Declining sex ratio in a first nation community.
Members of the Aamjiwnaang First Nation The Aamjiwnaang First Nation (also referred to in government sources as Sarnia Indian Reserve 45 or Chippewas of Sarnia First Nation) is a First Nations community of about 850 Chippewa (Ojibwe) Aboriginal peoples, located in a reserve on the shores of the St. community near Sarnia, Ontario Sarnia is a city in Southwestern Ontario, Canada (city population 71,419, census area population 88,793, in 2006). It is the largest city on Lake Huron and is located where the three upper Great Lakes empty into the St. Clair River. , Canada, voiced concerns that there appeared to be fewer male children in their community in recent years. In response to these concerns, we assessed the sex ratio (proportion of male births) of the Aamjiwnaang First Nation over the period 1984-2003 as part of a community-based participatory research Community-based participatory research (CBPR) is research that is conducted as an equal partnership between traditionally trained "experts" and members of a community. In CBPR projects, the community participates fully in all aspects of the research process. project. The trend in the proportion of male live births of the Aamjiwnaang First Nation has been declining continuously from the early 1990s to 2003, from an apparently stable sex ratio prior to this time. The proportion of male births (m) showed a statistically significant decline over the most recent 10-year period (1994-2003) (m = 0.412, p = 0.008) with the most pronounced decrease observed during the most recent 5 years (1999-2003) (m = 0.348, p = 0.006). Numerous factors have been associated with a decrease in the proportion of male births in a population, including a number of environmental and occupational chemical exposures. This community is located within the Great Lakes Great Lakes, group of five freshwater lakes, central North America, creating a natural border between the United States and Canada and forming the largest body of freshwater in the world, with a combined surface area of c.95,000 sq mi (246,050 sq km). St. Clair River The St. Clair River is a river in central North America which drains Lake Huron into Lake St Clair, forming part of the International Boundary between the Canadian province of Ontario and the U.S. state of Michigan. Area of Concern and is situated immediately adjacent to several large petrochemical, polymer, and chemical industrial plants. Although there are several potential factors that could be contributing to the observed decrease in sex ratio of the Aamjiwnaang First Nation, the close proximity of this community to a large aggregation of industries and potential exposures to compounds that may influence sex ratios warrants further assessment into the types of chemical exposures for this population. A community health survey is currently under way to gather more information about the health of the Aamjiwnaang community and to provide additional information about the factors that could be contributing to the observed decrease in the proportion of male births in recent years. Key words: community-based, endocrine disruption, environmental exposure, First Nation, sex ratio. Environ Health Perspect 113:1295-1298 (2005). doi:10.1289/ehp.8479 available via http://dx.doi.org/[Online 17 August 2005]
There is increasing evidence that the human live birth sex ratio can be altered by a number of environmental and occupational chemical exposures. For example, lower proportions of male offspring have been observed in populations exposed to dioxin dioxin
Aromatic compound, any of a group of contaminants produced in making herbicides (e.g., Agent Orange), disinfectants, and other agents. Their basic chemical structure consists of two benzene rings connected by a pair of oxygen atoms; when substituents on the rings are (Mocarelli et al. 2000), mercury (Sakamoto et al. 2001), pesticides (Garry et al. 2003; Goldsmith 1997; Jatrell et al. 2002), polychlorinated biphenyls polychlorinated biphenyls, (pol´ēklôr´nā´tid bīfē´n (PCBs) (del Rio Del Rio (rē`ō), city (1990 pop. 30,705), seat of Val Verde co., W Tex., on the Rio Grande opposite Ciudad Acuña, Mexico; founded 1868, inc. 1911. Gomez et al. 2002; Weisskopf et al. 2003), and parental smoking (Fukuda et al. 2002). it has been hypothesized that some of these environmental and occupational chemicals may act as endocrine-disrupting compounds (EDCs), influencing the sex ratio by changing the hormonal milieu of the parents (James 1996), or by inducing sex-specific mortality in utero in utero (in u´ter-o) [L.] within the uterus.
