Mycobacterium leprae and Leprosy: A Compendium
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1 Minireview Microbiol. Immunol., 45(11), ,2001 Mycobacterium leprae and Leprosy: A Compendium Shin Sasaki*'\ Fumihiko Takeshita', Kenji Okuda", and Norihisa lshil' Departments of'bioregulation and 'Microbiology, Leprosy Research Center; National Institute ofinfectious Diseases, Higashimurayama, Tokyo , Japan, and 'Department ofbacteriology, Yokohama City University School of Medicine, Yokohama, Kanagawa , Japan Received September 20,2001 Abstract: Leprosy is a chronic infectious disease caused by Mycobacterium leprae, which was discovered by G.H.A. Hansen in M. leprae is an exceptional bacterium because of its long generation time and no growth in artificial media. Entire sequencing of the bacterialgenome revealed numerous pseudogenes (inactive reading frames with functional counterparts in M. tuberculosis) which might be responsible for the very limited metabolic activity of M. leprae. The clinical demonstration of the disease is determined by the quality of host immune response. Thl-type immune response helps to kill the bacteria, but hosts are encroached upon when Th2-type response is predominant. The bacteria have affinity to the peripheral nerves and are likely to cause neuropathy. M. leprae/laminin-a2 complexes bind to alp dystroglycan complexes expressed on the Schwann cell surface. WHO recommends a chemotherapy protocol [multidrug therapy (MDT)] which effectively controls the disease and contributes to the global elimination program. Leprosy has been stigmatized throughout history, and recent topics regarding the disease in Japan are also discussed. Key words: Mycobacterium leprae, Leprosy, Pseudogene, Thlrrh2 dichotomy, Schwann cells Historical and Global Situation Leprosy, or Hansen's disease, is a chronic infectious disease which primarily affects the skin, the peripheral nerves, the upper respiratory tract, and also the eyes. The causative microbe is an acid-fast bacterium, M. leprae, which was identified in 1874 by the Norwegian physician Gerhard Henrik Armauer Hansen. M. leprae has several unique features, the most exceptional being that no successful culture has ever been reported in vitro. Leprosy has been documented since antiquity and still continues to be endemic in some developing countries, most of them located in tropical and subtropical zones. Throughout history, it has been feared as an incurable disease which causes severe deformities and disabilities resulting in stigmatization, and therefore the victims have suffered both from the disease itself and from public discrimination. Leprosy was considered as a divine punishment for sin in the Old Testament and *Address correspondence to Dr. Shin Sasaki, Department of Bioregulation, Leprosy Research Center, National Institute of Infectious Diseases, Aoba-cho, Higashimurayama, Tokyo , Japan. Fax: ssasaki@nih. go.jp a karma in Buddhism; the term leprosy originates from the Latin word lepros, which means defilement (19). In 1991, the World Health Organization (WHO) and its Member States committed themselves to eliminate leprosy as a public health problem by the year 2000 (37), elimination being defined as prevalence < I case per 10,000 persons. At the beginning of year 2000, the deadline of the program, 641,091 leprosy cases were registered for treatment and 678,758 cases were newly detected in the world (38). The prevalence rate at the global level is around 1.25 per 10,000 persons. Among 122 countries where the disease was considered endemic in 1985, 98 countries reached the elimination goal, and the global prevalence has been reduced by 86%. While leprosy remains a public health problem in 24 countries, 677,086 newly detected patients live in the top 11 countries where the disease is endemic, and represent 92% ofcases detected worldwide. The prevalence rate in these top 11 countries remains 4.1 per 10,000, and the Abbreviations: BB, mid-borderline; BL, borderline lepromatous; BT, borderline tuberculoid; ENL, erythema nodosum leprosum; IFN, interferon; IL, interleukin; LL, lepromatous; MB, multibacillary; MDT, multidrug therapy; PB, paucibacillary; POL-I, phenolic glycolipid I; RR, reversal reaction; Th cell, helper T cell; TT, tuberculoid. 729
