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On Porotic Hyperostosis and the Interpretation of Hominin Diets

Posted by Cranda28 on 09 Oct 2012 at 16:34 GMT

Written by JJ Crandall & DL Martin
Department of Anthropology,
University of Nevada, Las Vegas

Dominguez-Rodrigo and colleagues [1] recently presented the early evidence of porotic hyperostosis (PH) in the hominin fossil record. They discovered two fragments of non-adult parietal bone which they age at approximately ~2 years of age-at-death. Their methodology includes microscopic and visual analysis of the fragments from which they, in our opinion, correctly observe that the specimens exhibit porotic hyperostosis. From this find, the authors draw a number of conclusions about the subsistence regime of the family from which this subadult originates as well as suggest a cause-of-death from the two fragments and use these conclusions to infer that meat played a major role in hominin diet. Further, they suggest that the unavailability of such meat was a cause of malnourishment for individual OH 81 and also note that the physiology of the subadult would have been adapted towards the consumption of meat.
While we are not paleoanthropologists and are not in a position to discuss the species identification or estimation of age-at-death undertaken on the specimen we do wish to comment on the ways in which the authors understand porotic hyperostosis, its etiology and how it should be interpreted in fossilized/skeletonized samples. The authors in this study make a number of conclusions based on this data which we find troubling and seek to redress. First, we review how porotic hyperostosis, a pathological bony change that is related to a number of metabolic disorders including anemia, is generally interpreted. Then we use this information to critically discuss a number of the conclusions drawn in this study.
As Dominguez-Rodrigo and colleagues correctly summarize, porotic hyperostosis consists of the abnormal expansion of the medullary cavity due to the enlargement of the hematopoietic marrow. This expansion has typically seen by scholars as a response due to anemia since the 1960s [reviewed in 2]. Traditionally, scholars have assumed that iron-deficiency anemia served as the most common cause of PH [3]. Increasingly, however, this interpretation has been challenged based on re-assessments of clinical data, histological studies and other lines of evidence [2, 4, 5, 6, 7]. In particular, Walker and colleagues [5] provide convincing evidence that hemolytic and megaloblastic anemias are the disorders which cause PH, as the authors note [but see 7, 8]. This, however, is not the only etiological factor at debate in paleopathological discussions of PH. Even when scholars agree that megaloblastic anemia is the cause of PH, there remains contention over whether dietary deficiency, parasitism, genetic anemias, infection or prolonged weaning (or any combination thereof) are the pathways by which an individual acquires anemia [5]. The authors poorly address these alternative hypotheses for PH in this study and instead identify megaloblastic anemia as the most likely aetiology. We contend, however, that these alternatives are more likely and that even if B12 deficiency is the cause of PH in OH 81, a lack of meat in the diet cannot reasonably be posited as the sole, or even main, cause of the disorder as multiple other pathways lead to B12 deficiency in both infants and lactating mothers.
Our first comment relates the ways the authors refute the possibility of genetic anemia among early hominins. They say,
The relationship between porotic hyperostosis and hemolytic anemias, like sicklemia and thalassemia, has also been stressed, suggesting its linkage to malaria. Given that porotic hyperostosis is often documented in human infants of roughly the same age as OH 81 from areas from of malaria, we thus conclude that serious nutritional stress at a key phase in the development of the OH 81 individual was the most likely cause of the porotic hyperostosis observed on the fossil. [1:4]