In the uterus.
in utero adv. (Sakamoto et al. 2001).
The birth sex ratio (male:female) of a population is often reported as the male proportion (m = number of male births divided by the total of all births). Worldwide, the human live birth sex ratio is remarkably constant, ranging between 102 and 108 male to 100 female live births (m = 0.504-0.519) (Bartleby.com 2003). In Canada, the sex ratio is generally reported to be 105:100 (M:F) (m = 0.512) (Allan et al. 1997). Although the sex of the human embryo is genetically controlled and determined at the time of conception, there is evidence that the sex ratio can be partially influenced by both endogenous endogenous /en·dog·e·nous/ (en-doj´e-nus) produced within or caused by factors within the organism.
1. Originating or produced within an organism, tissue, or cell. and exogenous Exogenous
Describes facts outside the control of the firm. Converse of endogenous. factors. Endogenous parental hormone concentrations of gonadotropins and/or testosterone testosterone (tĕstŏs`tərōn), principal androgen, or male sex hormone. One of the group of compounds known as anabolic steroids, testosterone is secreted by the testes (see testis) but is also synthesized in small quantities in the at the time of conception are suspected to play a role in determining the sex of offspring (James 2004). Exogenous factors such as stress, parental disease, and exposure to certain chemicals appear to have some influence on the live birth sex ratio and may act by altering the parental hormone status (James 2004).
Sex ratios have been suggested as a noninvasive monitor of the reproductive health Within the framework of WHO's definition of health as a state of complete physical, mental and social well-being, and not merely the absence of disease or infirmity, reproductive health, or sexual health/hygiene of a population (Davis et al. 1998; James 1997a). Changes in the sex ratio have been used to assess the reproduction of populations with demonstrated exposures to EDCs (Mocarelli et al. 2000), as well as in communities near hazardous chemical sites (Williams et al. 1995). Altered live birth sex ratios may also be a useful indicator of public health, in that they reflect death at earlier stages of development than traditional indicators such as perinatal perinatal /peri·na·tal/ (-na´t'l) relating to the period shortly before and after birth; from the twentieth to twenty-ninth week of gestation to one to four weeks after birth.
adj. and infant mortality (hardware) infant mortality - It is common lore among hackers (and in the electronics industry at large) that the chances of sudden hardware failure drop off exponentially with a machine's time since first use (that is, until the relatively distant time at which enough mechanical (Williams et al. 1995).
Materials and Methods
We assessed the live birth sex ratios for the Aamjiwnaang First Nation community in Ontario, Canada, in response to concerns voiced by members of the community regarding the perception of fewer male children in recent years. This birth sex ratio assessment was part of a broader community-based investigation undertaken by the Aamjiwnaang in collaboration with the Occupational Health Clinics for Ontario Workers (OHCOW OHCOW Occupational Health Clinics for Ontario Workers ) along with scientific consultants, professionals, and students from a wide range of disciplines. The exploration included such quantitative measurements as soil, sediment, wildlife, fish, and air sampling, along with a door-to-door health survey and interviews. In keeping with the principles of community-based participatory research (Hall 1979, 2003; Hagey 1997; Hills and Mullett 2000; Keith and Brophy 2004), the community itself has been involved in all major decision-making about the direction of the research and has participated in much of the data collection.
