Causes of Low Case Detection and Pulmonary Smear Positive Rates of Tuberculosis in Northern Region of Ghana

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DOI: 10.21522/TIJPH.2013.04.02.Art013

Authors : Abass Abdul-Karim


The study had two main broad but related objectives. The first objective was to determine the actual causes of under detection of pulmonary TB cases in the Northern Region of Ghana. Data was collected through administering a structured questionnaire; and collection of sputum samples from the respondents. The second objective was to determine the actual causes of low smear positive rates by assessing the capacity to effectively perform sputum smear microscopy for Acid Fast Bacilli (AFBs) in the district hospitals where the study was conducted. Collection of data here involved the use of a structured checklist for the laboratory and the staff who performed Tb microscopy. In all, 26 laboratory staff who performed Tb microscopy in the study district hospital laboratories were involved. The study lasted for a period of three months. The study revealed that, 41.2% of the study participants did not go to hospital when they fell sick. Out of this figure, 20.4% (21) attributed their inability to do so to poverty, 4.9% (5) to lack of access, 35.9% (37) to stigma, 28.2% (29) to cultural beliefs and 10.6%(11) attributed it to other reasons.


[1] (2005) Tuberculosis bacteriology--priorities and indications in high prevalence countries: position of the technical staff of the Tuberculosis Division of the International Union Against Tuberculosis and Lung Disease. Int J Tuberc Lung Dis 9, 355-361.

[2] Addo K., Owusu-Darko K., Yeboah-Manu D., Caulley P., Minamikawa M., Bonsu F., Leinhardt C., Akpedonu P. and Ofori-Adjei D. (2007) Mycobacterial species causing pulmonary tuberculosis at the korle bu teaching hospital, accra, ghana. Ghana Med J 41, 52-57.

[3] Addo K.K., Dan-Dzide M., Yeboah-Manu D., Owusu-Darko K., Caulley P., Minamikawa M., Bonsu F., Lienhardt C., Akpedonu P. and Ofori-Adjei D. (2006) Improving the laboratory diagnosis of TB in Ghana: the impact of a quality assurance system. Int J Tuberc Lung Dis 10, 812-817.

[4] Adeleye I.A., Onubogu C.C., Ayolabi C.I., Isawumi A.O. and Nshiogu M.E. (2008) Screening of crude extracts of twelve medicinal plants and “wonder-cure” concoction used in Nigeria unorthodox medicine for activity against Mycobacterium tuberculosis isolated from tuberculosis patients’ sputum. African Journal of Biotechnology 7, 3182-3187.

[5] Aziz M., Becx-Bleumink B.F., Bretzel G., Humes R. and Iademarco M.F. (2002) External quality assessment for AFB smear microscopy. Washington: Association of Public Health Laboratories.

[6] Aziz M. and Bretzel G. (2002) Use of a standardised checklist to assess peripheral sputum smear microscopy laboratories for tuberculosis diagnosis in Uganda. Int J Tuberc Lung Dis 6, 340-349.

[7] Aziz M.A., Rysweska K., Laszlo A. and Blanc L. (2006) Strategic approach for the strengthening of laboratory services for tuberculosis control, 2006-2009. Geneva: WHO.

[8] Baghdadi J.E., Orlova M., Alter A., Ranque B., Chentoufi M., Lazrak F., Archane M.I., Casanova J.L., Benslimane A., Schurr E. and Abel L. (2006) An autosomal dominant major gene confers predisposition to pulmonary tuberculosis in adults. J Exp Med 203, 1679-1684.

[9] Banerji D. and Andersen S. (1963) A Sociological Study of Awareness of Symptoms among Persons with Pulmonary Tuberculosis. Bull World Health Organ 29, 665-683.

[10] Barnes D.S. (1995) The Making of a Social Disease: Tuberculosis in Nineteenth-century France. . University of California Press.

[11] Bass J.B., Jr. (1989) The face of TB changes again. Hosp Pract (Off Ed) 24, 81-85, 88, 93-85, passim.

[12] Becker M.H. (1985) Patient adherence to prescribed therapies. Med Care 23, 539-555.

[13] Blaak E. (2001) Gender differences in fat metabolism. Curr Opin Clin Nutr Metab Care 4, 499-502.

[14] Bonah C. (2005) The 'experimental stable' of the BCG vaccine: safety, efficacy, proof, and standards, 1921-1933. Stud Hist Philos Biol Biomed Sci 36, 696-721.

