Trachoma in Asia-A Disappearing Scourge

Taiwan Journal of Ophthalmology xxx (2016) 1e3

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Taiwan Journal of Ophthalmology

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Review article Trachoma in AsiadA disappearing scourge

* Hugh R. Taylor

Melbourne School of Population and Global Health, The University of Melbourne, Carlton, Victoria, 3053, Australia article info abstract

Article history: Trachoma is an ancient blinding eye disease. With improvements in hygiene and living conditions and Received 4 January 2016 development of targeted strategies by the World Health Organization, trachoma is being progressively Received in revised form eliminated. Great progress is being seen in Asian countries, many of which are becoming trachoma free. 1 April 2016 Accepted 6 April 2016 Available online xxx

Keywords: targeted strategies trachoma elimination World Health Organization

1. Introduction hygiene, chances of individuals repeatedly being infected with Chlamydia increased, leading to the development of trachoma. A Trachoma is the blinding infection caused by Chlamydia tra- single episode of chlamydial eye infection will usually resolve chomatis.1 C. trachomatis is a Gram-negative bacteria that first without serious sequelae, but repeated episodes of reinfection lead evolved at the time of the dinosaurs.2 Basically, every vertebrate to blinding trachoma. species has evolved around its own particular species of Chla- Clinically significant outbreaks of chlamydial infection are also mydia.3 The human strains separated into a predominantly ocular seen in a variety of other animal species, particularly when they are strain and general strains some 2e5 million years ago at about the crowded together.5 When birds are crowded together, they develop time when early human ancestors were evolving; however, modern psittacosis; when cows, pigs, or sheep are crowded, they develop humans evolved only some 100,000 years ago. problems such as chlamydial abortions. Even koalas and crocodiles, Given this extraordinary history of coevolution, infection with when overcrowded, develop symptomatic chlamydial infections.6 Chlamydia does not seem to have presented a major problem with the evolution and health of early mankind. However, with the development of early settlements and the start of agriculture at the 2. Pathogenesis end of the past Ice Age some 12,000 years ago, things changed. th The key to understanding the pathogenesis of trachoma is that References to trachoma in China date back to the 27 century BC when Emperor Huang Ti Nei Ching underwent surgery for trichi- frequent and repeated episodes of reinfection are needed for the 7,8 asis.4 Some of the earliest written records of trachoma are found in development of severe disease. Repeated episodes of infection th th induce a marked and sustained inflammatory response that, with bone writing from the Chang Dynasty (16 e11 century BC). 1 Trachoma became a common and important condition in the time, leads to scarring and structural damage. The changes in Yangtze and Yellow River Valleys in China. Similarly, trachoma also trachoma are an immune response to the chlamydial antigens appeared in the small farming communities developing in the released, as the Chlamydia organisms divide in the conjunctival 9 Euphrates Valley in Mesopotamia, along the Nile Valley in Egypt, epithelial cells. In the eye, of course, this is characterized by the fl and along the Indus and Ganges Rivers in South Asia.1 As people characteristic in ammation, with follicles in the upper tarsal con- fl started to live in settlements, with increased crowding and poor junctiva lid, and scarring later. The more severe the in ammation and the longer it persists, the more severe the scarring. With time, the scars will contract to turn in the eye lashes, causing trichiasis, Conflicts of interest: The author has no conflicts of interest to declare. corneal scarring, and blindness. * Melbourne School of Population and Global Health, The University of Mel- bourne, Level 5, 207 Bouverie Street, Carlton, Victoria, 3053, Australia The key to preventing trachoma is to prevent the repeated epi- E-mail address: [email protected]. sodes of reinfection by preventing transmission. Trachoma is http://dx.doi.org/10.1016/j.tjo.2016.04.002 2211-5056

