found no evidence for porotic hyperostosis in earlier sites (i.e., hunting and gatheringhorticulture) or in highland areas, but found that porotic hyperostosis was confined to skeletal material from relatively recent coastal sites. These sites do not appear to be associated with an iron-poor diet as there is evidence for a heavy reliance on oysters and clams, and utilization of reptiles, birds, deer, and rodents. Ubelaker found that evidence for porotic hyperostosis in Ecuador loosely follows a temporal trend, but does not correlate closely with increasing time or reliance upon maize agriculture. The idea that environmental and cultural conditions could have an important affect on anemia in the past is not a new one. Hengen (1971) was probably the first to suggest this when he said: Changes in the hygienic conditions and of the incidence of iron deficiency anemias in former times depended without doubt largely on deviations of the climate, differences in the habits of daily life, procuring and preparation of food, types of housing, keeping of domestic animals, disposal of excrement and so on.

Other researchers have touched on this issue, but even so, diet has been considered t o be an important etiological factor in producing porotic hyperostosis in most studies. The time has come for diet to be de-emphasized as a factor and pathogen load to be emphasized. The complex interaction between environmental and cultural factors that is involved in generating pathogen load in any one population can be appreciated from a study by Dunn (1972). Dunn surveyed the prevalence and density of intestinal parasitism in Malayan aborigines inhabiting the southern Malay peninsula. A great diversity


of habitat and culture was represented as villages are found in a variety of ecosystems including primary forest, secondary forest or scrub vegetation, or near rubber estates and large towns. Dunn was able to compare parasitism between those aborigines who had left their traditional forest environment and those who were still forest dwellers and subsistence cultivators. Dunn examined the relationships among cultural-ecological groups, sanitation, and intestinal parasitism. Sanitary status was estimated for each group by considering not only the excreta and rubbish disposal practices but also a number of other environmental and cultural variables that interacted with sanitary behavior t o produce different sanitary conditions. These were:

1. Population density and crowding: the larger and denser the population, the more heavily contaminated were their living conditions. 2. Land availability around the village: large tracts of land around the village minimized contamination. 3. Community mobility: the greater the mobility of the community, the cleaner the environment. 4. Subsistence: agriculturalists had more contact with the land and a greater chance of being exposed to soil pathogens. 5. House style: ground level housing as opposed to pile housing meant a greater chance of exposure to pathogens. 6. Domestic animals: these animals can act as scavengers and reduce environmental contamination. 7. Helminth viability: at cooler, higher elevations the viability of helminth eggs is reduced.

When villages were assessed for overall sanitary status they ranged from fairly good to poor. When Dunn examined the prevalence and abundance of intestinal parasites he found a general correspondence between the sanitary score and the intestinal burden. The lower the sanitary assessment the heavier the intestinal burden. Unfortunately there was no information on differences in the iron status among these groups. It was mentioned that severe anemia is rare in Malayan aborigines but that marginal anemia is common and seemed to be the product of a group of contributory factors (including hookwork and perhaps Trichuris) that vary in relative importance from one



cultural-ecologicalsetting to another (Dunn, 1972). Dunn noted that the number of species of parasite was closely related to the complexity of the ecosystem; the greater the complexity, the greater the number of species of parasite. For example, the Negritos, who subsisted on hunting and gathering and fishing in the complex ecosystem of the Malayan rain forest, had more species of intestinal parasite than any other ethnic group. Where that ecosystem was simplified by settlement and cultivation some species of human parasite that depend on intermediate hosts disappeared because they could not adapt. However, the more adaptable parasites, such as Ascaris, Trichuris, Giardia, and Entamoeba histolytica became much more successful in terms of prevalence and intensity. DISCUSSION

The acceptance of the two concepts, that diet is of little importance in the development of iron deficiency anemia, and that iron deficiency is an adaptive response to stress, has a profound effect on the interpretation of porotic hyperostosis. In the past a high prevalence of porotic hyperostosis in a population has often been interpreted to mean a diet low in iron or bioavailable iron, even if other factors were considered to be operative. Porotic hyperostosis has also been interpreted to be indicative of maladaptation. However, viewing porotic hyperostosis in the light of the new perspective provides alternative interpretations. First, it suggests that a high incidence in a group is indicative of a heavy pathogen load in the environment of that group, for whatever reason. Secondly, it suggests that as part of their attempt to adapt, those individuals with porotic hyperostosis have gone into the iron-deficiency mode, where dietary absorption of iron is inhibited and serum iron decreased, making it more difficult for pathogens to obtain the necessary iron for growth and development. When this happens, the amount of iron in the diet is irrelevant; absorption of iron by the intestine will still be diminished. The hypoferremic situation could be prolonged because of high levels of andor chronic exposure to microorganisms, and iron deficiency anemia would ensue, stimulating the formation of new red blood cells, and increasing the size of the marrow (marrow hyperplasia) to produce the bone changes known as porotic hyperostosis. These lesions probably devel-

