Transgenic cotton and farmers’ health in Pakistan

Autoři: Shahzad Kouser aff001;  David J. Spielman aff002;  Matin Qaim aff003
Působiště autorů: Department of Economics, COMSATS University Islamabad, Islamabad, Pakistan aff001;  Environment and Production Technology Division, International Food Policy Research Institute, Washington, DC, United States of America aff002;  Department of Agricultural Economics and Rural Development, University of Goettingen, Germany aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Despite substantial research on the economic effects of transgenic insect-resistant Bacillus thuringiensis (Bt) cotton, there is still limited work on this technology’s impacts on human health. Due to the inbuilt insect resistance, Bt cotton requires fewer pesticide sprays than conventional cotton, which is not only advantageous from economic and environmental perspectives, but may also result in health benefits for farmers. Using socioeconomic and biophysical data from Pakistan, we provide the first evidence of a direct association between Bt gene expression in the plant and health benefits. A key feature of this study is that Bt cotton cultivation in Pakistan occurs in a poorly regulated market: farmers are often mistaken in their beliefs about whether they have planted Bt cotton or conventional cotton, which may affect their pesticide-use strategies and thus their pesticide exposure. We employ a cost-of-illness approach and variations in the measurement of Bt adoption to estimate the relationship between Bt cotton and farmers’ health. Bt adoption based on farmers’ beliefs does not reduce the pesticide-induced cost of illness. However, adoption based on measuring Bt gene expression is associated with significant health cost savings. Extrapolating the estimates for true Bt seeds to Pakistan’s entire Bt cotton area results in annual health cost savings of around US$ 7 million. These findings have important implications for the regulation of seed markets in Pakistan and beyond: improved regulations that ensure claimed crop traits are really expressed can increase the benefits for farmers and society at large.

Klíčová slova:

Agricultural workers – Cotton – Crops – Fiber crops – Gene expression – Health economics – Toxins – Pesticides


1. Zehr UB. Cotton: Biotechnological Advances. Heidelberg: Springer. 2010.

2. Morse S, Bennett R, Ismael Y. Why Bt cotton pays for small-scale farmers in South Africa. Nat. Biotechnol. 2004; 22: 379–380.

3. Lu Y, Wu K, Jiang Y, Guo Y, Desneux N. Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature. 2012; 487: 362–367. doi: 10.1038/nature11153 22722864

4. Huang J, Chen R, Qiao F, Su H, Wu K. Does expression of Bt toxin matter in farmer's pesticide use? Plant Biotechnol. J. 2014; 12(4): 399–401. doi: 10.1111/pbi.12189 24702829

5. Klümper W, Qaim M. A meta-analysis of the impacts of genetically modified crops. PLoS ONE. 2014; 9(11): e111629. doi: 10.1371/journal.pone.0111629 25365303

6. Kouser S, Qaim M. Bt cotton, damage control and optimal levels of pesticide use in Pakistan. Environ. Dev. Econ. 2014; 19(6): 704–723.

7. Kouser S, Qaim M. Valuing financial, health, and environmental benefits of Bt cotton in Pakistan. Agric. Econ. 2013; 44(3): 323–335.

8. Brethour C, Weersink A. An economic evaluation of the environmental benefits from pesticide reduction. Agric. Econ. 2001: 25; 219–226.

9. Pemsl DE, Gutierrez AP, Waibel H. The economics of biotechnology under ecosystem disruption. Ecol. Econ. 2008; 66: 177–183.

10. Yao Y-S, Han P, Niu C-Y, Dong Y-C, Gao X-W, Cui J-J, et al. Transgenic Bt cotton does not disrupt the top-down forces regulating the cotton aphid in Central China. PLoS ONE. 2016; 11(11): e0166771. doi: 10.1371/journal.pone.0166771 27870914

11. Wei J, Zhang L, Yang S, Xie B, An S, Liang G. Assessment of the lethal and sublethal effects by spinetoram on cotton bollworm. PLoS ONE. 2018; 13(9): e0204154. doi: 10.1371/journal.pone.0204154 30216388

12. Damalas CA, Eleftherohorinos IG. Pesticide exposure, safety issues, and risk assessment indicators. Int. J. Environ. Res. Public Health. 2011; 8: 1402–1419. doi: 10.3390/ijerph8051402 21655127

13. Gesesew HA, Woldemichael K, Massa D, Mwanri L. Farmers knowledge, attitudes, practices and health problems associated with pesticide use in rural irrigation villages, Southwest Ethiopia. PLoS ONE. 2016; 11(9): e0162527. doi: 10.1371/journal.pone.0162527 27622668

14. Hu R, Huang X, Huang J, Li Y, Zhang C, Yin Y, et al. Long- and short-term health effects of pesticide exposure: A cohort study from China. PLoS ONE. 2015; 10(6): e0128766. doi: 10.1371/journal.pone.0128766 26042669

15. Pingali PL, Marquez CB, Palis FG. Pesticides and Philippine rice farmer health: a medical and economic analysis. Am. J. Agric. Econ. 1994; 76: 587–592.

