Skip to main content

Archived Comments for: Parallel assessment of male reproductive function in workers and wild rats exposed to pesticides in banana plantations in Guadeloupe

Back to article

  1. Sentinel species for male reproductive disorders

    Michael Joffe, Imperial College London

    8 August 2008

    Dear Sir

    Multigner et al. are to be congratulated on their pioneering study on male reproductive parameters both in rats and in humans, comparing those highly exposed to pesticides in a banana plantation with those who are not highly exposed [1]. Their intention to investigate how well rats perform as sentinel indicators for humans is important.

    However, their findings cannot be taken at face value, because the two species are not comparable in respect of the developmental stage at which they were exposed to pesticides. One cannot be certain, but it appears that the men were exposed only as adults, whereas it is clear that the rats had been highly exposed at all stages of development as they were conceived in the banana plantation and grew up there. As it is highly likely that the male reproductive system is most susceptible to toxic insult in the early stages of development, their findings of a significantly lower serum concentration of serum testosterone in the rats, but not in the humans, could merely reflect differing stages of exposure, not a species difference. Stage of development at the time of exposure is barely mentioned in the paper, at the end of the penultimate paragraph of the Discussion section.

    Another issue is the framing of the problem, which is subject to the vagueness that unfortunately characterises the literature on male reproduction. Early toxic exposure leading to a low adult serum concentration of testosterone could occur by means of any mechanism that reduces the quantity of hormone-secreting tissue in the testis. It does not have to be via an endocrine disrupting mechanism. So why is male reproductive toxicity described from the perspective of endocrine disruption? Even DBCP is described as “not formally identified as [an] endocrine disruptor”, suggesting that this could be its mode of action, when it is a known mutagen that causes dominant lethal mutations [2,3].

    Similarly, in the opening paragraph there is the customary reference to the rise in testicular cancer, as if this were relevant to the type of pesticide exposure that is the focus of the study. The rise in this disease, which has been dramatic – at least a four-fold increase in a matter of decades, in a large number of countries – started 100 years ago in continental Europe [4] and even earlier in England and Wales [5]. A large proportion of this increase had occurred before the introduction of any of the modern classes of pesticides (or any suggested endocrine disruptors such as phthalates). Even if pesticides affect the testicular cancer risk [6] they do not come close to explaining the basic epidemiological findings.

    Returning to the question of sentinel species, one of the puzzles of testicular cancer is that no satisfactory animal model has ever been found, despite the high degree of conservation of the male reproductive system in mammalian evolution.

    Yours sincerely

    Michael Joffe

    PS: the references need checking – some authors’ names are mis-spelt, and several other details are wrong.


    1. Multigner L, Kadhel P, Pascal M, Huc-Terki F, Kercret H, Massart C, Janky E, Auger J, Jégou B. Parallel assessment of male reproductive function in workers and wild rats. Environmental Health, 2008; 7: 40.

    2. Whorton MD, Foliart DE. Mutagenicity, carcinogenicity and reproductive effects of dibromochloropropane (DBCP). Mutat Res 1983; 123: 13-30.

    3. Ryu J-C, Kim Y-J, Chai Y-G. Mutation spectrum of 1,2-dibromo-3-chloropropane, an endocrine disruptor, in the lacI transgenic Big Blue Rat2 fibroblast cell line. Mutagenesis 2002; 17: 301-07.

    4. Bergström R, Adami H-O, Möhner M, et al. Increase in testicular cancer incidence in six European countries: a birth cohort phenomenon. J Natl Cancer Inst 1996; 88: 727-33.

    5. Davies JM. Testicular cancer in England and Wales: some epidemiological aspects. Lancet 1981; i: 928-32.

    6. Hardell L, van Bavel B, Lindstrom G, Carlberg M, Dreifaldt AC, Wijkstrom H, Starkhammar H, Eriksson M, Hallquist A, Kolmert T. Increased concentrations of polychlorinated biphenyls, hexachlorobenzene, and chlordanes in mothers of men with testicular cancer. Environ Health Perspect 2003; 111: 930-34.

    Competing interests

    I have no competing interests

  2. Response to Dr Joffe's coments

    Luc Multigner, INSERM

    8 August 2008

    We thank Dr Joffe for his comments, with which we largely agree. We have stressed in our publication that the comparative physiology, nature of exposure, development stage at exposure, and a number of ecological factors are of course different between human and rat. These differences must be considered when interpreting wild animals as sentinel species for human health risks. Our study, we feel, makes that abundantly clear, being essentially a prototype in advance of more detailed investigations to come. Concerning testicular cancer, our references to this topic and to the apparent decline in semen quality were made to situate our work in a more general context for readers interested in human reproductive health. We also agree with Dr Joffe that although the influence of substances with endocrine activity is a prevalent hypothesis to explain the worrying trends in male reproductive health, other contributing factors must also be considered [1]

    L Multigner, P Kadhel, Ml Pascal, F Huc-Terki, H Kercret, C Massart, E Janky, J Auger,and B Jégou.

    [1]Joffe M. Are problems with male reproductive health caused by endocrine disruption? Occup Environ Med, 2001; 58: 281-287

    Competing interests