[15] Borgdorff M.W., Nagelkerke N.J., Dye C. and Nunn P. (2000) Gender and tuberculosis: a comparison of prevalence surveys with notification data to explore sex differences in case detection. Int J Tuberc Lung Dis 4, 123-132.

[16] Bustamante J., Picard C., Fieschi C., Filipe-Santos O., Feinberg J., Perronne C., Chapgier A., de Beaucoudrey L., Vogt G., Sanlaville D., Lemainque A., Emile J.F., Abel L. and Casanova J.L. (2007) A novel X-linked recessive form of Mendelian susceptibility to mycobaterial disease. J Med Genet 44, e65.

[17] Calippe B., Douin-Echinard V., Laffargue M., Laurell H., Rana-Poussine V., Pipy B., Guery J.C., Bayard F., Arnal J.F. and Gourdy P. (2008) Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J Immunol 180, 7980-7988.

[18] Chrisman N. and Kleinman A. (1983) Popular health care, social networks, and cultural meanings: the orientation of medical anthropology. In Handbook of health, health care, and the health professions,, pp. 569-590 [D. Mechanic, editor]. New York: The Free Press.

[19] Comstock G.W. (1994) The International Tuberculosis Campaign: a pioneering venture in mass vaccination and research. Clin Infect Dis 19, 528-540.

[20] Curry F.J. (1968) Neighborhood clinica for more effective outpatient treatment of tuberculosis. N Engl J Med 279, 1262-1267.

[21] Daniel T.M. (1982) Selective primary health care: strategies for control of disease in the developing world. II. Tuberculosis. Rev Infect Dis 4, 1254-1265.

[22] Daniel T.M. (2004) The impact of tuberculosis on civilization. Infect Dis Clin North Am 18, 157-165.

[23] Davila S., Hibberd M.L., Hari Dass R., Wong H.E., Sahiratmadja E., Bonnard C., Alisjahbana B., Szeszko J.S., Balabanova Y., Drobniewski F., van Crevel R., van de Vosse E., Nejentsev S., Ottenhoff T.H. and Seielstad M. (2008) Genetic association and expression studies indicate a role of toll-like receptor 8 in pulmonary tuberculosis. PLoS Genet 4, e1000218.

[24] Deuschle K. and Adair J. (1960) An interdisciplinary approach to public health on the Navajo Indian reservation: medical and anthropological aspects. Ann NY Acad Sci 17, 887-905.

[25] Drobniewski F.A., Caws M., Gibson A. and Young D. (2003) Modern laboratory diagnosis of tuberculosis. Lancet Infect Dis 3, 141-147.

[26] Drobniewski F.A., Hoffner S., Rusch-Gerdes S., Skenders G. and Thomsen V. (2006) Recommended standards for modern tuberculosis laboratory services in Europe. Eur Respir J 28, 903-909.

[27] Dubos R.J. and Jean D. (1987) The White Plague: Tuberculosis, Man, and Society. Rutgers University Press.

[28] Ebara R.V.B., Madunagu E.U. and Otung I.N. (1990) Microbiological exploitation of Cardiac Glycosides and Alkaloids from Garcinia kola and Borreriaocymoides. J. Bacteriol 871, 398-401.

[29] Fortin A., Abel L., Casanova J.L. and Gros P. (2007) Host genetics of mycobacterial diseases in mice and men: forward genetic studies of BCG-osis and tuberculosis. Annu Rev Genomics Hum Genet 8, 163-192.

[30] Fox W. (1983) Compliance of patients and physicians: experience and lessons from tuberculosis-I. Br Med J (Clin Res Ed) 287, 33-35.

[31] Friemodt-Moller J. (1968) Domiciliary drug therapy of pulmonary tuberculosis in a rural population in India. Tubercle 49 (supp.), 22-23.

[32] Gangadharam P.R.J., Reichmann L.B. and Hershfield E.S. (1993) Drug resistance in tuberculosis. In A Comprehensive International Approach, pp. 293-328. [M. Deke, editor].

[33] Gordon S. and Rylance J. (2009) Where there's smoke... there's tuberculosis. Thorax 64, 649-650.

[34] Grossman C.J. (1985) Interactions between the gonadal steroids and the immune system. Science 227, 257-261.

[35] Haefner D.P. and Kirscht J.P. (1970) Motivational and behavioral effects of modifying health beliefs. Public Health Rep 85, 478-484.

