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 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 development of 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 and/or 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.     

The causes of porotic hyperostosis and cribra orbitalia: A reappraisal of the iron‐deficiency‐anemia hypothesis

Porosities in the outer table of the cranial vault (porotic hyperostosis) and orbital roof (cribra orbitalia) are among the most frequent pathological lesions seen in ancient human skeletal collections. Since the 1950s, chronic iron‐deficiency anemia has been widely accepted as the probable cause of both conditions. Based on this proposed etiology, bioarchaeologists use the prevalence of these conditions to infer living conditions conducive to dietary iron deficiency, iron malabsorption, and iron loss from both diarrheal disease and intestinal parasites in earlier human populations. This iron‐deficiency‐anemia hypothesis is inconsistent with recent hematological research that shows iron deficiency per se cannot sustain the massive red blood cell production that causes the marrow expansion responsible for these lesions. Several lines of evidence suggest that the accelerated loss and compensatory over‐production of red blood cells seen in hemolytic and megaloblastic anemias is the most likely proximate cause of porotic hyperostosis. Although cranial vault and orbital roof porosities are sometimes conflated under the term porotic hyperostosis, paleopathological and clinical evidence suggests they often have different etiologies. Reconsidering the etiology of these skeletal conditions has important implications for current interpretations of malnutrition and infectious disease in earlier human populations. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Porotic hyperostosis in a marine-dependent California Indian population

A maize-based iron- and protein-deficient diet is commonly cited as the most important cause of porotic hyperostosis among American Indian agriculturalists. An alternative to this maize dependence hypothesis is suggested by the analysis of 432 crania from the nonagricultural, fish-dependent population of the Channel Island area of southern California. Cribra orbitalia, a form of porotic hyperostosis associated with iron deficiency anemia, is just as common among these fisherpeople, whose diet was rich in iron and essential amino acids, as it is among maize-dependent agriculturalists. Northern Channel Island crania have much more cribra orbitalia than those from the California mainland. The highest incidence is on San Miguel, a small geographically isolated island with a shortage of fresh water and terrestrial resources. The Indians who lived on Santa Cruz, the largest of the northern Channel Islands with the greatest diversity of terrestrial plants and animals, have less cribra orbitalia than those who lived on Santa Rosa or San Miguel Island. This geographical distribution appears to be explained by island-mainland and interisland differences in water contamination, exposure to fish-borne parasites, and nutritional adequacy of the diet. The prevalence of porotic hyperostosis in a population with a heavy dietary dependence on marine resources shows that among prehistoric American Indians, this condition is not always associated with an iron- and protein-deficient diet of cultigens. It seems likely that high nutrient losses associated with diarrheal disease are often more significant in the etiology of porotic hyperostosis than a low dietary intake of essential nutrients.     

Porotic hyperostosis: representative of a childhood condition

Porotic hyperostosis is currently considered to be one of several stress markers available for assessing the health and nutritional status of past human populations. The present study questions one of the basic assumptions underlying its use; that is, that the occurrence of porotic hyperostosis in an individual represents an episode of anemia that was current or had occurred within a relatively short period prior to death. A synthesis of data from a Romano-British site Poundbury Camp, anthropological and clinical studies, and information on bone physiology suggests that lesions of porotic hyperostosis seen in adults are most probably representative of a childhood episode of anemia. Lesions seen in adults are the result of bone changes occurring in the growth period that have not undergone complete remodelling. This viewpoint has implications for future interpretation of data on porotic hyperostosis obtained from skeletal collections.     

河南渑池笃忠遗址仰韶晚期出土的人骨骨病研究

本文对河南省渑池笃忠遗址仰韶晚期灰坑出土人骨的骨病做了详细的观察.在牙病方面.对龋病、牙周病、牙釉质发育不全等情况做了记录和分析,应用两样本率差异的x2检验,比较了龋病在性别、年龄的差异.研究结果表明,笃忠组龋病的患齿率性别差异不显著,与年龄变化也没有明显的关系.此外,笃忠组人骨标本中还观察到错(牙合)畸形、骨瘤、退行...     