Aamjiwnaang First Nation. The Chippewas of Aamjiwnaang have approximately 850 band members residing on the Aamjiwnaang reserve land (Information Management Branch Department of Indian Affairs and Northern Development 2001). This reserve is located within the area identified as the St. Clair River Area of Concern by the Canada-U.S. Great Lakes International Joint Commission (Environment Canada Environment Canada (EC), legally incorporated as the Department of the Environment under the Department of the Environment Act ( R.S., 1985, c. E-10 ), is the department of the Government of Canada with responsibility for coordinating environmental policies and 2005) and is situated immediately adjacent to the Sarnia-Lambton Chemical Valley--one of Canada's largest concentrations of industry. The reserve is surrounded by several large petrochemical, polymer, and chemical industrial plants. The community provided informed consent and assistance to collect live birth sex ratio data from the Department of Indian and Northern Affairs database (Indian and Northern Affairs Canada The Department of Indian Affairs and Northern Development (FIP: Indian and Northern Affairs Canada, French: Affaires indiennes et du Nord Canada, DIAND , Ottawa, Ontario, Canada) for the period 1984-2003 (representing the full length of record). Births and deaths of members of the Aamjiwnaang First Nation are reported on a monthly basis to the Department of Indian and Northern Affairs by the Aamjiwnaang Lands and Memberships clerk.
Statistical analysis. We calculated the proportion of male births for the Aamjiwnaang community by dividing the number of male live births by the total of all live births for each year 1984-2003. We used linear regression Linear regression
A statistical technique for fitting a straight line to a set of data points. to examine the trend in the proportion of male births over time. Based on the data, we produced two lineal That which comes in a line, particularly a direct line, as from parent to child or grandparent to grandchild.
LINEAL. That which comes in a line. Lineal consanguinity is that which subsists between persons, one of whom is descended in a direct line from the other. : regression lines to estimate a point in time where slopes of the regression lines deviate and the trend in the proportion of male births begins to decline. We then calculated the proportion of live male births for both 5- and 10-year intervals over the duration of the study period and compared these data to the expected proportion of males for Canada (m = 0.512), as well as a "control" First Nation community (m = 0.520) using Pearson's chi-square analysis. The "control" community sex ratio was calculated from comparable data for a genetically similar, yet geographically distinct, Chippewa First Nation band that has requested to remain anonymous. Because the male proportion in the "control" community (m = 0.520) was not statistically different from the expected Canadian male proportion ([chi square chi square (kī),
n a nonparametric statistic used with discrete data in the form of frequency count (nominal data) or percentages or proportions that can be reduced to frequencies. ] = 0.098, df = 1, p = 0.754), all analyses shown were performed using the Canadian male proportion (m = 0.512) as the expected value Expected value
The weighted average of a probability distribution. Also known as the mean value. .
Altered sex ratios. Examination of the proportion of male births for the Aamjiwnaang community over the study period 1984-2003 (Figure 1) shows that the proportion of male births appears to be relatively stable for the period 1984-1992; linear regression ([r.sup.2] = 0.000) shows a slope not significantly different from zero (p = 0.990). A second linear regression for the period 1993-2003 ([r.sup.2] = 0.547) shows a declining trend in the proportion of male births with a statistically significant deviation of slope from zero (p - 0.009).
When the sex ratio data were categorized cat·e·go·rize
tr.v. cat·e·go·rized, cat·e·go·riz·ing, cat·e·go·riz·es
To put into a category or categories; classify.
cat into 5- and 10-year periods, we found a highly significant decrease in the proportion of male live births (m = 0.348, [chi square] = 7.472, df = 1, p = 0.006) for the Aamjiwnaang community during the most recent 5-year interval (1999-2003) compared with the expected sex ratio (Table 1). We also observed a statistically significant decrease in the proportion of male births when the data were categorized into 10-year intervals over the period 1994-2003 (m = 0.412, [chi square] = 7.100, df = 1, p = 0.008) (Table 1).
Evidence of chemical exposures influencing sex ratios. Normal variation in sex ratio can be expected in any population, especially with a small sample size; however, the extent of the sex ratio deviation for Aamjiwnaang appears to be outside the range of normal. Following relatively stable sex ratios from 1984-1992, there was a significant decline in the proportion of male live births for the period 1993-2003 (Figure 1). The continuing reduction in the proportion of male births is most apparent in the most recent 5-year period (1999-2003, m = 0.348; Table 1), indicating that there may be an ongoing process manifesting as a reduction in sex ratio starting in the early to mid-1990s. Previous studies have demonstrated that populations exposed to environmental contaminants such as endocrine disruptors, either through their close proximity to industrial plants or through other sources such as food, can have significant changes in the reproductive ability of the community, including the sex ratio. Table 2 summarizes some findings on the influence of environmental and occupational exposures on sex ratios.