[36] Hamid Salim M.A., Declercq E., Van Deun A. and Saki K.A. (2004) Gender differences in tuberculosis: a prevalence survey done in Bangladesh. Int J Tuberc Lung Dis 8, 952-957.

[37] Hargreaves N.J., Kadzakumanja O., Whitty C.J., Salaniponi F.M., Harries A.D. and Squire S.B. (2001) 'Smear-negative' pulmonary tuberculosis in a DOTS programme: poor outcomes in an area of high HIV seroprevalence. Int J Tuberc Lung Dis 5, 847-854.

[38] Hawken M.P., Muhindi D.W., Chakaya J.M., Bhatt S.M., Ng'ang'a L.W. and Porter J.D. (2001) Under-diagnosis of smear-positive pulmonary tuberculosis in Nairobi, Kenya. Int J Tuberc Lung Dis 5, 360-363.

[39] Herrera M., Senties R., Esquivel E. and Armas J. (1971) [Social problems of the tuberculosis patient in long term care hospitals]. Salud Publica Mex 13, 749-762.

[40] Hill A.V. (2006) Aspects of genetic susceptibility to human infectious diseases. Annu Rev Genet 40, 469-486.

[41] Hochbaum G.M. (1956) Why people seek diagnostic x-rays. Public Health Rep 71, 377-380.

[42] Holmes C.B., Hausler H. and Nunn P. (1998) A review of sex differences in the epidemiology of tuberculosis. Int J Tuberc Lung Dis 2, 96-104.

[43] Hunt L.M., Jordan B., Irwin S. and Browner C.H. (1989) Compliance and the patient's perspective: controlling symptoms in everyday life. Cult Med Psychiatry 13, 315-334.

[44] Janele D., Lang T., Capellino S., Cutolo M., Da Silva J.A. and Straub R.H. (2006) Effects of testosterone, 17beta-estradiol, and downstream estrogens on cytokine secretion from human leukocytes in the presence and absence of cortisol. Ann N Y Acad Sci 1069, 168-182.

[45] Janz N.K. and Becker M.H. (1984) The Health Belief Model: a decade later. Health Educ Q 11, 1-47.

[46] Jasmer R.M., Roemer M., Hamilton J., Bunter J., Braden C.R., Shinnick T.M. and Desmond E.P. (2002) A prospective, multicenter study of laboratory cross-contamination of Mycobacterium tuberculosis cultures. Emerg Infect Dis 8, 1260-1263.

[47] Kendall C. and Thoits P. The impact of culture on the cognitive structure of illness. Cult Med Psychiatry 11, 465-494.

[48] Khan M.S., Dar O., Sismanidis C., Shah K. and Godfrey-Faussett P. (2007) Improvement of tuberculosis case detection and reduction of discrepancies between men and women by simple sputum-submission instructions: a pragmatic randomised controlled trial. Lancet 369, 1955-1960.

[49] Kochi A. (1991) The global tuberculosis situation and the new control strategy of the World Health Organization. Tubercle 72, 1-6.

[50] Kopanoff D.E., Snider D.E., Jr. and Johnson M. (1988) Recurrent tuberculosis: why do patients develop disease again? A United States Public Health Service cooperative survey. Am J Public Health 78, 30-33.

[51] Kumate J. (1990) Las enfermedadestransmisibles. In Salud y crisis en Mexico, pp. 17-39 [SigloVeintiuno, editor. Mexico City: I. Almada Bay.

[52] Kusznierz G.F., Latini O.A. and Sequeira M.D. (2004) Quality assessment of smear microscopy for acid-fast bacilli in the Argentine tuberculosis laboratory network, 1983-2001. Int J Tuberc Lung Dis 8, 1234-1241.

[53] Laszlo A., Rahman M., Espinal M. and Raviglione M. (2002) Quality assurance programme for drug susceptibility testing of Mycobacterium tuberculosis in the WHO/IUATLD Supranational Reference Laboratory Network: five rounds of proficiency testing, 1994-1998. Int J Tuberc Lung Dis 6, 748-756.

[54] Leff A.R. and Leff D.R. (1986) Tuberculosis: a reflection of political institutions and social concerns in the United States. Perspect Biol Med 30, 27-39.

[55] Leone M., Honstettre A., Lepidi H., Capo C., Bayard F., Raoult D. and Mege J.L. (2004) Effect of sex on Coxiella burnetii infection: protective role of 17beta-estradiol. J Infect Dis 189, 339-345.