2 730 S. SASAKI ET AL Table I. Registered prevalence of leprosy and detection rate in the top II countries where the disease is endemic Country Registered cases Prevalence Cases detected Detection rate (I January 2000) per 10,000 in 1999 per 100,000 India 495, , Brazil 78, , Myanmar 28, , Indonesia 23,156 l.l 17, Nepal 13, , Madagascar 7, , Ethiopia 7, , Mozambique 7, , Congo DR 5, , Tanzania UR 4, , Guinea 1, , Total 672, , (WHO Weekly Epidemiological Record 75: , 2000) Table 2. Comparison of genome features Feature M.leprae M. tuberculosis Genome size (bp) 3,268,203 4,411,532 G+C (%) Protein coding (%) Protein-coding genes (no.) 1,604 3,959 Pseudogenes (no.) 1,116 6 Gene density (bp per gene) 2,037 1,114 Average gene length (bp) 1,011 1,012 Average unknown gene length (bp) (Nature 409: ,2001) distribution is very uneven (Table 1). Of the 11 countries, India accounts for 80% of the detection and is a major concern for global leprosy control. In Japan, around 20 patients a year are newly registered as having leprosy, and more than 50% of the cases detected are among immigrants from countries where the disease is endemic (12). The disease is generally more common in males by a ratio of about 1.5 to 1 (36). Bacteriology and Genomics ofmycobacterium leprae The pathogen of leprosy, M. leprae, cannot be cultured in artificial media, and therefore it is impossible to meet Koch's postulates. Instead, it multiplies extensively in footpads of nude mice (31), nine-banded armadillos (Dasypus novemcinctus) (16), and, to a limited extent, in normal mice footpads. Armadillos are also known to be an extrahuman reservoir of the leprosy bacillus, and may playa role in the epidemiology of the disease in humans in the southern and southwestern United States (18). Naturally acquired leprosy has been reported in three species of non-human primates (chimpanzees, sooty mangabeys, and cynomolgus macaques), thus qualifying the disease as a zoonosis (28). Taxonomically, M. leprae belongs to the genus Mycobacterium, which is a single genus of the family Mycobacteriaceae, in the order Actinomycetales (26). M. leprae is an obligate intracellular parasite which measures 0.3--o.5X4.Q-7.0!-lm and multiplies very slowly, with a generation time of 12 to 14 days. It grows best around 30 C, and hence it prefers the cooler areas of human bodies. The bacterium can remain viable for several days ex vivo. The gram-positive type of the cell wall is highly complex and contains proteins, phenolic glycolipid, arabinoglycan, peptideglycan, and mycolic acid, the latter possibly being responsible for its acid-fastness. An antibody against phenolic glycolipid-i (PGL-I) of M. leprae can be detected among the patients and healthy individuals in area where the disease is endemic, suggesting that the antibody levels reflect the bacterial loads (6). Measurement of anti-pgl-i antibody could be useful in the assessment of patients and groups at highrisk for leprosy (3, 4), and provides serological parameters in monitoring patients following chemotherapy (6). Although this antibody is useful for diagnostic purposes, no neutralization activity against the leprosy bacillus has been reported. Considerable progress has been made in the field of genomics, and the entire genome sequence of M. leprae has been analysed (8). The most striking feature of the leprosy bacillus genome is the extensive deletion and inactivation of genes referred to as gene degradation (Table 2); only 49.5% of the genome contains proteincoding genes, and 27% contains recognizable pseudogenes (inactive reading frames with functional counterparts in the tuberculosis bacillus) (7, 8). Analysis ofthe genomic sequence revealed that the genes encoding various enzymes are replaced by pseudogenes (8), which suggests limited metabolic activity of the leprosy bacillus. This genomic feature might correspond to its unique
3 MINIREVIEW 731 bacteriological characteristics such as exceptionally slow growth and failure to multiply in synthetic media. The leprosy bacillus seems to be scrapping most of its genetic inheritance in order to thrive, although it maintains residual elements required to survive inside humans and some other animals. Disease Spectrum and Diagnostic Procedures Infection with the leprosy bacillus, although it is a unique pathogen, induces very diversifiedclinical features corresponding to host's immune response. Leprosy develops apparent polarity in the disease spectrumtuberculoid and lepromatous leprosy. Patients with tuberculoid leprosy generally have a few large macular hypopigmented or erythematous anaesthetic lesions which have a well defined, often raised margin or occasionally are scaly plaques (13). By contrast, lepromatous leprosy is usually widespread and may consist of erythematous macules, and papules and/or nodules. Occa- Infection with M. leprae No disease (healthy carrier?) Spontaneous cure Indeterminate group PB MB negative Skin-smears positive no Contagious? yes Type 1 Dominant cytoklne Type 2 (IL-2, IFN-y) profile (ll-4, Il-5) Fig. 1. Disease spectrum of leprosy (The Lancet 353 : ; partially modified).
