Swan, SH, RL Kruse, L Fan, DB Barr, EZ Drobnis, JB Redmon, C Wang, C Brazil and JW Overstreet and the Study for the Future of Families Research Group. 2003. Semen quality in relation to biomarkers of pesticide exposure. Environmental Health Perspectives.

Swan, SH, C Brazil, EZ Brobnis, F Liu, RL Kruse, M Hatch, JB Redmon, C Wang, JW Overstreet, and the Study for Future Families Research Group. 2003. Geographic differences in semen quality of fertile US males. Environmental Health Perspectives 111. doi:10.1289/ehp.5927

In the most sophisticated study of geographic variation in US sperm count yet conducted, scientists from four different geographic regions across America report they find important differences in sperm density and motility. Men in Missouri have the lowest sperm count compared to New York, Minneapolis and Los Angeles. The cause of these differences are not yet known. The scientists conducting the study hypothesize it may be related to the intensity of pesticide use in industrial agriculture in Missouri compared to the other, more urban areas. More...

Guo, YL, PC Hsu, CC Hsu and GH Lambert. 2000. Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. The Lancet 356:

Guo et al. revisit the children exposed in the womb to PCBs and dibenzofurans because their mothers had ingested contaminated rice wine in Taiwan in 1979, examining aspects of the sperm of boys 16+ yrs old and comparing these with unexposed counterparts. They find significant impacts on sperm quality but not sperm quantity, with increases in the percentage of abnormally-formed sperm, decreases in motility and decreases in sperm strength in the exposed cohorts compared to normal boys.

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Swan et al. revisit the controversy launched by the 1992 paper by Carlsen et al. that reported a large average decline in sperm count from studies around the world. In this paper, they add 47 studies to the data set and repeat the multivariate statistical analysis reported by Swan et al. in 1997. Their results are remarkably consistent with both the original Carlsen et al. paper and the subsequent Swan et al. reanalysis: on average, human sperm density has declined significantly over the past 5 decades. The congruence of the results suggests that the overall results do not rest upon any particular data set within the study, supporting the general robustness of the original conclusions. More...

Andersen, AG, TK Jensen, E Carlsen, N Jørgensen, AM Andersson, T Krarup, N Keiding and NE Skakkebæk. 2000. High frequency of sub-optimal semen quality in an unselected population of young men. Human Reproduction 15(2): 366-372.

This study found a median sperm concentration of 41 million sperm per ml (mean =57.4 m/ml) among young men in Denmark participating in a compulsory medical examination for military service. Sperm count of normal, healthy young men is often above 100 million/ml.

It is important for two reasons:

• Almost all other studies are of men participating because of aspects of their reproductive status. Hence they are not a representative sample of the population at large and may contain significant biases (for example, Acacio et al., or Fisch et al., below).
• The sperm counts revealed are extraordinarily low for healthy young men. "Among men with no history of reproductive diseases and a period of abstinence above 48 h, as many as 18% and 40% respectively had concentrations below 20 and 40 million/ml." Recent data suggest that reproductive impairment begins to appear when sperm counts drop beneath 40 million per ml.

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Acacio, BD, T Gottfried, R Israel and RZ Sokol. 2000. Evaluation of a large cohort of men presenting for a screening semen analysis. Fertility and Sterility 73:595-597.

This paper purports to demonstrate that there has been no change in sperm count the Los Angeles area over the past several decades. The authors measured sperm count in male patients at an infertility clinic over a three year time period (1994-97) and compared their results with data from 1951.

The methodology, however, makes it impossible to support their conclusion with the data presented. Unfortunately, several newspapers carried stories about this finding, presenting it as additional evidence that sperm count is not declining. They used a measurement technique known to produce high counts, and their sample of men was biased. More...

Shanna Swan has emerged as an important analytical voice in the scientific debate over trends in semen quality. Trained as a statistician and a reproductive epidemiologist, she was brought into this issue at the request of the National Research Council as an independent and widely respected analyst who could evaluate the many competing viewpoints on whether sperm quality or density had declined. As a newcomer to the sperm count debate, she had no stake in its outcome. She expected, at the outset, that a rigorous, independent review of the data would reveal that were no trends.

"Thus further analysis of these studies supports a significant decline in sperm density in the United States and Europe. However, some intraregional differences were as large as mean decline in sperm density between 1938 and 1990, and recent reports from Europe and the United States further support large interarea differences in sperm density. Identifying the cause(s) of these regional and temporal differences, whether environmental or other, is clearly warranted."

This paper analyzes several of the assumptions made in uses of existing sperm count data in studies of global trends.

"Critics [of Carlsen et al.] suggested that historical methods (of counting sperm or conducting studies) were variable and unreliable, differing from modern methods both qualitatively and quantitatively. To address this issue we analyzed these studies for trends in counting methods or their variability. We found neither. Alternative analyses produced some differences in trend estimates, but statistical factors alone could not count for the total decline in sperm density. We reviewed the study populations to identify trends in population characteristics, such as abstinence time, that might explain the decline. However, controlling analytically for such factors only increased the rate of decline. We conclude that historical data on sperm density, despite large random error, are surprisingly reliable. Nonetheless, understanding causes of temporal and geographic differences in sperm density must await contemporary data.