[56] Lieban R.W. (1976) Traditional medical beliefs and the choice of practitioners in a Philippine city. Soc Sci Med 10, 289-296.

[57] Lienhardt C., Fielding K., Sillah J.S., Bah B., Gustafson P., Warndorff D., Palayew M., Lisse I., Donkor S., Diallo S., Manneh K., Adegbola R., Aaby P., Bah-Sow O., Bennett S. and McAdam K. (2005) Investigation of the risk factors for tuberculosis: a case-control study in three countries in West Africa. Int J Epidemiol 34, 914-923.

[58] Lin C.M., Davidson T.M. and Ancoli-Israel S. (2008) Gender differences in obstructive sleep apnea and treatment implications. Sleep Med Rev 12, 481-496.

[59] Liu P.T., Stenger S., Li H., Wenzel L., Tan B.H., Krutzik S.R., Ochoa M.T., Schauber J., Wu K., Meinken C., Kamen D.L., Wagner M., Bals R., Steinmeyer A., Zugel U., Gallo R.L., Eisenberg D., Hewison M., Hollis B.W., Adams J.S., Bloom B.R. and Modlin R.L. (2006) Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311, 1770-1773.

[60] Marriott I. and Huet-Hudson Y.M. (2006) Sexual dimorphism in innate immune responses to infectious organisms. Immunol Res 34, 177-192.

[61] Martin R., Hearn T.L., Ridderhof J.C. and Demby A. (2005) Implementation of a quality systems approach for laboratory practice in resource-constrained countries. AIDS 19 Suppl 2, S59-65.

[62] Martinez A., Balandrano S., Parissi A., Zuniga A., Sanchez M., Ridderhof J., Lipman H.B. and Madison B. (2005) Evaluation of new external quality assessment guidelines involving random blinded rechecking of acid-fast bacilli smears in a pilot project setting in Mexico. Int J Tuberc Lung Dis 9, 301-305.

[63] Mata J.I. (1985) Integrating the client's perspective in planning a tuberculosis education and treatment program in Honduras. Med Anthropol 9, 57-64.

[64] Maulitz R.C. and Maulitz S.R. (1973) The King's Evil in Oxfordshire. Med Hist 17, 87-89.

[65] McCarthy O.R. (2001) The key to the sanatoria. J R Soc Med 94, 413-417.

[66] McClelland C. (1909) "Galen on Tuberculosis".The Physician and Surgeon. Detroit and Ann Arbor: Keating and Bryant 31, 400-404.

[67] Miller E.N., Jamieson S.E., Joberty C., Fakiola M., Hudson D., Peacock C.S., Cordell H.J., Shaw M.A., Lins-Lainson Z., Shaw J.J., Ramos F., Silveira F. and Blackwell J.M. (2004) Genome-wide scans for leprosy and tuberculosis susceptibility genes in Brazilians. Genes Immun 5, 63-67.

[68] Moysen J.S. and Arroyo Acevedo P. (1984) Critica de la validez de los metodos de deteccion y confirmacion de la tuberculosis pulmonarcomo un problema de saludpublica. SaludPublica de Mexico 26, 546-555.

[69] Mundy C.J., Harries A.D., Banerjee A., Salaniponi F.M., Gilks C.F. and Squire S.B. (2002) Quality assessment of sputum transportation, smear preparation and AFB microscopy in a rural district in Malawi. Int J Tuberc Lung Dis 6, 47-54.

[70] Munyati S.S., Dhoba T., Makanza E.D., Mungofa S., Wellington M., Mutsvangwa J., Gwanzura L., Hakim J., Nyakabau M., Mason P.R., Robertson V., Rusakaniko S., Butterworth A.E. and Corbett E.L. (2005) Chronic cough in primary health care attendees, Harare, Zimbabwe: diagnosis and impact of HIV infection. Clin Infect Dis 40, 1818-1827.

[71] Nashold F.E., Spach K.M., Spanier J.A. and Hayes C.E. (2009) Estrogen controls vitamin D3-mediated resistance to experimental autoimmune encephalomyelitis by controlling vitamin D3 metabolism and receptor expression. J Immunol 183, 3672-3681.

[72] Ober C., Loisel D.A. and Gilad Y. (2008) Sex-specific genetic architecture of human disease. Nat Rev Genet 9, 911-922.

[73] Pamra S.P. (1980) Problems of tuberculosis in developing countries. Clin Chest Med 1, 265-271.