4 732 S. SASAKI ET AL sionally the disease is diffuse without distinct lesions (13). Borderline cases positioned in between these two extremes are also found. It is agreed that crucial defense at the battlefront against M. leprae is attained by cellmediated immunity, and therefore the outcome of infection depends how the host responds to the pathogen-the magnitude of cell-mediated immunity determines the extent of the disease (19). Early pioneering works revealed an apparent relationship between the dominant cytokine profiles and the clinical presentation of leprosy; interleukin 2 (ll-2) and interferon gamma (IFN-y) were markedly dominant in tuberculoid lesions, whereas IL-4, IL-5 and IL-I0 were characteristic of lepromatous lesions (30, 39). Th 1-Th2 dichotomy is a central determinant of type of host defense (5); the T helper type 1 (Thl) subset characterized by predominant IL-2 and IFN-y preferentially elicits cell-mediated immunity, whereas Th2 cells which produce IL-4, 5, and 10 augment humoral immunity. Both the classic reciprocal relation between antibody production and cell-mediated immunity and resistance or susceptibility to the leprosy bacillus can be explained by T cell subsets differing in patterns of cytokine production. As a mechanism responsible for T cell activation against mycobacterium, the CD l-mediated lipid antigen presentation pathway is notable (1, 20). It displays a unique facet of host defense independent of classical peptide antigen presentation through MHC molecules. Recently, Ochoa et al discovered a novel mechanism by which T cells contribute to host defense against mycobacteria using a leprosy model (21). Granulysin, an antimicrobial protein, is preferentially expressed by T cells in tuberculoid lesions but not lepromatous lesions. In vitro assay revealed that granulysin-expressing T cells obtained from leprosy lesions were able to reduce the viability of mycobacteria. This study indicates that granulysin plays a significant role in host defense against mycobacteria including M. leprae. Figure I illustrates the disease spectrum and classification of leprosy. Recent epidemiological studies indicate that transmission of the leprosy bacillus is effected by airborne droplet infection through the respiratory system, in which the nose plays a central role (9, 11,22). It is believed that there is widespread subclinical transmission of M. leprae with transient infection of the nose in areas of endemicity, although most of these cases do not develop clinical disease (reviewed in (34)). According to the Ridley-Jopling classification system (27), the disease can be classified into 6 categories: indeterminate (I), tuberculoid (TT), borderline tuberculoid (BT), midborderline (BB), borderline lepromatous (BL), and lepromatous (LL) on the basis of dermatological, neurological, and histopathological findings. Most of the newly diagnosed patients, however, live in developing countries where no sufficient medical resources are available. Since the Ridley-Jopling classification system is not practical in these countries, WHO established a more simplified classification system which consists of just two categories-paucibacillary (PB) and multibacillary (MB) (36). PB leprosy is defined as five or fewer skin lesions with no bacilli in skin smears, and MB leprosy cases have six or more lesions and may be skinsmear positive. As for the correlation between two classification systems, I, TT, and part of BT are generally equivalent to PB leprosy, and part of BT, BB, BL, and LL correspond to MB leprosy. Figure 2 shows the flowchart for diagnosis and classification cited from an atlas designed for use in the areas of endemicity (17). The procedure is very simple and clear, so that patients can be diagnosed and classified without satisfactory medical facilities or staff. In advanced countries, for example in Japan, the Ridley-Jopling classification is generally used and in-depth examination is preferentially attempted by using histopathological, serological, and molecular biological tests. Leprous Nerve Damage Peripheral nerves are also a major target of the leprosy bacillus. The involvement of nerves by the primary infection and the immunologically mediated episodes referred to as leprosy reactions result in impairment of nerve function and severe disabilities. Leprosy causes a 'mononeuritis multiplex' which results in autonomic, sensory, and motor neuropathy. When detected and treated appropriately, primary impairments can be reversible. Actually, skin lesions with sensory disturbance are a persuasive clue to suspicion of