山东广饶县中南世纪城墓地出土明代人骨的初步研究

本文对广饶县中南世纪城墓地出土的明代人骨进行了多方面的生物考古学研究,包括性别、年龄的分布,身高的复原以及古病理的观察。牙病方面,对龋病、牙釉质发育不全和错(牙合)畸形进行了观察记录,从性别、年龄、龋患程度及好发牙位等方面对该人群的龋患情况进行统计分析。研究结果表明,该人群牙齿患龋率不具备明显的性别差异,与年龄变化也无显著相关性,好发牙位多为臼齿。此外,还观察到多孔性骨肥厚、骨关节疾病等病理现象以及一处愈合较好的骨折创伤。     

Anemia and childhood mortality: latitudinal patterning along the coast of pre-Columbian Peru

Hrdlicka ([1914] Smithson. Inst. Misc. Collect. 61:1-69) reported that pre-Columbian skeletal material from the coastal lowland Andean region exhibited a high frequency of porotic hyperostosis, a pathological condition of bone that generally is thought to indicate childhood anemia. While subsequent studies tended to reinforce this conclusion, factors implicated in the condition have yet to be fully explored in the region as a whole. This study explores regional and intravalley variation as one step in establishing biocultural variables that increase the apparent risk of childhood anemia. The study sample includes 1,465 individuals: 512 from Peruvian collections housed at the Field Museum of Natural History, and 953 from systematically excavated contexts from Moquegua, Peru. Environmental stressors, such as parasites and disease, rather than specific dietary practices were found to be more likely associated with childhood anemia in these coastal Andean samples. The study supports cribra orbitalia as an earlier expression of porotic hyperostosis and suggests that porotic hyperostosis, as recorded here, cannot be easily dismissed as a result of cranial shape modification. No clear temporal patterns were observed. Finally, the study establishes that comparing data for children and adults can reveal the relative association between childhood anemia and mortality. Childhood mortality associated with anemia was elevated where the presence of tuberculosis or tuberculosis-like conditions was more common and the presence of water-borne pathogens was negligible. In contrast, those buried at lower altitudes, closer to the coast, and consuming mainly marine resources were less likely to die in childhood with anemia than in the other contexts studied.     

Porotic Hyperostosis and Paleoepidemiology: A Forensic Perspective on Anemia among the Ancient Maya

Porotic lesions caused by childhood anemia are commonly found on ancient Maya crania and have been cited as evidence for extremely poor nutrition during the Classic Period. We reconsider this characterization in the light of recent data on childhood anemia in rural Guatemala and the prevalence of porotic hyperostosis in crania of forensic skeletal remains of rural highland Maya from Plan de Sanchez, Baja Verapaz, which date to 1982. The abundance of porotic hyperostosis in adults from Plan de Sanchez fits well with the number of modern rural children suffering from anemia, but the lesions are very rare compared to archaeological series. Although some minor change in diet and infection may contribute to differences in porotic hyperostosis, it is likely that higher mortality leads to fewer anemic lesions in modern adult crania. We hypothesize that more anemic children survived to adulthood in the past than do today, [iron-deficiency anemia, porotic hyperostosis, Maya, nutrition, forensic anthropology, osteological paradox]     

Patterns of anemia and infection from medieval York,England

An assessment of the presence and patterns of porotic hyperostosis and periosteal reactions in the skeletal population (n = 1,014) from St. Helen-on-the-Walls, York, are used to examine health and disease in urban medieval England. The analyses of these two lesions indicate that 58% of the population display evidence of porotic hyperostosis and that 21.5% of the population display periosteal reactions. Through differential diagnosis it is asserted that porotic hyperostosis is associated with iron-deficiency anemia, and that periosteal reactions may be the result of endemic treponematosis and/or non-specific infection, including parasitic infestation. An association between the presence of remodeled lesions and adulthood is noticeable for both porotic hyperostosis and periosteal reactions, as is a pattern of increased average age at death for those displaying both conditions. © 1993 Wiley-Liss, Inc.     

