The Effect of Chemical Warfare Agents on the Immune System of Survivors in Halabja

Salih A. Hama1, Bahrouz M.A. Al-Jaff2, Bakhtiar M. Mahmud3

College of Science, University of Sulaimani, 2 College of Education, Kalar, 3 College of Medicine, University of Sulaimani

To evaluate the incidence of immunocompetence, including cell-mediated and antibody fitness, among
survivors of the chemical bombardment of Halabja in the Kurdistan region of Iraq, forty exposed and forty
unexposed subjects regarded as controls were studied to determine their immune system status 12 years after
bombardment. Skin reactivity to tuberculin, D.T.P. vaccine, T.T toxoid and measles vaccine was negative in
62.5% of the exposed cases in compare to unexposed persons who showed no negative reactions 0%. The
total leukocyte count was normal among 70% of exposed cases, whereas the total lymphocyte count was within

sub-normal ranges in 80% of exposed cases. All the subjects displaying negative skin reactions had sub-
normal lymphocyte counts, which reflect impaired cell-mediated immunity. The immunoglobulin assay for

exposed cases revealed sub-normal values for IgG (12.5%) and IgA (52.5%), while the IgM level was above
the normal range in 22.5% of cases when compared to that of controls that showed no abnormal values. This
result revealed that there was a deficiency in antibody-mediated immunity. There were significant differences
between the exposed and the control samples with respect to total leukocytes (p = 11× 10-5), neutrophil count
(p = 0.88 × 10-3), lymphocyte count (p = 0.0), IgG (p = 0. 74 × 10-10) and IgA (p = 0. 1 × 10-10). The
immunological reactions were more closely related to the effects of mustard gas, which appeared to be long

Keywords: Chemical warfare; Immune system; Immunocompromised patients;
Immunocompetence; Cell-mediated immunity; Antibody-mediated immunity


 1.         Papirmeister B, Feister AJ & Robinson SI. Medical defense against mustard gas: toxic mechanisms and pharmacological implications. Boca Raton, CRC press. 1991.

2.         Atkinson WS. Delayed keratitis due to mustard gas. Arch. Ophthalmology 194838: 291-301. 3. Medema J. Mustard gas, the science of H. Nuclear, Biological, and Chemical defense. Technol Int 1986; 1: 66-71.

4.         Dickman S. Nerve gas could hang over West German farms. Nature 1988; 332: 573.

5.         Stewart M.J. Report on cases of poisoning by mustard gas (dichloroethyl sulfide) with special reference to the histological changes and to alterations in the leukocyte count. Chemical Warfare Medical Committee (London). Report 17. As cited In: Smith H. In: Review of the literature on the systemic action of mustard gas to August1, 1943. OSRD. Report No. 1717. Prepared for the Office of Scientific New York: Research and Development, 1918. 

6.         Krumbhar EB. Bone marrow changes in mustard gas poisoning. J Am Med Assoc1919; 73: 715.

7.         Anslow WP & Houck CR. Systemic pharmacology and pathology of sulfur and nitrogen mustard. In: Renshaw B. ed. Chemical warfare Agents, and Related Chemical Problems. Office of Scientific Research and Development, Summary Technical Report of Division 9. Washington, DC, National Defence Research Committee.1946.

8.         Alexander SF. Medciel Report of the Bariharbor mustard casualties. Military Surgeon 1947; 101: 1-17.

9.         Philips FS. Recent contributions to the pharmacology of bis (2-halo ethyl)-amines and sulfides. J Pharmacol and Exper ther 1950; 99: 218-323.

10.      Balali M. First report of delayed toxic effects of yperite poisoning in Iranian fighters. In: Heyndricks B. ed. Terrorism: Analysis and Detection of Explosives. Proceedings of the Second World Congress on New Compounds in Biological and Chemical Warfare. Gent, Belgie, Rijks Universiteit, 1987: 489.

11.      Eisenmenger W., Drasch G, von Clarmann M, Kretschmer E & Roider G. Clinical and morphological findings on mustard gas [bis(2-chloroethyl)sulfide] poisoning. J Forensic Sci, 1688, 36,.