What then can we conclude from these analyses? Do they suggest an average decline in sperm density between 1938-1990? The above discussion supports this conclusion. Does this imply that uniform decline in sperm density has occurred worldwide? The analyses of these studies by several authors and more recent data argue against this conclusion ....Therefore we believe that the trend summarized by Carlsen et al. reflects a significant decline in the USA (between 1938 and 1990) and northern Europe (at least post-1970), but the scarcity of data elsewhere prohibits drawing any conclusion about the rest of the world.

It must be remembered that none of these analyses have attempted to identify the causes of the trends in semen quality, although the identification of such causes is of considerable interest.

Although we cannot hope to obtain convincing evidence of exposures that might have produced the temporal trends described here, we have an indirect means of addressing this question. If indeed, environmental factors influence semen quality, these factors, unless uniformly distributed geographically, would be expected to produce not only temporal variation in sperm density, but geographic variation as well. A carefully controlled, cross-sectional study of semen quality conducted in several cities, with differing types and levels of environmental exposures, would be invaluable for assessing such geographic variation and its causes. Suppose such a study identified significant differences in sperm density between geographic areas that cannot be explained by host factors (such as age and ethnicity) and personal behaviors (such as drinking and smoking)? It might then be possible, using biomarkers of environmental exposures, for example, to point to environmental factors that have contributed to these differences. One class of chemicals that will be particularly relevant to examine are the "endocrine disrupters," those chemicals that act to alter hormone activity, particularly in offspring, when administered exposure occurs during the relevant developmental period. Several of these chemicals (methoxychlor, bisphenol A, and dioxin) are plausible candidates because very low doses prenatally has been shown to depress sperm counts in laboratory animals. A unique global study is now underway (The International Study of Semen Quality in Partners of Pregnant Women)..."

Pajarinen et al. compare the quality of sperm production of Finnish men in 1991 vs. 1981 by conducting post-mortems of men who had died suddenly from factors unrelated to reproductive health. This sampling allowed them to circumvent the biases that plague most studies dependent upon sperm donors. The Finnish team found a drop in the percentage of men with normal, healthy sperm production from 56.4% in 1981 to 26.9% in 1991. This change was accompanied by a decrease in the average weight of the men's testes, a decrease in the size of seminiferous tubules, and an increase in the proportion of fibrous tissue. These changes over time could not be explained by changes in body mass index, smoking, alcohol drinking or exposure to drugs. "Deteriorating spermatogenesis may thus be one important factor in the explanation of declining sperm counts observed worldwide."

Each of these studies was based upon men volunteering sperm before vasectomy. This introduces biases into the samples, as men volunteering for vasectomy are known to have sperm counts higher than the population average. The New York analysis, moreover, is built on small number of samples per year. Further, it is not stated in the methodology whether or not donors are asked to return for subsequent donations if their first donations are determined to have low counts. This procedure, while appropriate for the medical goals of a sperm donation or storage clinic, would invalidate the use of these data in trend analysis.

Fisch and Golubuff's reanalysis has also been questioned (e.g., in a paper delivered by N. Skakkebaek at the 1996 Annual Meeting of the Society of Endocrinology). The New York data used by in this analysis involve a small number of samples taken over a long time span, with the data entered in the analysis as if they had been accumulated in a single year at the end of the study. This invalidates the analysis.

In the meantime, it is clear that sperm count has dropped significantly in some areas (for example, see Irvine et al., Auger et al., Toppari et al., Pajarinan et al.) whereas it appears not to have changed in other areas (e.g., Fisch et al., Paulsen et al.). This geographic variation may provide epidemiological clues as to what is causing sperm count declines in some areas and not in others.

Paulsen et al. note that this finding differs from that reported in the meta-analysis of Carlsen et al overall, but that the Seattle data examine only the latter part of the period studied by Carlsen et al. When Paulsen et al. reexamine Carlsen et al.'s data only for the time span studied in Seattle (1972-1993), there is no significant change. Further analysis leads Paulsen et al. to observe: "This suggests that there may have been a true decrease in sperm concentration earlier in the century that did not continue. Alternatively, this could be a 'stairstep' effect, due to some changes that occurred around mid-century."

This study is also notable in the sperm trend literature because of the lengths to which Irvine et al. went to avoid sampling biases. The Irvine team recruited the men broadly through several different methods and did not do any sort of screening that would select only for men of proven fertility or exclude those in particular occupations.

"Our findings support previous reports that the quality of human semen seems to be falling. In particular, we have observed a decline in sperm concentration and the total number of sperm and of motile sperm in the ejaculate in association with a later year of birth, such that men born in the 1970s are producing some 24% fewer motile sperm in their ejaculate than are men born in the 1950s."

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