Molecular Identification of Falciparum Malaria and Human Tuberculosis Co-Infections in Mummies from the Fayum Depression (Lower Egypt)

Albert Lalremruata,Raffaella Bianucci,Jürgen F. J. Kun,Andreas G. Nerlich,Markus Ball,Carsten M. Pusch,Beatrix Welte,Igor Mokrousov

doi:10.1371/journal.pone.0060307

Abstract

Due to the presence of the lake Quarun and to the particular nature of its irrigation system, it has been speculated that the Fayum, a large depression 80 kilometers south- west of modern Cairo, was exposed to the hazards of malaria in historic times. Similarly, it has been speculated that, in the same area, also human tuberculosis might have been far more widespread in the antiquity than in its recent past. If these hypotheses were confirmed, it would imply that frequent cases of co-infection between the two pathogens might have occurred in ancient populations. To substantiate those speculations, molecular analyses were carried out on sixteen mummified heads recovered from the necropolis of Abusir el Meleq (Fayum) dating from the 3rd Intermediate Period (1064- 656 BC) to the Roman Period (30 BC- 300 AD). Soft tissue biopsies were used for DNA extractions and PCR amplifications using well-suited protocols. A partial 196-bp fragment of Plasmodium falciparum apical membrane antigen 1 gene and a 123-bp fragment of the Mycobacterium tuberculosis complex insertion sequence IS6110 were amplified and sequenced in six and five of the sixteen specimens, respectively. A 100% concordance rates between our sequences and those of P. falciparum and M. tuberculosis complex ones were obtained. Lastly, concomitant PCR amplification of P. falciparum and M. tuberculosis complex DNA specific fragments was obtained in four mummies, three of which are 14 C dated to the Late and Graeco-Roman Periods. Our data confirm that the hydrography of Fayum was extremely conducive to the spread of malaria. They also support the notion that the agricultural boom and dense crowding occurred in this region, especially under the Ptolemies, highly increased the probability for the manifestation and spread of tuberculosis. Here we extend back-wards to ca. 800 BC new evidence for malaria tropica and human tuberculosis co-occurrence in ancient Lower Egypt.

Highlights

Tuberculosis (TB) and malaria, two of the most ancient and deadly diseases of mankind, have ravaged human communities since the beginning of civilization and remain a major global health problem in the 21st century [1,2]
DNA extracts from the positive apical membrane antigen 1 gene (AMA1) samples 1554, 1564 and 1622 showed amplification with K1 allele-specific primers whereas RO33 and MAD20 failed to amplify any of the 16 mummies tested (Table 1)
Before the eradication of malaria from Egypt, high levels of the infection appeared to have been limited to certain parts of the country and to be strictly linked to its geology [16]

Summary

Introduction

Tuberculosis (TB) and malaria, two of the most ancient and deadly diseases of mankind, have ravaged human communities since the beginning of civilization and remain a major global health problem in the 21st century [1,2]. TB causes ill-health among millions of people each year and ranks as the second leading cause of death of adults from an infectious disease worldwide, after the human immuno- deficiency virus (HIV). Malaria is the 5th cause of death from infectious diseases worldwide after respiratory infections, HIV/AIDS, diarrheal diseases and tuberculosis. In 2011, there were 1.2 million malaria deaths globally and malaria is recognized as the 2nd leading cause of death from infectious diseases in Africa, after HIV/AIDS [2,3]. In many parts of sub-Saharian Africa, the geographic overlap between TB and malaria is extensive and co-infection with TB and malaria is likely to be common [4,5]

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Results

Conclusion