There has been speculation that declining trends in the proportion of male births during the later part of the 20th century in industrialized in·dus·tri·al·ize
v. in·dus·tri·al·ized, in·dus·tri·al·iz·ing, in·dus·tri·al·iz·es
1. To develop industry in (a country or society, for example).
2. countries including Canada, the United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. (Allan et al. 1997), Sweden, Germany, Finland, Denmark, and the Netherlands (Davis et al. 1998) could be attributed to environmental contaminants and endocrine disruption. Conversely, other studies have shown increases in sex ratio (Lancaster and Day 1998), or no change (Grech et al. 2003), and it is unlikely that a single mechanism can account for the changes observed in any one country, given the scale of these studies (James 1998). However, changes in sex ratios of small populations can be used more reliably as a sentinel indicator of altered reproduction, especially when there is a documented exposure to environmental or occupational chemicals (James 1998).
There are several possible routes of exposure to chemicals that may affect the reproductive ability of a community. Populations can be exposed to contaminants through industrial accidents such as in Seveso, Italy, where young men exposed to high concentrations of dioxins sired significantly more female children than male (Mocarelli et al. 2000). Several studies have examined the sex ratios of communities exposed to different types of air pollution with conflicting results: a decrease in sex ratio was observed for residential areas exposed to air pollution from local incinerators (Williams et al. 1992); an increase in sex ratios was observed in areas close to a steel foundry (Lloyd et al. 1984, 1985), communities close to natural gas (Saadat et al. 2002) and petrochemical industry (Yang et al. 2000b); and no effect on sex ratio was observed for general air pollution (Williams et al. 1995) and in another (less powerful) study of municipalities close to a petroleum refinery plant (Yang et al. 2000a). Other routes of exposure to contaminants such as PCBs include food sources. Decreased sex ratios have been associated with maternal consumption of Great Lakes fish (Weisskopf et al. 2003) and fish contaminated contaminated,
v 1. made radioactive by the addition of small quantities of radioactive material.
2. made contaminated by adding infective or radiographic materials.
3. an infective surface or object. with methylmercury (Sakamoto et al. 2001). To make matters more complicated, paternal Great Lakes fish consumption appears to increase the offspring sex ratio (Karmaus et al. 2002).
Although there is mounting evidence that environmental and occupational exposures to contaminants can affect sex ratios, the results to date can be difficult to interpret because of conflicting results and the number of variables that appear to be involved. The effect of a chemical exposure on a population's sex ratio appears to depend on a number of factors, including parental age at the time of exposure, total exposure level, and whether it is a maternal or paternal exposure (Table 2). For example, similar exposures in men and women may have different effects on the sex of offspring, as observed with PCBs (Table 2).
Based on an assessment algorithm used by Jarrell (2002), there is reasonably strong evidence linking reduced sex ratios and environmental exposures of dioxin, dibromochloropropane, and hexachlorobenzene (HCB HCB
hexachlorobenzene. ). Although the mechanism of action of these compounds on sex ratio is not entirely clear, both dioxin and HCB bind to the aryl hydrocarbon receptor The Aryl hydrocarbon receptor (AhR) is member of the family of basic-helix-loop-helix transcription factors. AhR is a cytosolic transcription factor that is normally inactive, bound to several co-chaperones. and may alter sex ratios by changing the hormonal status of the parents. HCB is also associated with pregnancy loss in women (Jarrell et al. 1998). Similarly, other compounds such as methylmercury appear to increase the number of spontaneous abortions spon·ta·ne·ous abortion
A naturally occurring termination of a pregnancy. Also called miscarriage.
spontaneous abortion and stillbirths in exposed populations, ultimately altering the sex ratio of the surviving offspring (Sakamoto et al. 2001). The overall effects of other compounds such as PCBs on sex ratios will continue to be clarified with further research.