Please cite this article in press as: Taylor HR, Trachoma in AsiadA disappearing scourge, Taiwan Journal of Ophthalmology (2016), http:// dx.doi.org/10.1016/j.tjo.2016.04.002 2 H.R. Taylor / Taiwan Journal of Ophthalmology xxx (2016) 1e3 transmitted from one child to another through contact with to developed areas despite many attempts by the World Health Or- infected ocular and nasal secretions. This usually occurs by direct ganization (WHO) to combat it.15 contact with ﬁngers, while children play or sleep together, or by the use of shared towels or other materials used to clean children's faces. 4. Identiﬁcation of Chlamydia

3. The 19th and 29th centuries Chlamydia was first identified in conjunctival scrapings in studies undertaken in Indonesia, which used a Giesma stain to Although trachoma persisted in many areas over the past show the now characteristic intracytoplasmic inclusions.16 The 2000 years, it was really 200 years ago after the Napoleonic Wars, inability to culture Chlamydia led investigators to assume that it particularly during the fighting in Egypt, that trachoma was seen as was a virus; although it is still not possible to culture the organism, a major health problem and also a military problem in Europe.1 a number of experimental studies were undertaken to confirm its Although trachoma seems to have existed in many cities, it was infectious nature and understand some of its epidemiology.1 not until a large number of soldiers became incapable of fighting The organism that caused trachoma was not identified until because of their ocular infections that the authorities really took 1957 following the ground breaking research of four Chinese notice of it. This coincided with the start of the Industrial Revolu- ophthalmologists and scientists, Drs T'ang, Chang, Huang, and tion in Europe, a time when a large number of people moved from Wang,17 at Tongren Eye Hospital, Beijing, China. They were the first the countryside and crowded into slums and tenements on the group in the world to be able to culture Chlamydia. They showed outskirts of newly developing industrial towns. Trachoma became a that Chlamydia is a Gram-negative bacterium that can grow only major problem in the civilian population too. within the cytoplasm of cells and divide by binary fission. The The first International Congress of Ophthalmology was held in ability to culture Chlamydia led to an explosion in the research of 1857, and one of the two key agenda items was what to do about Chlamydia with the development of a variety of new and improved trachoma.10 From the military perspective, trachoma could be tests to identify infection and efforts to develop a vaccine.1 curtailed by having soldiers wash separately using clean water and not sharing towels.11 In the 1890s, the United States established a quarantine service for incoming emigrants from Central and 5. Trachoma in the 21st century Eastern Europe who were examined and sent back if they were found to have trachoma.12 In 1998, the World Health Assembly passed a resolution calling For the general population, there was little advancement in the for global elimination of blinding trachoma by the year 2020.18 It treatment of trachoma other than cauterization of the inflamed called on all member states to work and make that commitment a conjunctiva with silver nitrate or copper sulfate, or at times reality. The figures pulled together by WHO in 2003 suggested that curetting of follicles. Many variations of lid surgery that dated back some 49 million children in the Asia Pacific region had active to ancient times were used to correct trichiasis.1 trachoma and that over 3.5 million adults had trichiasis.19 Although trachoma became widespread around the world in the WHO advocated the use of the SAFE strategy to eliminate 1920s, it started to disappear in most developed countries as living blinding trachoma, which includes surgery for inturned lashes, conditions improved during the first half of the 20th century.1 The antibiotic treatment, promotion of facial cleanliness, and environ- advent of sulfonamides in the 1930s and then the development of mental improvement.20,21 Many countries undertook mass drug tetracyclines in the 1940s sped up this process so that trachoma had administration using an annual dose of azithromycin. Pfizer (New disappeared from most developed areas by the 1950s and 1960s. York, NY, USA), the manufacturer of this drug, committed to provide Data collected in Japan track the disappearance of trachoma during azithromycin free of charge for this work, and the distribution is the 20th century (Figure 1).13 Similar findings came from Taiwan.14 coordinated through the International Trachoma Initiative. So far, It has still remained an ongoing problem in most of the less Pfizer has donated over 500 million doses of azithromycin.22