12.      Zandieh T, Marzban S, Tarabad F & Ansari H. Defects of cell-mediated immunity in mustard gas injury after years. Scand J Immunol 1990; 32: 423.

13.      Smith KJ, Hurst CG, Moeller RB, Skelton HG & Sidell FR. Sulfur mustard: its continuing threat as a chemical warfare agent, the cutaneous lesions induced, progress in understanding its mechanism of action, its long-term health effects, and new developments for protection and therapy. J Am Acad Dermatol 1995; 32: 765-76

14.      Davidsohn I & Nelson DA. Methods used in the study of blood. In: Davidsohn I & Henry J, Saunders Company WB. ed, Clinical Diagnosis by Laboratory methods 15th. Philadelphia, Saunder 1974:100.

15.      Buckley CE. Delayed Hypersensitivity Skin Testing. In: Rose NR. ed, Manual of Clinical Laboratory Immunology. 3rd. Washington. DC, American Society for Microbiology, 1986

16.      WHO Scientific group. Primary immundeficiency diseases. Clin Exp Immunol, 1995, 99, S2-24.

17.      Buffone GJ. Immunonephelometric and turbidometric measurement of specific plasma proteins. In: Rose NR, and. Friedman H. eds, Manual of Clinical Immunology 2nd. Washington DC, American Society for Microbiology, 1980:23

18.      Foster RC & Ledue TB. Turbidimetry. In: Manual of Clinical Laboratory Immunology 3rd ed. Rose NR, Friedman H & Fahey JL, Washington, DC, American Society for Microbiology, 1986:25

19.      Blank JA, Joiner RL, Houchens DP, Dill GS & Hobson DW. Comparative immunotoxicity of 2,2'-dichlorodiethyl sulfide and cyclophosphamide: evaluation of L1210 tumor cell resistance, cell-mediated immunity, and humoral immunity. Int J Immunopharmacol 1991;13: 251-57.

20.      Kindred I.E. Histologic changes occurring in the haematopoitic organs of albino rats after single injections of 2-chlorethyl vesicants: a quantitative study. Archives of Pathology 1947; 43:253-95.

21.      Dean JH & Murray MJ. Toxic responses of the immune system. In: Amdur MO, Doull J & Klaassen CD, ed. Casarett and Doull's Toxicology. New York, Pergamon, 1991.

22.      Dacre J.C. & Goldman M. Toxicology and pharmacology of the chemical warfare agent sulfur mustard. Pharmacol Rev 1996; 48, 289.

23.      Hektoen L & Corper HC The effect of mustard gas (dichloroethyl sulfide) on antibody formation. J Infect Dis 1920; 28: 279.

24.      Spurr CL. Influence of nitrogen mustards on human tumors and tissues. Cancer 1947; 1, 383-98.

25.      Coutelier JP, Lison D, Simon O & Willems J. Effect of sulfur mustard on murine lymphocytes. Toxicol Lett 1991; 58: 143.

26.      Huntley CC & Lyerly A. Immunoglobulins determinations in allergic children. Am J Dis Child 1963; 106: 545-52.

27.      Infante AJ & Kamani NR. The evaluation of suspected immune deficiency by the primary care physician. Compr Ther 1997; 23: 89-94.

28.      Buckley RH. Primary immunodeficiency diseases due to defects in lymphocytes. N Engl J Med 2000; 343 (18) 1313-24. 29. Notarangelo LD, Duse M & Ugazio AG. Immunodeficiency with hyper-IgM (HIM). Immunodefic Rev1992; 3: 101-21.

30.      Harigel, Gert G., The Concept of Weapons of Mass Destruction: Chemical and Biological Weapons, Use in Warfare, Impact on Society and Environment, presented at the Conference on Biosecurity and ioterrorism, Istituto Diplomatico “Mario Toscano,” Rome, Italy, September 18–19, 2000.

Pianin, Eric, “Toxic Chemicals’ Security Worries Officials,” Washington Post, November 12, 2001, p.  14. 32. Karasik K. Toxic Warefare. Library of Congress Cataloging-in-Publication Data. RAND. USA: 2002