A 1996 assessment of soil and sediment contaminants on Aamjiwnaang reserve land has identified high concentrations [many exceeding sediment guidelines of the Ontario Ministry of the Environment and Energy (2004)] of several contaminants including PCBs, HCB, mirex mirex
an effective organic pesticide used in ant control and as a fire retardant; it is, however, very persistent in tissue and now banned because of residue problems. , polycyclic aromatic hydrocarbons polycyclic aromatic hydrocarbon
Any of a class of carcinogenic organic molecules that consist of three or more rings containing carbon and hydrogen and that are commonly produced by fossil fuel combustion. (PAHs), and metals (copper, nickel, lead, mercury, arsenic, chromium chromium (krō`mēəm) [Gr.,=color], metallic chemical element; symbol Cr; at. no. 24; at. wt. 51.996; m.p. about 1,857°C;; b.p. 2,672°C;; sp. gr. about 7.2 at 20°C;; valence +2, +3, +6. , manganese manganese (măng`gənēs, măn`–) [Lat.,=magnet], metallic chemical element; symbol Mn; at. no. 25; at. wt. 54.938; m.p. about 1,244°C;; b.p. about 1,962°C;; sp. gr. 7.2 to 7. , iron) (Leadley and Haffner 1996). Pollutants pollutants
see environmental pollution. released by the petrochemical industry surrounding the Aamjiwnaang reserve, as reported by the National Pollutant pol·lut·ant
Something that pollutes, especially a waste material that contaminates air, soil, or water. Release Inventory (Environment Canada 2002), are too numerous to name in entirety but include volatile organic compounds volatile organic compound Environment Any toxic cabon-based (organic) substance that easily become vapors or gases–eg, solvents–paint thinners, lacquer thinner, degreasers, dry cleaning fluids , ethylene, phthalates Phthalates, or phthalate esters, are a group of chemical compounds that are mainly used as plasticizers (substances added to plastics to increase their flexibility). They are chiefly used to turn polyvinyl chloride from a hard plastic into a flexible plastic. , dioxins and furans, HCB, vinyl chloride vinyl chloride
Colourless, flammable, toxic gas (H2C=CHCl), belonging to the family of organic compounds of halogens. It is produced in very large quantities and used principally to make PVC, as well as in other syntheses and in , PAHs, ammonia, acrylonitrile acrylonitrile /ac·ry·lo·ni·trile/ (ak?ri-lo-ni´tril) a colorless halogenated hydrocarbon used in the making of plastics and as a pesticide; its vapors are irritant to the respiratory tract and eyes, may cause systemic poisoning, and are , and metals (nickel, mercury, lead, cadmium cadmium (kăd`mēəm) [from cadmia, Lat. for calamine, with which cadmium is found associated], metallic chemical element; symbol Cd; at. no. 48; at. wt. 112.41; m.p. 321°C;; b.p. 765°C;; sp. gr. 8. , zinc, manganese). Because of the close proximity of this community to the large aggregation of petrochemical industry and potential exposures to compounds with known effects on sex ratios, further investigations into the types and routes of chemical exposures (air, water, food, soil, and sediment) are warranted for this population.