Recognition of sickle cell anemia in skeletal remains of children

The present study discusses in detail the osteological changes associated with sickle cell anemia in children and their importance in differential diagnosis. Posterior calcaneal and specific articular surface disruptive metacarpal lesions are diagnostic for sickle cell anemia. Calvarial thickening, tibial and femoral cortical bone thickening, and bowing are of more limited utility in differential diagnosis. Granular osteoporosis, pelvic demineralization and rib broadening are nonspecific. Localized calvarial “ballooning,” previously not described, may have diagnostic significance. Bone marrow hyperplastic response (porotic hyperostosis) in sickle cell anemia produces minimal radiologic changes contrasted with that observed in thalassemia and blood loss/hemolytic phenomenon. Two other issues, the osteological criteria for discriminating among the anemias and the purported relationship between porotic hyperostosis and iron deficiency anemia, are also discussed. There is sufficient information to properly diagnose the four major groups of anemias, and further, to establish that iron deficiency is only indirectly associated with porotic hyperostosis. The hyperproliferative bone marrow response (manifest as porotic hyperostosis) to blood loss or hemolysis exhausts iron stores, resulting in secondary iron deficiency. Am J Phys Anthropol 104:213–226, 1997. © 1997 Wiley-Liss, Inc.     

A radiographic study of porotic hyperostosis

Skull lesions known as porotic hyperostosis have been of interest to researchers since the mid-19th century. The etiology of porotic hyperostosis has long been a matter for speculation yet there has never been complete acceptance or substantiation of any one of the many theories proposed. Today the most widely accepted theory suggests that anemias of either acquired or genetic origin are responsible for porotic hyperostosis. The present study tests this hypothesis using criteria which were chosen after the examination of clinical radiographs of patients with various types of anemia. These criteria are: the presence of “hair-on-end” trabeculation, outer table thinning, texture changes, diploic thickening, orbital roof thickening, orbital rim changes, and the underdevelopment of frontal sinuses. A comparison of these criteria from the clinical X-rays with X-rays of skulls with porotic hyperostosis provides a more rigorous, repeatable, and standardized method upon which to base a diagnosis. This approach enables radiography to provide the necessary link between the clinical and anthropological with which to investigate the origin of porotic hyperostosis.     

Amino acid analysis of bone from a possible case of prehistoric iron deficiency anemia from the American southwest

It is possible that dietary conditions can result in the production of abnormal bone protein. For example, a heavily maize-dependent diet could be deficient in one or more essential amino acids necessary to normal human biochemistry and consequently necessary for normal bone protein synthesis. Amino acid analysis of bone tissues, thus, could provide a useful diagnostic tool in paleopathology. To test this potential we have compared the amino acid analyses of bone samples from a prehistoric Southwest Indian child exhibiting porotic hyperostosis with samples taken from (1) two children's skeletons lacking bone lesions but from the same area and time, (2) a modern child who died from accidental causes, and (3) adult human compact bone. Analytical results of the nonpathological prehistoric specimens were virtually identical to that of the modern infant, indicating remarkable preservation of bone protein. The pathological bone sample differed from the three control specimens by having as much as 25% less of those amino acids containing hydroxyl group and acidic side chains. We interpret the amino acid profile for the diseased child as indicating the presence of a greater proportion of helical protein (or less noncollagenous protein) as well as a lowered degree of hydroxylation of proline and lysine. One explanation for our data is that protein biosynthesis is altered in the child exhibiting porotic hyperostosis, and either some proteins important in the early phases of mineralization are not produced in sufficient quantity, or some necessary enzyme cofactors (e.g., dietary ferrous ions) are missing. We conclude that our data are compatible with, but do not prove, the hypothesis that the porotic hyperostosis exhibited by the Southwest Indian child is the result of iron deficiency anemia.     