[74] Perkins M.D., Roscigno G. and Zumla A. (2006) Progress towards improved tuberculosis diagnostics for developing countries. Lancet 367, 942-943.

[75] Petti C.A., Polage C.R., Quinn T.C., Ronald A.R. and Sande M.A. (2006) Laboratory medicine in Africa: a barrier to effective health care. Clin Infect Dis 42, 377-382.

[76] Pitchenik A.E. (1984) Monitoring compliance with anti-tuberculosis therapy. N Engl J Med 311, 799.

[77] Ridderhof J.C., Williams L.O., Legois S., Shult P.A., Metchock B., Kubista L.N., Handsfield J.H., Fehd R.J. and Robinson P.H. (2003) Assessment of laboratory performance of nucleic acid amplification tests for detection of Mycobacterium tuberculosis. J Clin Microbiol 41, 5258-5261.

[78] Rieder H.L., Arnadottir T., Tardencilla Gutierrez A.A., Kasalika A.C., Salaniponi F.L., Ba F., Diop A.H., Anagonou S., Gninafon M., Ringdal T., Trebucq A. and Enarson D.A. (1997) Evaluation of a standardized recording tool for sputum smear microscopy for acid-fast bacilli under routine conditions in low income countries. Int J Tuberc Lung Dis 1, 339-345.

[79] Roberts C.W., Walker W. and Alexander J. (2001) Sex-associated hormones and immunity to protozoan parasites. Clin Microbiol Rev 14, 476-488.

[80] Roden A.C., Moser M.T., Tri S.D., Mercader M., Kuntz S.M., Dong H., Hurwitz A.A., McKean D.J., Celis E., Leibovich B.C., Allison J.P. and Kwon E.D. (2004) Augmentation of T cell levels and responses induced by androgen deprivation. J Immunol 173, 6098-6108.

[81] Rosenstock I.M. (1974) Historical origins of the health belief model. In The health belief model and personal health behavior, pp. 1-8 [M.H. Becker and C.B. Slack, editors]. Thorofare, NJ.

[82] Rubel A.J. and Garro L.C. (1992) Social and cultural factors in the successful control of tuberculosis. Public Health Rep 107, 626-636.

[83] Rubel A.J. and O'Nell C.W. (1978) Difficulties of presenting complaints to physicians: susto illness as an example. In Modern medicine and medical anthropology in the United States-Mexico border population, pp. 147-154 [B. Velimirovic, editor]. Washington, DC: Pan American Health Organization.

[84] Ryan K.J. and Ray C.G. (2004) Sherris Medical Microbiology.

[85] San Antonio-Gaddy M., Richardson-Moore A., Burstein G.R., Newman D.R., Branson B.M. and Birkhead G.S. (2006) Rapid HIV antibody testing in the New York State Anonymous HIV Counseling and Testing Program: experience from the field. J Acquir Immune Defic Syndr 43, 446-450.

[86] Schaible U.E., Collins H.L., Priem F. and Kaufmann S.H. (2002) Correction of the iron overload defect in beta-2-microglobulin knockout mice by lactoferrin abolishes their increased susceptibility to tuberculosis. J Exp Med 196, 1507-1513.

[87] Shinnick T.M., Lademarco M. and Ridderhof J.C. (2005) National Plan for Reliable Tuberculosis Laboratory Services Using a Systems Approach: Recommendations from CDC and the Association of Public Health Laboratories Task Force on Tuberculosis Laboratory Services. MMWR Morb Mortal Wkly Rep 541, 12.

[88] Slutkin G. (1986) Management of tuberculosis in urban homeless indigents. Public Health Rep 101, 481-485.

[89] Small P.M., McClenny N.B., Singh S.P., Schoolnik G.K., Tompkins L.S. and Mickelsen P.A. (1993) Molecular strain typing of Mycobacterium tuberculosis to confirm cross-contamination in the mycobacteriology laboratory and modification of procedures to minimize occurrence of false-positive cultures. J Clin Microbiol 31, 1677-1682.

[90] Styblo K. (1989) Overview and epidemiologic assessment of the current global tuberculosis situation with an emphasis on control in developing countries. Rev Infect Dis 11 Suppl 2, S339-346.

[91] Sudre N., ten Dam G. and Kochi A. (1991) Tuberculosis in the present time: a global overview of the tuberculosis situation. Geneva: World Health Organization.