Evidence of altered wildlife reproduction in the area. A large body of literature has accumulated detailing the adverse effects of EDCs on the reproductive ability and sexual development of fish, amphibians amphibians
members of the animal class Amphibia. Includes frogs, toads, newts, salamanders and cecilians all capable of living on land or in water. , reptiles reptiles
terrestrial or aquatic vertebrates which breathe air through lungs and have a skin covering of horny scales. They are poikilothermic, oviparous or ovoviviparous, and, if they have legs they are short and constructed solely for crawling. , and birds. Numerous studies indicate that wildlife populations in the Great Lakes area are being adversely affected by the level of contamination, and that evidence from wildlife research could be used as a sentinel for human health effects (Fox 2001). In the Great Lakes area close to the Aamjiwnaang reserve, fish with intersex intersex /in·ter·sex/ (in´ter-seks)
female intersex a female pseudohermaphrodite. gonads (both male and female) have been reported in Lake St. Clair (Kavanagh et al. 2004). There is also ongoing research in the St. Clair River Area of Concern region of the Great Lakes that is documenting reduced hatching success and altered sexual development in turtles as well as changes in the sex ratios of birds (Environment Canada Canadian Wildlife Service The Canadian Wildlife Service or CWS (French: Service canadien de la faune, SCF) is an agency of the Government of Canada, administered by the Department of the Environment, also known as Environment Canada. 2003).
Other population factors influencing sex ratio. Numerous biological and environmental factors appear to have a minor influence on sex ratios, including parental age, parity, birth order, coital co·i·tus
Sexual union between a male and a female involving insertion of the penis into the vagina.
[Latin, from past participle of co rates, infertility, maternal nutrition (James 1996, 2004), illness such as insulin-dependent diabetes mellitus insulin-dependent diabetes mellitus
Abbr. IDDM See diabetes mellitus. (Rjasanowski et al. 1998), stress, war (Ansari-Lari and Saadat 2002), and selective reproductive practices (Allahbadia 2002). These influences on sex ratio are generally considered to play a small role, but cannot be ruled out completely without additional information about the study population.
One study has looked at the influence of race on sex ratios with North American North American
named after North America.
North American blastomycosis
see North American blastomycosis.
North American cattle tick
see boophilusannulatus. Indian couples having slightly higher sex ratios (more boys) than Caucasian couples (Khoury et al. 1984). Comparison of the "control" Chippewa First Nation community to the average sex ratio for Canada showed no significant difference between the two populations, indicating that race is likely not playing a role in the observed altered sex ratio of the Aamjiwnaang community.
Future studies. The Department of Indian and Northern Affairs database is the most accurate source of information for First Nations vital statistics in Canada. However, there are some limitations to this database because it potentially includes births of band members that are not residing on reserve land and does not provide additional information about, for example, parental age, parity, or stillbirths. A community health survey is under way to explore a broad range of health concerns among the residents of the Aamjiwnaang reserve, as well as to gather information on covariates that may influence live birth sex ratio, including parental age, length of residency in the community, sex of stillbirths, and lifestyle factors such as parental smoking.
The initial assessment of the sex ratios of the Aamjiwnaang community over the 20-year period 1984-2003 presented here indicates that there is a significant ongoing decrease in the proportion of male live births beginning in the early 1990s and continuing to the end of the study period 2003. Although several potential factors may be contributing to the observed decrease in sex ratio, the close proximity of this community to the large aggregation of petrochemical industry and potential exposures to compounds that may influence sex ratios warrants further assessment into the types of chemical exposures for this population. Because of the complexities of any population exposure, causality causality, in philosophy, the relationship between cause and effect. A distinction is often made between a cause that produces something new (e.g., a moth from a caterpillar) and one that produces a change in an existing substance (e.g. between a single compound and adverse effect is always difficult to assess. It is possible that the Aamjiwnaang community has had multiple chemical exposures over the years that may be contributing to the overall picture of a reduced sex ratio. Further assessment must include the identification of exposures to compounds that may already be associated with adverse effects on sex ratio, determination that the timing of exposure is appropriate for the observed change in sex ratio, and elimination of other potential influences on sex ratio.
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tr.v. pol·lut·ed, pol·lut·ing, pol·lutes
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pertaining to or arising from a gonad. See also testicular, ovarian.