leprosy. Most of the nerve destruction in leprosy, however, takes place during the leprosy reaction which consists of reversal reaction (RR; type 1 reaction) and erythema nodosum leprosum (ENL; type 2 reaction). In RR, the level of cell-mediated immunity against M. leprae is suddenly elevated and results in an inflammatory response in the areas of the skin and nerves affected by the disease. Acute inflammation in RR can destroy nerves and result in paralysis which can be permanent if not treated adequately (29). Clinically detectable neural involvement occurs in approximately 10% of PB and 40% of MB leprosy patients (33). How does the leprosy bacillus invade into peripheral nerves? M. leprae has an extreme predilection for the Schwann cells which surround peripheral nerve axons (23). A recent study has demonstrated that the speciesspecific PGL of M. leprae triggers uptake into Schwann cells by creating a complex with laminin-2 (24), an
5 MINIREVIEW ~~.~~ :.:':::»> :~;'-\.~~~L1.J:.f:: Skin lesions with sensory loss Leprosy... ".::: v:-.'.... o:.;l;;.:.;;.:. -.:.-.:.4:::.:::::I.... -:.:--.:-:..-:-:.:.:-: :-::;:O;.:::;.. ==:.:::::JI~==;;;;..:.:::::,.. ::::::::::»:!'"-:"-'.:-:;;.:.-: -,';;;;.:-:,;.:. "" Up to 5 skin ire I}.;;: lesions ~1IIII!I!I1IIII!I!I~lI,I!IIlIIII!I!IlIIII!I!I :.:...:.:.;.:..:.: :.:::.: :..:: :«:-:...:-::..::/.:::: :-:' <.;.:.; ::......:-:. :-::-:-:.:«:::... MB leprosy Fig. 2. Flowchart for diagnosis and classification of leprosy (A New Atlas of Leprosy, Sasakawa Foundation, Tokyo). extracellular matrix protein that is present in the basal lamina of Schwann cells. A 21 kda laminin binding receptor on M. leprae has also been identified (32), being a histone-like protein. Then, M. leprae/laminin-a2 complexes bind to alp dystroglycan complexes expressed on the Schwann cell surface (25). Although it is still a controversial point, Schwann cells are considered to express MHC class II molecules (reviewed in 33). Thus, a possible mechanism for peripheral nerve damage in RR is that infected Schwann cells process and present antigens derived from M. leprae to antigen-specific, inflammatory type I T cells and that these T cells subsequently attack and lyse infected Schwann cells (33). Besides the above mechanism, non-specific inflammatory effect mediated by TNF-a and TGF-p is also suggested as a responsible for the Schwann cell damage (15). For treatment of leprous neuropathy associated with RR, administration of corticosteroids along with anti-leprosy chemotherapy is required to prevent irreversible damage. Treatment and Control Strategy Leprosy control has three major strategic components: Early detection of patients, adequate treatment, and provision of comprehensive care for the prevention of disabilities and rehabilitation (10). Since the disease is caused by infection, needless to say, treatment with antibiotics against the leprosy bacillus plays a pivotal role in managing newly diagnosed patients. There are several
6 734 S. SASAKI ET AL effective chemotherapeutic agents against M. leprae. Dapsone (diaphenylsulfone: DDS), rifampicin (RFP), clofazimine (CLF, B663), ofloxacin (OFLX), and minocycline (MINO) are commonly used in the clinical field today, since they are components of the multidrug therapy (MDT) regimen recommended by WHO (36). Following the classification according to the flowchart (Fig. 2), PB patients receive 600 mg RFP monthly, supervised, and 100 mg DDS daily, unsupervised, for 6 months. Single-lesion PB (SLPB) patients can be treated with a single therapeutic dose consisting of 600 mg RFP, 400 mg OFLX, and 100 mg MINO. MB cases are treated with 600 mg RFP and 300 mg CLF monthly, supervised, and 100 mg DDS and 50 mg CLF daily, for 12 months. Leprosy reaction can occur in all borderline and lepromatous patients, most commonly during chemotherapy. Borderline cases develop type 1 reaction (RR), and type 2 reaction (ENL) takes place in lepromatous patients (13,33). The common treatment for reaction episodes is the use of corticosteroids (36), and thalidomide and/or CLF are also used for ENL cases (13). Prompt and adequate treatment of leprosy reaction along with antileprosy chemotherapy is the key to preventing irreversible nerve damage and disabilities. In the unfortunate case that permanent impairment occurs, patients should be given a course of rehabilitation. Since the outcome of leprosy affects physical, mental, and socio-economical aspects of patients, a rehabilitation program should ideally cover all of these aspects (reviewed in 35). From the viewpoint of prevention of the disease, vaccination