Porotic hyperostosis: new evidence to support the anemia theory

The etiology of skull lesions known as porotic hyperostosis has long been a matter for speculation. The most widely accepted theory at present suggests that an anemia, either acquired or genetic, is responsible for lesion development. However, acceptance of this theory is not universal and the nature of the relationship between orbital and vault lesions remains a controversial issue. This paper provides a much broader field of supportive evidence on which to base the anemia theory. This involves a synthesis of information from the clinical and anthropological literature as well as new data from two skeletal collections: Poundbury Camp, a Romano-British series, and the Hodgson collection, a 19th century East Asian series. A comparison is made between clinical and anthropological data at the macroscopic, microscopic, radiographic, and demographic levels of analysis. This approach reveals the similarities in expression between clinically diagnosed anemias and porotic hyperostosis.     

A radiographic technique of interest to physical anthropologists

A radiographic technique for processing a large number of human crania was developed to aid in the diagnosis of porotic hyperostosis in a large skeletal population. These images are made directly onto photographic paper, thereby reducing costs and increasing the rate of processing. The technique is especially well suited for radiographing human skeletal material and gives excellent diagnostic image quality.     

Contact in the Andes: bioarchaeology of systemic stress in colonial Mórrope, Peru

The biocultural interchange between the Eastern and Western Hemispheres beginning in the late fifteenth century initiated an unprecedented adaptive transition for Native Americans. This article presents findings from the initial population biological study of contact in the Central Andes of Peru using human skeletal remains. We test the hypothesis that as a consequence of Spanish colonization, the indigenous Mochica population of Mórrope on the north coast of Peru experienced elevated systemic biological stress. Using multivariate statistical methods, we examine childhood stress reflected in the prevalence of linear enamel hypoplasias and porotic hyperostosis, femoral growth velocity, and terminal adult stature. Nonspecific periosteal infection prevalence and D(30+)/D(5+) ratio estimations of female fertility characterized adult systemic stress. Compared to the late pre-Hispanic population, statistically significant patterns of increased porotic hyperostosis and periosteal inflammation, subadult growth faltering, and depressed female fertility indicate elevated postcontact stress among both children and adults in Mórrope. Terminal adult stature was unchanged. A significant decrease in linear enamel hypoplasia prevalence may not indicate improved health, but reflect effects of high-mortality epidemic disease. Various lines of physiological, archaeological, and ethnohistoric evidence point to specific socioeconomic and microenvironmental factors that shaped these outcomes, but the effects of postcontact population aggregation in this colonial town likely played a fundamental role in increased morbidity. These results inform a model of postcontact coastal Andean health outcomes on local and regional scales and contribute to expanding understandings of the diversity of indigenous biological variation in the postcontact Western Hemisphere.     

The etiology of porotic hyperostosis among the prehistoric and historic Anasazi Indians of Southwestern United States

Porotic hyperostosis was studied in 539 crania from maizegrowing prehistoric and historic groups who occupied two dissimilar ecological zones of the Plateau country of Arizona and New Mexico—canyon bottoms and sage plain. Defined as abnormal localized sieve-like structural changes involving the hematopoietic areas of the cranium, it was found in 185 (34.3%) of these skulls. More frequent in children than in adults, it shows significant frequency differences between both children and adults of the two ecological zones. The two ecological zones differ in the availability of iron in the diet; the canyon inhabitants depended heavily on maize (which interferes with iron absorption) while the sage plain people consumed more iron-rich animal products. We hypothesize that an increased dependence on maize produced more iron deficiency anemia and resulted in more porotic hyperostosis. Maize is known to have permitted a food surplus which in turn allowed for increased South-western population growth in marginal areas like the canyon bottoms. Heavy dependency on a single food type with consequent hematologic problems may have been an important reason for the subsequent abandonment of the Anasazi region.     