16. Abedullah, Kouser S, Qaim M. Bt cotton, pesticide use, and environmental efficiency in Pakistan. J. Agric. Econ. 2015; 66(1): 66–86.

17. Cuyno L, Norton GW, Rola A. Economic analysis of environmental benefits of integrated pest management: A Philippine case study. Agric. Econ. 2001; 25: 227–233.

18. Maumbe BM, Swinton SM. Hidden health costs of pesticide use in Zimbabwe’s smallholder cotton growers. Soc. Sci. Med. 2003; 57: 1559–1571. doi: 10.1016/s0277-9536(03)00016-9 12948567

19. Pingali PL, Marquez CB, Palis FG. Pesticides and Philippine rice farmer health: a medical and economic analysis. Am. J. Agric. Econ. 1994; 76: 587–592.

20. Pray C, Huang J, Hu R, Rozelle S. Five years of Bt cotton in China—the benefits continue. Plant J. 2002; 31: 423–430. doi: 10.1046/j.1365-313x.2002.01401.x 12182701

21. Huang J, Hu R, Pray C, Qiao F, Rozelle S. Biotechnology as an alternative to chemical pesticides: a case study of Bt cotton in China. Agric. Econ. 2003; 29: 55–67.

22. Bennett R, Buthelezi T, Ismael Y, Morse S. Bt cotton, pesticides, labour and health: a case study of smallholder farmers in the Makhathini Flats, Republic of South Africa. Outlook Agric. 2003; 32: 123–128.

23. Hossain F, Pray C, Lu Y, Huang J, Fan C, Hu R. Genetically modified cotton and farmers’ health in China. Int. J. Occup. Environ. Health. 2004; 10: 296–303. doi: 10.1179/oeh.2004.10.3.296 15473084

24. Kouser S, Qaim M. Impact of Bt cotton on pesticide poisoning in smallholder agriculture: a panel data analysis. Ecol. Econ. 2011; 70(11): 2105–2113.

25. Bourguet D, Guillemaud T. The hidden and external costs of pesticide use. Sustain. Agric. Rev. 2016; 19: 35–120.

26. Lee WJ, Cha ES, Park J, Ko Y, Kim HJ, Kim J. Incidence of acute occupational pesticide poisoning among male farmers in South Korea. Am. J. Ind. Med. 2012; 55: 799–807. doi: 10.1002/ajim.22024 22354866

27. Ma X, Smale M, Spielman DJ, Zambrano P, Nazli H, Zaidi F. A question of integrity: variants of Bt cotton, pesticides, and productivity in Pakistan. J. Agric. Econ. 2017; 68(2): 366–385.

28. Pemsl D, Voelker M, Wu L, Waibel H. Long-term impact of Bt cotton: findings from a case study in China using panel data. Int. J. Agric. Sustain. 2011; 9: 508–521.

29. Spielman DJ, Zaidi F, Zambrano P, Khan AA, Ali S, Cheema HMN, et al. What are farmers really planting? measuring the presence and effectiveness of Bt cotton in Pakistan. PLoS ONE. 2017; 12(5): e0176592. doi: 10.1371/journal.pone.0176592 28472094

30. Veettil PC, Krishna VV, Qaim M. Ecosystem impacts of pesticide reductions through Bt cotton adoption. Aust. J. Agric. Resour. Econ. 2017; 61: 115–134.

31. Herring RJ. Stealth seeds: bioproperty, biosafety, biopolitics. J. Dev. Stud. 2007; 43(1): 130–157.

32. Ashour M, Gilligan DO, Hoel JB, Karachiwalla NI. Do beliefs about herbicide quality correspond with actual quality in local markets? Evidence from Uganda. J. Dev. Stud. 2019; 55(6): 1285–1306.

33. Bold T, Kaizzi KC, Svensson J, Yanagizawa-Drott D. Lemon technologies and adoption: measurement, theory and evidence from agricultural markets in Uganda. Q. J. Econ. 2017; 132(3): 1055–1100.

34. Herring R, Paarlberg R. The political economy of biotechnology. Annu. Rev. Resour. Econ. 2016; 8: 307–416.

35. GoP. Pakistan Economic Survey 2014–15. Ministry of Finance, Government of Pakistan, Islamabad. 2015. Available from

36. Jabbar A, Mallick S. Pesticides and environment situation in Pakistan. Sustainable Development Policy Institute (SDPI). 1994. Working Paper Series No. 19.

37. NFDC. Pesticide use survey report 2002. 2002. National Fertilizer Development Center (NFDC) Government of Pakistan, Islamabad, Pakistan.