against the leprosy bacillus is a possible strategy-bcg vaccination is reported to be partially effective for protection against leprosy (2, 14). But a worldwide BCG vaccination program against M. leprae is not economically feasible (13), and a cost-effective DNA vaccine could become a promising substitute. At present, no vaccination against leprosy is currently available, so adequate treatment with MDT is only weapon available against M. leprae in pursuing a global leprosy control program. Social Sequelae from Leprosy in Japan Leprosy occupies a very special place in the history of medicine worldwide; it was extremely feared and considered one of the most despicable diseases. The victims were despised and often isolated in "leper" colonies or leprosariums. Even today, patients are likely to be shunned by their neighbors and contact is avoided. Particularly in Japan, the state enforced a "leper" isolation policy based on the 1953 Leprosy Prevention Law. The policy was continued even after publication of the advisory by the WHO Expert Committee on Leprosy in 1959, in which repeal of special statute for leprosy control was encouraged. Once diagnosed as having leprosy, patients were confined in national leprosariums and strictly isolated from the general public. A considerable number of women at the leprosarium were forced to have abortions and men were sterilized. The law continued up to 1996, long after the development of effective antibiotics against the leprosy bacillus and after studies proving that the disease was not as contagious as once believed. Former patients launched a lawsuit against the state. The plaintiffs demanded compensation for inadequate treatment while they lived in isolated facilities operated by the state. A verdict was reached and year 2001 became a milestone for the victims of leprosy in Japan. The May 11 ruling by Kumamoto District Court found that the Diet contravened the constitution and the Health Ministry violated human rights by isolating the patients in national leprosariums for under the 1953 law. It ordered the government to pay a total of 1.8 billion yen ($15 million) to 127 plaintiffs. Prime Minister Junichiro Koizumi on May 25 announced a government decision not to appeal the ruling, which ordered the state to pay compensation to former patients. Following the statement by Koizumi, a bill was passed by the Diet to assure compensation not only for the plaintiffs but also for all former leprosarium internees. In addition to the announcement of a compensation package, the state officially apologized to the patients for inadequate treatment under the 1953 law. The former patients accepted the apology from the state, lawsuits still pending were dropped and a settlement was reached between the plaintiffs and the state. The ruling and official apology by the state provide an occasion for serious consideration of the miserable history of leprosy patients. Should the state alone bear the blame for the isolation policy? Would patients have been able to join the public community without hindrance if the law had been repealed earlier? Why was the disease stigmatized and the victims were despised throughout history? About 4,400 people are still living in 15 leprosariums nationwide despite the termination of the isolation policy. Most of them are elderly people who feel that they will bring humiliation to their relatives if they return home. This work was supported by a Health Science Research Grant of Research on Emerging and Re-emerging Infectious Diseases from the Ministry of Health, Labor, and Welfare, Japan.
7 MINIREVIEW 735 References I) Beckman, E.M., Porcelli, S.A, Morita, Ci'L, Behar, S.M., Furlong, S.T., and Brenner, M.B Recognition of a lipid antigen by CDI-restricted a~+ T cells. Nature 372: ) Bertolli. J., Pangi, c., Frerichs, R, and Halloran, M.E A case-control study of the effectiveness of BCG vaccine for preventing leprosy in Yangon, Myanmar. Int. J. Epidemiol. 26: ) Buhrer, S.S., Smits, H.L., Gussenhoven, G.e., van Ingen, e.w, and Klatser, P.R A simple dipstick assay for the detection of antibodies to phenolic glycolipid-i of Mycobacterium leprae. Am. J. Trop. Med. Hyg. 58: ) Butlin, c.n., Soares, D., Neupane, K.D., Failbus, S.S., and Roche, P.W IgM anti-phenolic glycolipid-i antibody measurements from skin-smear sites: correlation with venous antibody levels and the bacterial index. Int. J. Lepr. Other Mycobact. Dis. 65: ) Chitanova, T., and Mackay, e T cell effector subsets: extending the Thlffh2 paradigm, p In Dixon, F. (ed), Adv. 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