Possible congenital hemolytic anemia in prehistoric coastal inhabitants of Israel.

The spread of thalassemia among prehistoric populations of the Mediterranean Basin has been linked to the increased risk to early agriculturalists posed by the Plasmodium falciparum parasite. The diagnosis of the disease in human skeletal remains, however, has usually been based on a single pathological criterion, porotic hyperostosis. This paper reports on what we believe to be the earliest case of thalassemia yet identified in the prehistoric record. Our diagnosis of the disease in an individual from the submerged Prepottery Neolithic B village of Atlit-Yam off the Israeli coast is based on a pathological humerus demonstrating a pattern of deformation characteristic of clinical thalassemia. The implications of these findings for our understanding of human societies undergoing the transition from foraging to agriculture in the Near East are discussed.     

Endemic disease patterns in Paleopathology: Porotic hyperostosis

Recent research has shown that constitutional factors can elicit a porotic skeletal lesion pattern related to iron-deficiency anemia, even when adequate dietary iron is available. This study considers the pattern of skeletal involvement under conditions of chronic or endemic dietary stress. Analysis focused on 54 subadults aged 0–10 years at death from the Arroyo Hondo site. Early age of onset is documented in the pattern of coincident active periosteal reactions and porotic lesions under 6 months. Endemically inadequate diets affecting pregnant females and their fetuses, acting synergistically with immediately acquired infections, not weaning diets, are the probable major underlying causes for the early onset of iron-deficiency anemia at Arroyo Hondo.     

Diet, residential origin, and pathology at Machu Picchu, Peru

Pathological conditions in human skeletal remains provide a wealth of information about archaeological populations, but many are limited in their interpretive significance by their nonspecific etiologies. This study analyzes three common pathological conditions known to manifest in infancy and childhood in the skeletal population from Machu Picchu, Peru (N = 74) with published carbon, nitrogen, oxygen, strontium, and lead isotopic data (Turner et al.: J Archaeol Sci 36 (2009) 317–332; Turner et al.: Chungara: Revista de Antropología Chilena 42 (2010) 515–524) to distinguish early‐life diet from residential origins as significantly associated with pathologies among the site's inhabitants. Analyses of variance indicate highly significant variation between enamel δ¹⁸O values, which serve as a rough proxy of local environment, and both cribra orbitalia (CO) and porotic hyperostosis (PH), generally understood to be markers of anemia. Results tentatively suggest that individuals manifesting these lesions may have lived closer to the arid coasts; however, no significant variation was found in parameters of diet (enamel δ¹³C_carbonate, dentin δ¹³C_collagen, dentin δ¹⁵N) by either CO or PH, suggesting that the primary factors causing anemia may have been more significantly related to residential origin rather than diet. Linear enamel hypoplasia (LEH) frequency significantly varied by both dietary and residential parameters, supporting models of LEH formation from a synergy of dietary and environmental factors. These results support previous research on the etiology of PH in the Andes; they also represent a useful approach to refining site‐specific interpretations of pathological conditions in archaeological populations, and exploring etiological variation between populations. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Cribra orbitalia in the aborigines of Hawaii and Australia

Cranii of 53 Hawaiian aboriginal infants and children, and 45 from Australian aboriginal children were inspected. Cribra orbitalia was present in 22.8% of the former and 26.6% of the latter; osteoporotic pitting (symmetrical osteoporosis; porotic hyperostosis) was also present in the latter. The frequency compares favorably with that found in pre-Columbian North American Pueblo Indians, 24.7%. It is associated with a widespread skeletal involvement suggestive of an active bone marrow. The findings support the concept that cribra orbitalia is related to symmetrical osteoporosis and that it may be associated with a blood disorder.