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Historical, Skeletal, and Molecular Data Leprosy Was the Scourge Of Journal of Interdisciplinary History, XLIX:3 (Winter, 2019), 367–395. Samuel Mark The Origin and Spread of Leprosy: Historical, Skeletal, and Molecular Data Leprosy was the scourge of ancient societies and continued to be a significant health problem in a number of countries until quite recently. A combination of early diagnosis and treatment with multi-drug therapy has greatly re- duced the number of cases of leprosy worldwide, especially in the last twenty-five years. Today, nearly 83 percent of the more than 200,000 new cases reported annually are from three countries— India, Brazil, and Indonesia. Nevertheless, many Western countries have not yet been able to eradicate leprosy completely. In the United States, the appearance of three strains of M. leprae—SNP subtypes 3K (nine cases), 3J (one case), and 3M (one case)—indicates that new cases continue to arrive from abroad. Another occasional source of infection is apparent contact with armadillos, ranging from Texas to Florida and Georgia. Hence, leprosy continues to remain a health concern even in developed countries. Employing a variety of methods—with attention to both historical sources and molecular data—this article examines the likely origins of leprosy, indicating what we can know about the spread of a disease that has social as well as medical consequences.1 Prior to 2005, India was widely accepted as the country of origin for Mycobacterium leprae primarily due to detailed descrip- tions of the progressive forms of leprosy in the Sushruta Samhita, Samuel Mark is Professor of Maritime Studies, Texas A&M University at Galveston. He is the author of From Egypt to Mesopotamia: A Study of Predynastic Trade Routes (College Station, 1997); Homeric Seafaring (College Station, 2005). The author thanks the anonymous referees for suggestions and comments that greatly improved this article. © 2018 by the Massachusetts Institute of Technology and The Journal of Interdisciplinary History, Inc., https://doi.org/10.1162/jinh_a_01301 1 World Health Organization, “Global Leprosy Update, 2016: Accelerating Reduction of Disease Burden,” Weekly Epidemiological Record, XXXV (2017), 501, 505 (Table 2); Joshua Lane et al., “Borderline Tuberculoid Leprosy in a Woman from the State of Georgia with Armadillo Exposure,” Journal of the American Academy of Dermatology, LV (2006), 714–716; Rahul Sharma et al., “Zoonotic Leprosy in the Southeastern United States,” Emerging Infectious Diseases, XXI (2015), 2127–2134. Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jinh_a_01301 by guest on 26 September 2021 368 | SAMUEL MARK an Indian medical text dating to c. 600 B.C. In 2005, Monot et al. greatly increased our understanding of M. leprae and our ability to map it geographically based on the discovery that four single- nucleotide polymorphisms (SNPs) correlated with general geo- graphical regions consistent with an origin for M. leprae in either East Africa or India. In 2009, Monot et al. proposed an origin for M. leprae in East Africa (henceforth, the East African model) after comparing Brazilian and Indian genome sequences, allowing them to define sixteen SNP-subtypes (1A–D, 2E–H, 3I–M, 4N–P). They proposed that the geographical locations of these subtypes were consistent with migration patterns of early humans and trade routes. SNP-subtype 2H was the earliest in East Africa, leading to 2F in Iran and finally 1A in India. Subtype 2F would have evolved into 3K, leading to 3M in Europe. Since type 3 is associated with European populations, and only 3K was reported in China, it must have spread from either Iran or Turkey via the Silk Road, instead of via maritime routes from India to southern China (Figure 1).2 Weng et al. found that 3K was the most common type of M. leprae in both coastal and inland provinces of China, whereas subtypes 1D (seventeen cases) and 1A (one case) appeared only in the coastal provinces of Guangdong, Fujian, and Guangxi, and only SNP type 2 (subtype unknown, 1 case) appeared in the autonomous province of Xinjiang. Based on these data, Weng et al. proposed that M. leprae could have originated in East Africa and spread to China via southern maritime routes mainly through Guangzhou in Guangdong province, a port of entry that likely dates to the Han dynasty (202 B.C.– A.D. 220). According to Paine, however, ports along the southern coast of China were importing goods as early as the eighth century 3 B.C. 2 For works that propose leprosy as originating in India, see Dharmendra, “Leprosy in Ancient Indian Medicine,” International Journal of Leprosy, XV (1947), 424–430; Johs Andersen, Studies in the Medieval Diagnosis of Leprosy in Denmark: An Osteoarchaeological, Historical and Clinical Study (Copenhagen, 1969), 10–45, 123; Mark, “Alexander the Great, Seafaring, and the Spread of Leprosy,” Journal of the History of Medicine and Allied Sciences, LVII (2002), 286–311; Marc Monot et al., “On the Origin of Leprosy,” Science, CCCVIII (2005), 1040–1042; idem et al., “Compar- ative Genomic and Phylogeographic Analysis of Mycobacterium leprae,” Nature Genetics, XLI (2009), 1282–1289. 