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Constanze A. Mackenzie, (1) Ada Lockridge, (2) and Margaret Keith (3)
(1) Faculty of Medicine, University of Ottawa
Address correspondence to C.A.Mackenzie, c/o 171 Kendall St., Point Edward, ON, Canada, N7V 4G6. Telephone: (519) 337-4627. Fax: (519) 337-9442. E-mail: firstname.lastname@example.org
We thank the Aamjiwnaang Environmental Committee for their interest and assistance. We also thank T. Colborn, M. Gilbertson, and N. Birken for comments and encouragement, and W. Teel and J. Brophy for facilitating this study.
C.M. received funding from the McConnell Foundation, Ecosystem Health Program, Faculty of Medicine, University of Western Ontario Western is one of Canada's leading universities, ranked #1 in the Globe and Mail University Report Card 2005 for overall quality of education. It ranked #3 among medical-doctoral level universities according to Maclean's Magazine 2005 University Rankings. .
The authors declare they have no competing financial interests.
Received 7 July 2005; accepted 16 August 2005.
Table 1. Total live births, proportion of live male births (male live births/total live births), [chi square], and p-value for Aamjiwnaang First Nation 1984-2003 arranged in 5- and 10-year periods. Total Proportion live male [chi Period births births square] (a) p-Value 5-Year 1984-1988 173 0.538 0.185 0.667 1989-1993 185 0.551 0.532 0.466 1994-1998 215 0.451 1.574 0.210 1999-2003 132 0.348 7.472 0.006 * 10-Year 1984-1993 358 0.545 0.807 0.369 1994-2003 347 0.412 7.100 0.008 * (a) Chi-square was performed using an expected male proportion equal to 0.512; df = 1. * Highly significant statistical deviation (p < 0.01) from the expected proportion of males using Chi-square analysis. Table 2. The influence of environmental and occupational exposures on sex ratio. Decreased sex ratio Increased sex ratio Exposure type (fewer boys) (fewer girls) Dioxin Paternal environmental exposure postindustrial accident (Mocarelli et al. 1996, 2000) Paternal exposure as pesticide producers (Ryan et al. 2002) PCBs Paternal consumption of Paternal exposure rice oil contaminated to PCBs in Great with PCBs at < 20 years Lakes fish eaters of age (del Rio Gomez (Karmaus et al. et al. 2002) 2002) Maternal exposure to PCBs in Great Lakes fish (Weisskopf et al. 2003) Pesticides Paternal exposure to nematocide DBCP (Goldsmith 1997) Pesticide applicators (Garry et al. 2003) HCB exposure (Jarrell et al. 2002) Methylmercury Maternal exposure to methylmercury- contaminated fish (Sakamoto et al. 2001) Petroleum Municipalities exposed to petrochemical air pollution (Yang et al. 2000b) Natural gas exposure (Saadat et al. 2002) Air pollution Air pollution from Air pollution from incinerators (Williams local steel foundry et al. 1992) (Lloyd et al. 1984, 1985) Radiation Maternal exposure to Paternal occupational non-ionizing radiation exposure to ionizing (electromagnetic radiation (Dickinson radiation, strong static) et al. 1996) and paternal exposure to high voltage (James 1997b) Occupation Paternal exposure carbon type setters (Milham 1993) Infertility Maternal exposure to treatment clomiphene citrate (Jarrell 2002) Lifestyle Parental smoking (Fukuda et al. 2002) Exposure type No effect Dioxin Paternal occupational exposure (Schnorr et al. 2001) PCBs Consumption of rice oil contaminated with PCBs and PCDFs (Yoshimura et al. 2001) Pesticides Maternal exposure to HCB (Jarrell et al. 1998) Methylmercury Petroleum Municipalities adjacent to a petroleum refinery plant (Yang et al. 2000a) Air pollution General air pollution (Williams et al. 1995) Radiation Background ionizing radiation (Saadat 2003) Occupation Infertility treatment Lifestyle Abbreviations: DBCP, dibromochloropropane; PCDFs, polychlorinated dibenzofurans.