This method of refuting the possibility of hemolytic anemias as an etiology for the PH observed on OH 81 is highly problematic. PH is relatively common in prehistoric and modern human populations with prevalence rates ranging from 10% to 50% [reviewed in 9]. What decades of research has made clear is that multiple dietary, ecological and cultural variables all shape individual’s risks of exhibiting PH [5]. Therefore, finding cases of PH that are not due to hemolytic anemias in ecological contexts different from those faced by OH 81 is not sufficient evidence to discredit the possibility of these conditions being the causal agent of the PH observed in this case. It is well known that hemolytic anemias are most common in areas where malaria is high [10, 11], and that malaria has long been a major issue in the region where OH 81 was uncovered [12]. In light of this as well as new genetic evidence that P.reichenowl was a health threat to early hominins and that P. falciparum emerged as a health threat as hominin evolution progressed [13] we find hemolytic anemia an equally compelling alternative to the narrative offered up by these authors and urge scholars to more carefully attend to differential diagnoses of these conditions in past populations.
Even if, however, we accept that megaloblastic anemia is the cause of PH in individual OH 81 further simplifications of the etiology of PH persist. First, the authors posit that there are two pathways by which the individual would have developed a B12 deficient diet: Either the maternal diet is lacking or OH 81 may have been weaning and had a meat deficient diet themselves. Here again the authors prematurely jump to meat as the sole factor resulting in PH in individual OH 81. In their alternate hypothesis they suggest individual OH 81 might have been weaning onto a meat-deficient diet. We instead highlight the fact that shifts in weaning during human evolution are multifactorial. As has recently been noted, changes in hominin ecology emerging with genus Homo may be linked to the increased consumption of meat but may also result from greater social cohesion, improved processing of foods including, but not limited to, the use of cooking as well as increased food sharing [14]. To attribute malnutrition among hominin communities then to one causal factor (meat consumption) is problematic as it fails to consider other avenues by which individuals likely obtained B12. Given that insects and other foods consumed by primates and likely early hominins contain B12 [15], and given that infant recommended dietary allowances are estimated at less than one microgram [16], it seems unlikely to us that individuals could not have met this dietary requirement for a duration sufficient to develop advanced PH even in the face of occasional food shortages. Without convincing evidence that food shortages and undernutrition were a chronic issue among hominins and evidence to the contrary among human hunter-gatherers [17] we find the paper’s central argument dubious.
Finally, the authors suggest that OH 81 developed PH as a result of a lacking nutritional intake of B12 from breastmilk. The study hypothesizes that this is evidence of meat deficiency in the diet of OH 81’s mother. This claim is central to the piece and has received great attention since the publication of the article. Here, again, we demonstrate that this “just so” story centering meat as the driver in human evolution is too simplistic. Much as the authors failed to adequately address the complex, multifactorial nature of PH in other contexts as we have highlighted above, they again oversimply the ways B12 is acquired by individuals and put to use in the body in their central hypothesis.
Inadequate dietary uptake of Vitamin B12 is only one of several avenues by which an individual may exhibit a B12-deficiency. There are a number of additional factors to consider which the authors again fail to address or even give credence to. Clinical studies document a number of disorders which inhibit B12 digestion. These include achloryhydria, or low/absent production of gastric acid in the gut which can be caused by a number of genetic conditions, hyperthyroidism, pellagra, cancer or even Helicobacter pylori infection [18]. Additionally, other conditions inhibiting the uptake and metabolism of B12 include giardia and other parasitic conditions [19], Homocystinuria, or the overabundance or deficiency of transcobalamin in the body [20]. Dominguez-Rodrigo and colleagues fail to consider these alternative stressors on dietary B12 intake. While some of these conditions are rare, certainly parasitic infections were common among our hominin ancestors [21] and are worth considering as they have traditionally been linked, alongside diarrheal diseases, with PH by researchers [5]. Here, again, the authors are dismissive noting that the Hadza hunter-gatherers of Tanzania exhibit constant evidence of parasitic infection but show no rates of PH [page 4]. This is again misleading as the source they cite does not address osteological or paleopathological research among the Hadza. Absence of evidence in paleopathology is not sufficient evidence of absence. Abundant evidence of PH has been documented among other hunter-gatherers [21] leaving us again dissatisfied with the ways Dominguez-Rodrigo and colleagues refute alternative hypotheses in their quest to find meat at all turns in hominin evolution.
In summary, we wish to re-emphasize that evidence of porotic hyperostosis in ancient remains is not unilateral evidence of a meat deficient diet. In response to the findings presented by Dominguez-Rodrigo and colleagues, we feel compelled to remind scholars of the problematic nature of the skeletal and fossil records. Paleopathology, or the study of ancient diseases and abnormal bony changes like PH, lends itself to the identification of broad community patterns in health rather than the identification of specific paucities (such as a lack of meat) and has increasingly emphasized the need to carefully qualify differential diagnoses. While we remain open to scholarly work that refines our ability to identify specific deficiencies in the diet, we echo other scholars in noting that “Both CO…and PH… are not specific and have thus been attributed to various types of anemia and non-anemia-related etiologies, including, most recently, waterborne parasite-induced hemoblastic anemia” [19:44]. This picture of porotic hyperostosis is much more complex and challenging to interpret than the narrative proposed by these scholars. Without fully addressing alternative hypotheses, which are admittedly difficult to invalidate for all scholars of ancient health and disease, we remain unconvinced that PH can be linked to the consumption of meat directly. And while we do not seek to undermine the role meat consumption and hunting might play in hominin evolution, we are open to a more complex picture of the evolution of diet and subsistence in the genus Homo that obtains B12 from meat, insect and other sources and considers the impact of social behavior and processing in preventing the kind of chronic B12 deficiency that would be required to develop PH as severe as the case importantly documented here.