3 Xiaoman Weng et al., “Molecular, Ethno-Spatial Epidemiology of Leprosy in China: Novel Insights for Tracing Leprosy in Endemic and Non Endemic Provinces,” Infection, Genetics and Evolution, XIV (2013), 361–368; Lincoln Paine, The Sea and Civilization: A Maritime History of the World (New York, 2015), 171–173. Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jinh_a_01301 by guest on 26 September 2021 THE ORIGIN AND SPREAD OF LEPROXY | 369 Fig.1 Distribution of M. leprae SNP Types and Subtypes from Africa to Japan. SOURCES This figure is based on data from Masanori Matsuoka et al., “Genotypic Analysis of Mycobacterium leprae Isolates from Japan and other Asian Countries Reveals a Global Trans- mission Pattern of leprosy,” FEMS Microbiology Letters, CCLXI (2006), 150–154; idem et al., “Various Genotypes of Mycobacterium leprae from Mexico Reveal Distinct Geographic Distri- bution,” Leprosy Revue, LXXX (2009), 322–326; Marc Monot et al., “Comparative Genomic and Phylogeographic Analysis of Mycobacterium leprae,” Nature Genetics, XLI (2009), 1282–1289 (Figure 4); Florence Reibel et al., “New Insights into the Geographic Distribution of Myco- bacterium leprae SNP Genotypes Determined for Isolates from Leprosy Cases Diagnosed in Metropolitan France and French Territories,” PLoS Neglected Tropical Diseases, IX (2015), 1–10; Xiaoman Weng et al., “Molecular, Ethno-Spatial Epidemiology of Leprosy in China: Novel Insights for Tracing Leprosy in Endemic and Non Endemic Provinces,” Infection, Genetics and Evolution, XIV (2013), 361–368. Schuenemann et al. challenged the East African model after comparing five M. leprae samples from medieval skeletons with eleven modern samples that had longer branch lengths from accu- mulated substitutions. The authors calculated average distances be- tween strains. Using a strict clock model, which assumes that all strains evolve at the same evolutionary rate, they calculated the most likely divergence date for the most recent common ancestor for all known M. leprae strains to have been 3,126 years ago, or 1114 B.C. (within a range of 4,562 to 1,975 years ago, or 2546 B.C.toA.D. 43). They also calculated a most likely date and date ranges for some SNP subtypes. Subtype 3K was the oldest (782 B.C., 2157 B.C.toA.D. 389), followed by 3L (no date or range given) and 3I (A.D. 516, 35 B.C.to A.D. 908). Branch 1 (1D=A.D. 621, A.D.46to1106;1B=A.D. 810, A.D. 292 to 1246; 1A=A.D. 1317, A.D. 959 to 1612) and Branch 2 (2F=A.D. 735, A.D. 466 to 964) possibly diverged at the same time; the Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jinh_a_01301 by guest on 26 September 2021 370 | SAMUEL MARK latest is branch 4 (4N=A.D. 1045, A.D.558to1467;4P,4O=A.D. 1246, A.D. 842 to 1610). A most likely date or date range was not given for subtype 3J, 3M, 1C, 2E, 2G, or 2H. Schuenemann et al. proposed that these data supported an origin in India (henceforth, the Indian model). Additional evidence derived from a skeleton from India exhibiting lesions diagnosed as leprous, dating to c. 2000 B.C. This date is consistent with the earliest date in their 4 date range for subtype 3K of 2157 B.C. Singh et al. discovered a second species that caused leprosy, Mycobacterium lepromatosis. Comparing a near-complete genome sequence of M. lepromatosis with that of M. leprae, they calculated a divergence time for the most recent common ancestor for all M. leprae strains as 3,607 years ago (1592 B.C.) with a range of 5,525 to 2,204 years ago (3508 to 187 B.C.). They also stated that subtype 5 3K was in a separate branch 0 from all other SNP 3 subtypes. The most recent common ancestor for all known strains of M. leprae has never been found in any species. However, chim- panzees and some species of monkeys and Eurasian red squirrels (Sciurus vulgaris) are susceptible to M. leprae, and Eurasian red squirrels are also susceptible to M. lepromatosis.Hence,somere- searchers propose that M. lepromatosis and M. leprae diverged from their most recent common ancestor about 13.9 million years ago, when each acquired a new host, possibly different species of mon- keys or apes, or even a rodent vector. Sometime around 1592 B.C. or 1114 B.C., or within the previously cited date ranges of 3508 to 187 B.C.or2545B.C.toA.D. 42, humans were probably first infected with M. leprae from contact with an infected animal, beginning the divergences of known SNP types and subtypes. M. lepromatosis also reached humans in a similar manner at an unknown time and place as migrations and long-distance trade spread both species of leprosy 4 Verena Schuenemann et al., “Genome-wide Comparison of Medieval and Modern Mycobacterium leprae,” Science, CCCXLI (2013), 179–183.
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