[92] Tsuyuguchi K., Suzuki K., Matsumoto H., Tanaka E., Amitani R. and Kuze F. (2001) Effect of oestrogen on Mycobacterium avium complex pulmonary infection in mice. Clin Exp Immunol 123, 428-434.

[93] Tuberculosis Research Centre M., and National Tuberculosis Institute, Bangalore (1984) A controlled clinical trial of 3- and 5-month regimes in the treatment of sputum positive pulmonary tuberculosis. Ann Rev Respir Dis 130, 1091-1094.

[94] Van Deun A., Kim S.J. and Rieder H.L. (2005) Will the bleach method keep its promise in sputum smear microscopy? Int J Tuberc Lung Dis 9, 700; author reply 700-701.

[95] Van Deun A. and Portaels F. (1998) Limitations and requirements for quality control of sputum smear microscopy for acid-fast bacilli. Int J Tuberc Lung Dis 2, 756-765.

[96] Vidal S.M., Malo D., Vogan K., Skamene E. and Gros P. (1993) Natural resistance to infection with intracellular parasites: isolation of a candidate for Bcg. Cell 73, 469-485.

[97] Weiss M.G., Sommerfeld J. and Uplekar M.W. (2008) Social and cultural dimensions of gender and tuberculosis. Int J Tuberc Lung Dis 12, 829-830.

[98] WHO (1998a) Laboratory services in TB control, Part I: Organization and management. Geneva: World Health Organization.

[99] WHO (1998b) Laboratory services in TB control, Part II: Microscopy. Geneva: World Health Organization.

[100] WHO (1998c) Laboratory services in TB control. Part III: Culture. Geneva: World Health Organization.

[101] WHO (1998d) Laboratory services in tuberculosis control; part I: organization and management. Geneva.

[102] WHO (2004) The WHO/IUATLD Global Project on Anti-Tuberculosis Drug Resistance Surveillance. Anti-tuberculosis drug resistance in the world. Geneva: WHO.

[103] WHO (2005) Global Tuberculosis Control Report: World Health Organization.

[104] WHO (2006) The Stop TB Strategy. Geneva.

[105] WHO (2007) Use of Liquid TB Culture and Drug Susceptibility Testing in Low- and Medium-income Settings: World Health Organization.

[106] WHO (2008a) Policy Guidance on Drug Susceptibility Testing (DST) of Second-line Anti-Tuberculosis Drugs. Geneva: World Health Organization.

[107] WHO (2008b) Policy Statement. Molecular Line Probe Assay for Rapid Screening of Patients at Risk of Multidrug-resistant (MDR) TB. Geneva: World Health Organization.

[108] WHO (2010a) Policy Statement on Fluorescent Light Emitting Diode Microscopy for Diagnosis of Tuberculosis: World Health Organization.

[109] WHO (2010b) Policy Statement on Non-commercial Culture and DST Methods for rapid screening of Patients at Risk of Multidrug-resistant Tuberculosis. Geneva: World Health Organization.

[110] WHO (2011a) Intensifying TB case detection in Ghana.

[111] WHO (2011b) Policy Statement Automated real-time nucleic acid amplification technology for rapid and simultaneous detection of tuberculosis and rifampicin resistance: Xpert MTB/RIF system Geneva: World Health Organization.

[112] Wolfart W. (1990) Surgical treatment of tuberculosis and its modifications—collapse therapy and resection treatment and their present-day sequelae. OffentlGesundheitswes 52, 506–511.

[113] Yamamoto Y., Saito H., Setogawa T. and Tomioka H. (1991) Sex differences in host resistance to Mycobacterium marinum infection in mice. Infect Immun 59, 4089-4096.

[114] Yamamoto Y., Tomioka H., Sato K., Saito H., Yamada Y. and Setogawa T. (1990) Sex differences in the susceptibility of mice to infection induced by Mycobacterium intracellulare. Am Rev Respir Dis 142, 430-433.

[115] Young J.C. and Garro L.Y. (1982) Variation in the choice of treatment in two Mexican communities. Soc Sci Med 16, 1453-1465.

[116] Zimmermann M.B. and Hurrell R.F. (2007) Nutritional iron deficiency. Lancet 370, 511-520.

[117] Zink A.R., Sola C., Reischl U., Grabner W., Rastogi N., Wolf H. and Nerlich A.G. (2003) Characterization of Mycobacterium tuberculosis complex DNAs from Egyptian mummies by spoligotyping. J Clin Microbiol 41, 359-367.