38. Arshad M, Suhail A, Arif MJ, Khan MA. Transgenic-Bt and non-transgenic cotton effects on survival and growth of Helicoverpa armigera. Int. J. Agric. Biol. 2009; 11: 473–476.

39. Karim S. Management of Helicoverpa armigera: a review and prospectus for Pakistan. Pak. J. Biol. Sci. 2000; 3: 1213–1222.

40. Khan MA, Iqbal M, Ahmad I, Soomro MH, Chaudhary MA. Economic evaluation of pesticide use externalities in the cotton zones of Punjab, Pakistan. Pak. Dev. Rev. 2002; 41: 683–698.

41. Khan M, Damalas CA. Occupational exposure to pesticides and resultant health problems among cotton farmers of Punjab, Pakistan. Int. J. Environ. Health Res. 2015; 25(5): 508–521. doi: 10.1080/09603123.2014.980781 25397689

42. Bakhsh K, Ahmad N, Tabasum S, Hassan S, Hassan I. Health hazards and adoption of personal protective equipment during cotton harvesting in Pakistan. Sci. Total Environ. 2017; 598: 1058–1064. doi: 10.1016/j.scitotenv.2017.04.043 28482453

43. Khan M, Damalas CA. Farmers’ knowledge about common pests and pesticide safety in conventional cotton production in Pakistan. Crop Prot. 2015; 77: 45–51.

44. Khan M, Mahmood HZ, Damalas CA. Pesticide use and risk perceptions among farmers in the cotton belt of Punjab, Pakistan. Crop Prot. 2015; 67: 184–190.

45. Saeed MF, Shaheen M, Ahmad I, Zakir A, Nadeem M, Chishti AA, et al. Pesticide exposure in the local community of Vehari District in Pakistan: an assessment of knowledge and residues in human blood. Sci. Total Environ. 2017; 587–588: 137–144. doi: 10.1016/j.scitotenv.2017.02.086 28237471

46. Hayat K, Afzal M, Aqueel MA, Ali S, Saeed MF, Qureshi AK, et al. Insecticide toxic effects and blood biochemical alterations in occupationally exposed individuals in Punjab, Pakistan. Sci. Total Environ. 2019; 655: 106–111.

47. Bakhsh K, Ahmad N, Kamran MA, Hassan S, Abbas Q, Saeed R, et al. Occupational hazards and health cost of women cotton pickers in Pakistani Punjab. BMC Public Helath. 2016; 16: 1–11.

48. Memon QUA, Wagan SA, Chunyu D, Shuangxi X, Jingdong L, Damalas CA. Health problems from pesticide exposure and personal protective measures among women cotton workers in southern Pakistan. Sci. Total Environ. 2019; 685: 659–666. doi: 10.1016/j.scitotenv.2019.05.173 31200258

49. Khan MA, Iqbal M, Ahmad I. Environment-friendly cotton production through implementing integrated pest management approach. Pak. Dev. Rev. 2007; 46: 1119–1135.

50. Rana MA. The Seed industry in Pakistan: regulation, politics and entrepreneurship. Pakistan Strategy Support Program Working Paper 19. 2014. Washington, DC: International Food Policy Research Institute.

51. Spielman DJ, Nazli H, Ma X, Zambrano P, Zaidi F. Technological opportunity, regulatory uncertainty, and Bt cotton in Pakistan. AgBioForum 2015; 18(1): 98–112.

52. Ishtiaq M, Saleem MA. Generating susceptible strain and resistance status of field populations of Spodoptera exigua (Lepidoptera: Noctuidae) against some conventional and new chemistry insecticides in Pakistan. J. Econ. Entomol. 2011; 104: 1343–1348. doi: 10.1603/ec10383 21882702

53. Ali A, Abdulai A. The adoption of genetically modified cotton and poverty reduction in Pakistan. J. Agric. Econ. 2010; 61: 175–192.

54. Bakhsh K. Impacts of Bt cotton on profitability, productivity and farm inputs in Pakistan: use of panel models. Environ. Dev. Econ. 2017; 22(4): 373–391.

55. ISAAA. Global Status of Commercialized Biotech/GM Crops in 2017. 2017. ISAAA Briefs No. 53, International Service for the Acquisition of Agri-Biotech Applications, Ithaca NY.

56. Abedullah, Kouser S, Ali H. Pesticide or wastewater: which one is a bigger culprit for acute health symptoms among vegetable growers in Pakistan's Punjab? Hum. Ecol. Risk. Assess. 2016; 22(4): 941–957.

57. Asfaw S, Mithöfer D, Waibel H. Agrifood supply chain, private‐sector standards, and farmers’ health: evidence from Kenya. Agric. Econ. 2010; 41: 251–263.

58. Athukorala W, Wilson C, Robinson T. Determinants of health costs due to farmers’ exposure to pesticides: an empirical analysis. J. Agric. Econ. 2012; 63: 158–174.