Figure 1. Trachoma prevalence in Japanese school children.13

National representatives of endemic countries and nongovern- family Chlamydiaceae, including a new genus and five new species, and fi ment organizations meet each year under the auspices of WHO at standards for the identi cation of organisms. Int J Syst Bacteriol. 1999;49: 415e440. the Global Alliance to Eliminate Trachoma. Over the past decade, 4. Chen YZ. Ramble in Chinese ophthalmology, past and present. Chin Med J. remarkable progress has been made and trachoma has been elim- 1981;94:1e4. inated from a number of African and Middle East countries.21 5. Kaltenboeck B. Recent advances in the knowledge of animal chlamydial in- fi fections. In: Chernesky M, Caldwell H, Christiansen G, Clarke IN, Kaltenboeck B, Striking progress has also been made in the Asia Paci c region. Knirsch C, et al., eds. Chlamydial Infections. Proceedings of the Eleventh Inter- Most striking of all is the oral announcement of elimination of national Symposium on Human Chlamydial Infections, Niagara-on-the-Lake, trachoma from China that was made in September 2015 at the In- Ontario, Canada, June 18e23, 2006. San Francisco, CA, USA: International Chlamydia Symposium; 2006:399e408. ternational Agency for the Prevention Blindness meetings held in 6. Weigler BJ, Girjes AA, White NA, Kunst ND, Carrick FN, Lavin MF. Aspects of the Beijing. Great progress has also been made in Cambodia and Nepal epidemiology of Chlamydia psittaci infection in a population of koalas (Phas- that seem to have eliminated trachoma, and Vietnam and Laos colarctos cinereus) in southeastern Queensland, Australia. J Wildl Dis. 1988;24: 282e291. where trachoma is now reported to be seen only in some small, 7. Taylor HR, Johnson SL, Prendergast RA, Schachter J, Dawson CR, Silverstein AM. 23 more remote areas in the northern part of each country. Data are An animal model of trachoma II. The importance of repeated reinfection. Invest still awaited from India where much progress is thought to have Ophthalmol Vis Sci. 1982;23:507e519. been made. Published reports of recent surveys are still awaited. 8. Gambhir M, Basanez MG, Burton MJ, et al. The development of an age- structured model for trachoma transmission dynamics, pathogenesis and Although active trachoma has been reduced in, or has dis- control. PLoS Negl Trop Dis. 2009;3:e462. appeared from, most areas, trichiasis still continues to be a major 9. Taylor HR, Maclean IW, Brunham RC, Pal S, Whittum-Hudson J. Chlamydial e problem. The need to identify and provide trichiasis surgery to heat shock proteins and trachoma. Infect Immun. 1990;58:3061 3063. 10. Duke-Elder SA. Century of International Ophthalmology (1857e1957). London: older people, who had severe trachoma in their childhood and Whitefriars Press Ltd; 1958. progress to develop trichiasis, will continue for many years.24 11. Treacher Collins E. Introductory Chapter. Trachoma by J Boldt. London: Hodder and Stoughton; 1904. xie1ii. However, active trachoma still remains a problem in some “ ” fi 12. Allen SK, Semba RD. The trachoma menace in the United States, countries in the Asia Paci c region. It persists in Afghanistan, 1897e1960dhistory of ophthalmology. Surv Ophthalmol. 2002;47:500e509. Myanmar, Pakistan, Papua New Guinea, and the Pacific Island 13. Konyama K. History of trachoma control in Asia. Rev Int Trach. countries of Fiji, Kiribati, Solomon Islands, and Vanuatu. Of course, 2004e2005;1981e1982:107e168. fi 14. Assaad FA, Maxwell-Lyons F. The use of catalytic models as tools for elucidating trachoma has been a signi cant problem in the Australian the clinical and epidemiological features of trachoma. Bull World Health Org. Aboriginal population for many years, but significant progress has 1966;34:341e355. been made over the past few years.25 The prevalence of trachom- 15. Nataf R. Organization of Control of Trachoma and Associated Infections in Un- fl d derdeveloped Countries. Report No.: WHO/Trachoma/19. Geneva: WHO; 1951. atous in ammation follicular is now less than 5%, although some 16. Halberstaedter L, von Prowazek S. Uber zelleinschusse parasitarer natur beim Aboriginal communities still have higher levels of trachoma. trachom [On cell inclusions of a parasitic nature in trachoma]. Arb K Gesundh Amt. 1907;26:44e47. 6. Summary 17. T'ang FF, Chang HL, Huang YT, Wang KC. Studies on the etiology of trachoma with special reference to isolation of the virus in chick embryo. Chin Med J. 1957;75:429e447. Trachoma is an ancient disease that occurs in areas of poor 18. World Health Organization (WHO). WHA51.11 Global Elimination of Blinding personal and community hygiene, where frequent exchange of Trachoma. Geneva: WHO; 1998. Available from: http://www.who.int/ blindness/causes/WHA51.11/en/index.html. infected eye secretions is facilitated. The global efforts to eliminate 19. World Health Organization (WHO). Report of the 2nd Global Scientific Meeting trachoma together with the continuing improvement in living on Trachoma, August 25e27, 2003. Report No.: WHO/PBD/GET 03.1. Geneva, conditions and housing have seen a rapid decline of trachoma in Switzerland: WHO; 2003. fi 20. Francis V, Turner V. Achieving Community Support for Trachoma Control. Report many regions in the Asia Paci c and around the world. With No. WHO/PBL/93.36. Geneva: World Health Organization; 1993. continuing efforts on the remaining “hotspots,” we can feel confi- 21. World Health Organization (WHO). Nineteenth Annual Meeting of the World dent of eliminating trachoma as a blinding disease from the Asia Health Organization (WHO) Alliance for the Global Elimination of Blinding e fi Trachoma by 2020 (GET2020). April 27 29, 2015. Hammamet, Tunisia. Paci c region by the year 2020. 22. International Coalition for Trachoma Control (ICTC). Trachoma Partners Cele- brate Exceptional Progress 2015. Available from: http://www. References trachomacoalition.org/news-blogs/trachoma-partners-celebrate-exceptional- progress. [Accessed 21 April 2016]. 23. Global Atlas of Trachoma; 2015. Available from: http://www.trachomaatlas.org/ 1. Taylor HR. Trachoma: A Blinding Scourge from the Bronze Age to the Twenty-first [Accessed 21 April 2016]. Century. Melbourne: Centre for Eye Research Australia; 2008. 24. International Coalition for Trachoma Control (ICTC). The End in Sight. 2020 2. Stephens RS. Chlamydial evolution: a billion years and counting. In: INSight 2011. Available from: http://trachoma.org/end-sight-2020-insight. Schachter J, Christiansen G, Clarke IN, Hammerschlag MR, Kaltenboeck B, [Accessed 29 April 2016]. Kuo CC, et al., eds. Chlamydial Infections. Proceedings of the Tenth International 25. National Trachoma Surveillance and Reporting Unit. The National Trachoma Symposium on Human Chlamydial Infections, Antalya, Turkey, June 16e21, 2002. Surveillance Reference Group, Taylor HR. Australian Trachoma Surveillance Report San Francisco: International Chlamydia Symposium; 2002:3e12. 2014. The Kirby Institute, UNSW; 2015. Available from: http://kirby.unsw.edu. 3. Everett KDE, Bush RM, Andersen AA. Emended description of the order au/surveillance/Australian-Trachoma-Surveillance-Reports [Accessed 21 April Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae 2016]. fam. nov., each containing one monotypic genus, revised taxonomy of the

Please cite this article in press as: Taylor HR, Trachoma in AsiadA disappearing scourge, Taiwan Journal of Ophthalmology (2016), http:// dx.doi.org/10.1016/j.tjo.2016.04.002