oped exclusively in childhood when the bone is particularly susceptible to alterations associated with anemia (Stuart-Macadam, 1985). There is a real problem in attempting to ascertain blood measures (i.e., the severity of anemia) from skeletal changes. There does not appear to be any consistency between the severity of the clinical disease and the severity of the skull changes. Caffey (1951) has documented cases of patients of the same age and with similar clinical and hematological findings who show very different degrees of skull change. This appears to be the result of individual variability, perhaps associated with differences in amount and distribution of hematopoietic (red) marrow in the skull. Severity of bone change as well as distribution of bone change can be affected. Some individuals develop changes of the vault only, some the orbit only, or sometimes changes are more pronounced in one area of the vault than another (Caffey, 1937; McAfee, 1958; Middlemiss, 1961). Acceptance of the new perspective dramatically alters the way porotic hyperostosis can be perceived with respect to the interaction of a population and its environment. Porotic hyperostosis does not indicate a diet that is low in iron or bioavailable iron and so cannot be called upon t o provide information about the dietary status of a population. It is not just an indicator of nutritional stress. It certainly is an indicator of stress; however, the stress that is more often involved is the pathogen load encountered by a population. The occurrence of porotic hyperostosis reflects the attempts of that population to cope with and adapt to its environment. It suggests that there was a primary response of iron withholding as an adaptation to disease and/or pathogen load, followed by the development of iron deficiency anemia as the threshold between hypoferremia and anemia was surmounted. This would occur particularly when other factors such as physiological status (for example, pregnancy), growth requirements, blood loss (as in parasitic infestation), or in rare cases diet, tipped the balance. It could be said that chronic hypoferremia is an evolutionary response to persistent microbial invasion (Kent and Weinberg, 1989; Sturat-Macadam 1988). Populations that were chronically exposed to heavy pathogen loads have adapted by lowering their iron status, resulting in an increased susceptibility to iron deficiency anemia. Rather than being seen as a sign of



weakness or maladaptation, porotic hyperostosis should be viewed as a sign that the population is attempting to adapt to adverse environmental conditions. The term adaptive must, of course, be considered in context. What is adaptive in one situation or environment may not be in another. This is certainly true in the case of hypoferremia and so porotic hyperostosis must always be viewed in the light of human iron metabolism and body physiology. The critical feature of human iron metabolism is conservation; there is a fine line between too much and too little. The body is constantly striving to maintain a balance. Too little iron can be associated with severe anemia which impairs the quality of life and can eventually lead to a failure of the cardiac and respiratory systems, while too much iron can produce fibrotic scarring, and eventual failure of several organs, including the liver, pancreas, heart, and endocrine system (Cook, 1990). The immune system is compromised in both situations, either from too much iron or too little. In between the more obvious extremes there is a grey area which is more ambiguous; some studies suggest detrimental effects while others argue against them. For example, some studies (Aukett et al., 1986; Pollitt, 1989, Pollitt et al., 1989) suggest that mild iron deficiency may affect mental achievement. However, the presence of parasitic infestation was a confounding factor in one study by Pollitt (1989).Dallman (1989) and Wadsworth (1990) suggest that an overall improvement in nutrition could have been associated with improved mental facilities. Apparently ingestion of oral iron stimulates the appetite and those children in the study by Aukett et al. who showed improved mental development with increased hemoglobin levels also gained weight. So it is possible that the increase in calories and other nutrients could also have affected mental achievement. There is epidemiological evidence that suggests that anemia during pregnancy is associated with an increased risk to the fetus; however, the data are far from conclusive (Dallman, 1989). It is well documented that iron deficiency impairs work performance and exercise capacity (Dallman, 1989).When the body is at rest the cardiovascular and metabolic effects of mild iron deficiency anemia are barely detectable, but with agricultural work and standardized exercise, tachycardia and lactic acidosis develop. These data indicate that there are cer-

tainly negative aspects of iron deficiency, and this must always be considered when talking about adaptation. However, in an area of endemic disease or very high pathogen load the problems associated with iron deficiency may be minor compared with the morbidity and mortality associated with severe bacterial disease. In a different environment, one with low pathogen load and few diseases, the negative effects of iron deficiency would loom larger. In terms of human evolutionary history, hypoferremia would have been advantageous in times and places where the diseaselpathogen load was heavy. Then it would be expected that iron deficiency anemia would occur with the most frequency. It is precisely this pattern which occurs in the archaeological record with respect to porotic hyperostosis. For example, porotic hyperostosis occurs with greater frequency in lowland areas compared with highland, in tropical areas compared with temperate, and in areas of greater population density. However, as it has been aptly pointed out (Mensforth et al., 1978; Lallo et al., 1977)the etiology of porotic hyperostosis is not simplistic but can best be understood in terms of synergistic interactions. It is incorrect to focus exclusively on any one factor in terms of an explanatory model. However, with respect to porotic hyperostosis the emphasis has traditionally been on diet to the exclusion of andlor neglect of other factors. This paper attempts to redress the balance by illustrating that new perspectives can lead to different interpretations of the same data. The story of porotic hyperostosis is not yet complete, but perhaps some new pages have been written. ACKNOWLEDGMENTS

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Porotic hyperostosis: a new perspective.

Porotic hyperostosis is a paleopathologic condition that has intrigued researchers for over a century and a half. It is now generally accepted that an...
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