Works Cited
1. Dominguez-Rodrigo M, Pickering TR, Diez-Martin, F, Mabulla A, Musiba, C, Trancho, G, Baquedano E, Bunn HT, Barboni D, Santonja M, Uribelarrea D, Ashley GM, Martinez-Avila MS, Barba R, Gidna A, Yravedra J, Arriaza C (2012) Earliest porotic hyperostosis on a 1.5-million-year-old hominin, Olduvai Gorge, Tanzania. PLoS ONE 7(10):e46414. Doi:10.1371/journal.pone.0046414
2. Wapler U, Crubezy E, Schultz M (2004) Is Cribra Orbitalia synonymous with anemia? Analysis and interpretation of cranial pathology in Sudan. Am J Phys Anthropol 123:333-339.
3. Stuart-Macadam PL (1992) Porotic hyperostosis: a new perspective. Am J Phys Anthropol 80: 187-193.
4. Schultz M (2001) Paleohistopathology of bone: a new approach to the study of ancient diseases. Am J Phys Anth 33: 106-147.
5. Walker PL, Bathurst RR, Richman R, Gjerdrum T, Andrushko VA (2009) The causes of porotic hyperostosis and cribra orbitalia: a reappraisal of the iron-deficiency anemia hypothesis. Am J Phys Anthropol 139: 109-125.
6. Weston DA (2009) Paleohistopathological analysis of pathology museum specimens: can periosteal reaction microstructure explain lesion etiology? Am J Phys Anthropol 140(1):186-193.
7. Sanford, MK, Van Gerven DP, Meglen RR (1983) Elemental hair analysis: new evidence on the etiology of cribra orbitalia in Sudanese Nubia. Hum. Biol.55(4): 831-844.
8. Oxenham MF, Cavill I (2010) Porotic hyperostosis and cribra orbitalia: the erythpoietic response to iron-deficiency anaemia. Anthropol Sci 118(3):119-200.
9. DeGusta D (2010) Cribra orbitalia: a non-human primate perspective. Int J Osteoarchaeol 20:597-602.
10. Livingstone, FB (1958) Anthropological implications of sickle cell gene distribution in West Africa. Am Anth 60(3): 533-562.
11. Angel JL (1966) Porotic hyperostosis, anemias, malarias and marshes in the prehistoric Mediterranean. Science 153: 760-763.
12. Ministry of Health (2002) Health statistics abstract. Burden of disease and health utilization statistics. Vol 1. Dar Es Salaam, Tanzania: Ministry of Health, 3-3.
13. Rich SM, Leendertz FH, Xu G, LeBreton M, Djoko CF, Aminake MN, Takang EE, Diffo JLD, Pike BL, Rosenthal BM, Formenty P, Boesch C, Ayala FJ, Wolfe ND (2009) The origin of malignant malaria. Proc Natl Acad Sci USA 106(35): 14902-14907.
14. Humphrey LT (2010) Weaning Behavior in Human Evolution. Semin Cell Biol 21: 453-461.
15. Wakayama EJ, Dillwith JW, Howard RW, Blomquist GJ (1984) Vitamin B12 levels in selected insects. Insect Biochem 14(2): 175-179.
16. Institute of Medicine. Food and Nutrition Board (1998) Dietary Reference Intakes: Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin, and Choline. Washington, DC: National Academy Press.
17. Benyshek DC, Watson JT (2006) Exploring the thrifty genotype’s food-shortage assumptions: A cross-cultural comparison of ethnographic accounts of food security among foraging and agricultural societies. Am J Phys Anthropol 131: 120-126.
18. El-Omar EM, Oien K, El-Nujumi A, Gillen D, Wirz A, Dahill S, Williams C, Ardill JE, McColl KE (1997) Helicobacter pylori infection and chronic gastric acid hyposecretion. Gastroenterol113(1): 15-24.
19. Cordingley FT, Crawford GPM (1986) Giardia infection causes vitamin B12 deficiency. Aust NZ J Med 16(1): 78-79.
20. Adcock BB, McKnight JT (2002) Cobalamin pseudodeficiency due to a transcobalamin I deficiency. South Med J95(9):1060-1062.
21. Armelagos GJ (2010) Health and Disease in Prehistoric Populations in Transition. In: Brown PJ, Barrett R, editors. Understanding and applying medical anthropology. Boston: McGraw Hill. pp. 50-60.
22. Zuckerman MK, Turner BL, Armelagos GJ (2012) Evolutionary thought in paleopathology and the rise of the biocultural approach. In: Grauer AL, editor. A Companion to Paleopathology. New York: Wiley-Blackwell. pp. 34-57.

No competing interests declared.

RE: On Porotic Hyperostosis and the Interpretation of Hominin Diets

Cranda28 replied to Cranda28 on 09 Oct 2012 at 17:52 GMT

A few corrections:

"Our first comment relates the ways the authors refute the possibility of genetic anemia among early hominins" should say "relates to the ways."

Additionally, an error regarding citations:
“Both CO…and PH… are not specific and have thus been attributed to various types of anemia and non-anemia-related etiologies, including, most recently, waterborne parasite-induced hemoblastic anemia” [19:44] should instead read [22:14]

No competing interests declared.