59. Wilson C. Empirical evidence showing the relationships between three approaches for pollution control. Environ. Resour. Econ. 2003; 4: 97–101.

60. Garming H, Waibel H. Pesticides and farmer health in Nicaragua—a willingness-to-pay approach to evaluation. Eur. J. Health Econ. 2008; 10(2): 125–133. doi: 10.1007/s10198-008-0110-9 18521638

61. Khan M. Economic evaluation of health cost of pesticide use: willingness to pay method. Pak. Dev. Rev. 2009; 48(4): 459–470.

62. Khan M, Damalas CA. Farmers' willingness to pay for less health risks by pesticide use: a case study from the cotton belt of Punjab, Pakistan. Sci. Total Environ. 2015; 530–531: 297–303. doi: 10.1016/j.scitotenv.2015.05.110 26047864

63. Wooldridge JM. Econometric Analysis of Cross Section and Panel Data. Cambridge: The MIT Press. 2002.

64. Krishna VV, Qaim M. Potential impacts of Bt eggplant on economic surplus and farmers’ health in India. Agric. Econ. 2008; 38(3): 167–180.

65. Atreya K. Health costs from short-term exposure to pesticides in Nepal. Soc. Sci. Med. 2008; 67: 511–519. doi: 10.1016/j.socscimed.2008.04.005 18514373

66. Cragg JG. Some statistical models for limited dependent variables with application to the demand for durable goods. Econometrica. 1971; 1: 829–844.

67. Cooper JC, Keim RW. Incentive payments to encourage farmer adoption of water quality protection practices. Am. J. Agric. Econ. 1996; 78(1): 54–64.

68. Shiferaw BA, Kebede TA, You L. Technology adoption under seed access constraints and the economic impacts of improved pigeonpea varieties in Tanzania. Agric. Econ. 2008: 39(3): 309–323.

69. Xu Z, Burke WJ, Jayne TS, Govereh J. Do input subsidy programs “crowd in” or “crowd out” commercial market development? Modeling fertilizer demand in a two‐channel marketing system. Agric. Econ. 2009; 40(1): 79–94.

70. Gebregziabher G, Holden S. Does irrigation enhance and food deficits discourage fertilizer adoption in a risky environment? Evidence from Tigray, Ethiopia. J. Dev. Agric. Econ. 2011; 3(10): 514–528.

71. Ricker-Gilbert J, Jayne TS, Chirwa E. Subsidies and crowding out: A double-hurdle model of fertilizer demand in Malawi. Am. J. Agric. Econ. 2011; 93(1): 26–42.

72. Noltze M, Schwarze S, Qaim M. Understanding the adoption of system technologies in smallholder agriculture: the system of rice intensification (SRI) in Timor Leste. Agric. Syst. 2012; 108(1): 64–73.

73. Rao EJO, Qaim M. Supermarkets and agricultural labor demand in Kenya: A gendered perspective. Food Policy 2013; 38: 165–176.

74. Kouser S, Abedullah, Qaim M. Bt cotton and employment effects for female agricultural laborers in Pakistan. New Biotechnol. 2017; 34: 40–46.

75. Jones AM. A double hurdle model of cigarette consumption. J. Appl. Economet. 1989; 4(1): 23–39.

76. Burke WJ. Fitting and interpreting Cragg’s Tobit alternative using Stata. Stata J. 2009; 9(4): 584–592.

77. Maredia M, Reyes BA, Manu-Aduening J, Dankyi A, Hamazakaza P, Muimui K, et al. Testing alternative methods of varietal identification using DNA fingerprinting: Results of pilot studies in Ghana and Zambia. International Development Working Papers No. 246950. 2016. East Lansing, MI: Michigan State University.

78. Kranthi KR, Naidu S, Dhawad C, Tatwawadi A, Mate K, Patil E, et al. Temporal and intra-plant variability of Cry1Ac expression in Bt-cotton and its influence on the survival of the cotton bollworm, Helicoverpa armigera (Hubner) (Noctuidae: Lepidoptera). Curr. Sci. 2005; 89(2): 291–298.

79. Xu N, Fok M, Baid L, Zhoua Z. Effectiveness and chemical pest control of Bt cotton in the Yangtze River Valley, China. Crop Prot. 2008; 27(9): 1269–127.

80. Ali S, Shah SH, Ali GM, Iqbal A, Asad M, Zafar Y. Bt Cry toxin expression profile in selected Pakistani cotton genotypes. Curr. Sci. 2012; 102(12): 1632–1636.

81. Zhang C, Hu R, Huang J, Huang X, Shi G, Li Y, et al. Health effect of agricultural pesticide use in China: implications for the development of GM crops. Scientific Reports. 2016; 6(34918): 1–8.

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden