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Sport-Caught Fish Consumption and Conception Delay in Licensed Michigan Anglers
Environmental Research Section A 80, S183—S188 (1999) Article ID enrs.1998.3909, available online at http://www.idealibrary.com on
Sport-Caught Fish Consumption and Conception Delay in Licensed Michigan Anglers1 Jeanne M. Courval,* 2 Jane V. DeHoog,* Aryeh D. Stein,* Eugene M. Tay,* Jianping He,* Harold E. B. Humphrey,- and Nigel Paneth* *Department of Epidemiology, College of Human Medicine, Michigan State University, East Lansing, Michigan 48824-1316; and -Bureau of Epidemiology, Michigan Department of Community Health, Lansing, Michigan, 48809 Received January 9, 1998
woman’s partner included in the model, the OR were 0.8, 0.8, and 1.0, respectively. These data suggest a modest association, in men only, of sportcaught fish consumption with risk of conception delay. 1999 Academic Press Key Words: fish consumption; conception delay; Great Lakes.
Between 1993 and 1995, we surveyed 4931 licensed anglers aged 17–34 years residing in 10 Michigan counties bordering a Great Lake. Responses were received from 1443 anglers and 844 of their partners. Lifetime sport-caught fish consumption was estimated as the number of sport-caught fish meals consumed in the previous 12 months times years since 1970 in which sport-caught fish were consumed. Analysis was restricted to currently married couples (n ⴝ 626). Lifetime sport-caught fish consumption was categorized in men as 0 (14%); 1–114 (27%); 115–270 (30%); 271–1127 (29%) meals; and in women as 0 (28%); 1–54 (26%); 55–138 (27%); fand 139–1127 (19%) meals, respectively. Conception delay (ever having failed to conceive after 12 months of trying) was reported by 13% of both men and women. Among men, the unadjusted odds ratios (OR) for conception delay were 1.2, 1.3, and 2.0 across the three increasing levels of sport-caught fish consumption compared to none (trend test P ⴝ 0.06). After adjustment for age, race, region of Michigan, household income, educational attainment, smoking, alcohol consumption, and partner’s sport fish consumption, the OR for conception delay in men were 1.4, 1.8, and 2.8, respectively. In women, unadjusted OR for conception delay were 0.9, 1.0, and 1.4 with increasing sport-caught fish consumption (trend test P ⴝ 0.35). With the same covariates and the sport-caught fish consumption of the
INTRODUCTION
Polychlorinated biphenyls (PCBs) and organic pesticides, such as DDT and DDE, are widespread industrial contaminants in the Great Lakes basin. Although production and discharge of these compounds ceased in the 1970s, they persist in the environment and bioaccumulate in the food chain. Several studies in animals have suggested that elevated PCB levels may cause reproductive problems, including reproductive failure and effects on sexual development (Auerlich and Ringer, 1977; Allen et al., 1979; Gray et al., 1993; Krishnan and Safe, 1993). It has been hypothesized that these reproductive problems may be related to the tendency of this class of compounds to disrupt normal endocrine development. Few large human populations are chronically exposed to detectable levels of PCB. One group of people potentially at higher risk of PCB exposure is recreational anglers who consume their catch (Humphrey 1988). We are currently recruiting a population for a cohort study in which we will investigate associations between sport-caught fish consumption and human reproductive health. The analysis described here is based upon data from the baseline screening survey used to identify potential participants for the cohort study (Courval et al., 1996).
1 The Fisheaters Family Health Project is funded by the Great Lakes Human Health Effects Program, Agency for Toxic Substances and Disease Registry. Eugene Tay was recipient of a Science to Achieve Results (STAR) Graduate Fellowship from the Environmental Protection Agency. This study was approved by the Michigan State University Committee on Research Involving Human Subjects and was conducted according to the approved protocol. 2 To whom reprint requests should be addressed at Department of Epidemiology, Rollins School of Public Health, 1518 Clifton Road, NE, Atlanta, Georgia 30322.
S183 0013-9351/99 $30.00 Copyright 1999 by Academic Press All rights of reproduction in any form reserved.
S184
COURVAL ET AL.
MATERIALS AND METHODS
Screening Survey The methods and results of the screening survey have been previously described (Courval et al., 1996). Between 1993 and 1995, we surveyed a population of reproductive-aged (17—34 years old) Michigan anglers who lived in one of 10 Michigan counties bordering a Great Lake (Fig. 1). These anglers were identified from computerized fishing license information or from copies of fishing licenses, both of which were provided to us by the Michigan Department of Natural Resources. Licensed anglers were sent two questionnaires, one to be completed by the angler and one to be completed by their spouse or partner. The questionnaire solicited information concerning fishing habits and fish consumption, pregnancy and reproductive history, and selected demographic characteristics. Repeat mailings and a variety of small incentives were used to increase participation. We mailed surveys to 4931 households. The Post Office returned 505 surveys as undeliverable, and an additional 44 were returned uncompleted. A total of 1443 questionnaires were completed by licensed anglers, for a crude response rate of 29%. An additional 844 questionnaires were completed by other household members, usually
a partner, but occasionally a parent or an unrelated individual. In total, 2287 questionnaires were received. Population We defined a couple for this analysis as a male and a female returning their questionnaires together; 803 such couples were identified. Since we did not expect substantial numbers of unmarried people in this age range to have previously attempted to achieve pregnancy, we restricted the analysis to currently married couples. The sample for the present analysis thus consists of 626 married couples. Outcome of Interest We defined conception delay as a positive response to the question ‘‘Was there ever a period of 12 months or more during which you tried to conceive a child but were unable to?’’ Men were asked about attempts to father a child. Exposure Assessment We computed an index of lifetime fish consumption by multiplying the reported number of fish meals consumed in the previous 12 months by the number of years since 1970 in which any sportcaught fish was consumed. This method assumes that fish consumption patterns are relatively consistent across years that any fish is consumed. This index was then divided into four sex-specific consumption categories, with the lowest group including all those reporting no sport fish consumption. Statistical Methods
FIG. 1. Target counties for the Fisheaters Family Health Project, Michigan.
Initial analyses examined the distributions of all variables. Subsequently, we used logistic regression to investigate the impact of the consumption of sport-caught Great Lakes fish on conception delay among couples who responded to our screening survey. Analyses were conducted using SPSS (SPSS, Inc., Chicago, IL). Initial descriptive analyses, and unadjusted and adjusted logistic regression analyses, were stratified by sex. Conception requires contributions from both members of a couple. We tried to separate the male and female effects of sport fish consumption on conception delay in the logistic regression models by examining whether the association between an individual’s sport-caught fish consumption and conception delay persisted once information on their
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SPORT FISH CONSUMPTION AND CONCEPTION DELAY
partner’s sport fish consumption was taken into account. RESULTS
TABLE 1 Demographic, Health Behavior, and Sport Fish Related Characteristics of 626 Currently Married Couples Responding to a Survey of Reproductive-Aged Michigan Anglers, 1993–1995
Characteristics of Our Population Over 80% of women and over 90% of men were aged 25 years or older. Overall, the men in our study were slightly older than the women; 60% of men were at least 31-years old compared to 41% of the women. The overwhelming majority (greater than 94%) of respondents were Caucasian. A few identified themselves as Black, Hispanic, or Native American. About 40% of respondents had no postsecondary education. About 38% of men, and 15% of women, reported drinking alcohol at least weekly. In addition, 40% of men, and almost half of the women, reported never having smoked, while an additional 22% reported that they were former smokers. Men were more likely to have consumed any sport-caught fish than women and, among sport fish consumers, men ate more fish meals than women (Table 1). Approximately 80% of men had fathered a child, and a similar proportion of women had been pregnant (ever conceived). As would be expected, prevalence of prior conception increased with age (data not shown). About 13% of both men and women reported failing to conceive after 12 months of trying. Among women who reported a period of conception delay, over 75% also reported having at least one birth. We do not know whether the reported births followed episodes of reported delayed conception or occurred at a different period in life. Among women who had ever conceived, just over 10% had never had a live birth, and almost 25% had experienced one or more miscarriages. A small proportion had experienced a stillbirth or had had a child with a birth defect (Table 2). Logistic Regression Analyses We examined associations between selected demographic and behavioral characteristics, and prevalence of conception delay. Increased age, particularly among women, and non-Caucasian race were associated with increased prevalence of conception delay. A regional variation in conception delay was also noted. Current smoking was moderately associated with conception delay among women but not men, while former smoking was associated with conception delay in both sexes. Income, educational attainment, and alcohol intake were not associated with conception delay in either sex (Table 3).
Men
Women
Age (years)
425 years 26—30 years 31#years
% 7.6 32.2 60.2
% 15.6 43.0 41.4
Income
:$20,000/year $20,000—39,999/year 5$40,000/year
12.1 41.9 45.9
12.4 41.3 46.3
Region a
West Michigan Saginaw Bay SE Michigan Wayne county
34.5 27.7 13.8 24.0
34.5 27.5 13.8 24.0
Education
4High school Some college College graduate
43.8 34.7 21.4
38.7 39.7 21.6
Race/ethnicity
Caucasian Non-Caucasian
94.2 5.8
94.7 5.3
Alcohol use
None 41 drink/month 1—3 drinks/month 51 drink/week
7.8 33.7 19.5 38.2
12.2 54.6 17.3 15.1
Smoking
Never smoked Former smoker Current smoker
41.2 22.2 35.9
47.2 23.3 29.2
14.2 27.0 30.3 28.5
28.1 26.0 26.9 19.0
Lifetime consumption of sport-caught fish b None Low Medium High
a West Michigan—Muskegon, Ottawa, Allegan; Saginaw Bay— Bay, Midland, Saginaw; SE Michigan—St. Clair, Macomb, Monroe; Wayne County—Wayne County. b Men: low, 1—114 meals; medium, 115—270 meals; high, 271—1127 meals. Women: low, 1—54 meals; medium, 55—138 meals; high, 139—1127 meals.
In unadjusted logistic regression analyses, a modest association between high lifetime sport-caught fish consumption and conception delay was observed for women. A slightly stronger association was noted among men, with those in the highest consumption group having an odds ratio of 2.0 relative to those with no consumption (Table 4). For women, the test for trend was not significant (P"0.35). For men, the test for linear trend was of marginal significance, with a P value of 0.06. In women, the odds ratios were unaltered after adjustment for potential confounders, but in men, the associations were strengthened when several potential confounders,
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COURVAL ET AL.
TABLE 2
TABLE 3
Reproductive History of 626 Currently Married Couples Responding to a Survey of Reproductive-Aged Michigan Anglers, 1993–1995
Unadjusted Odds Ratios (95% Confidence Intervals) for the Associations between Conception Delay and Potential Confounders in 626 Currently Married Couples Responding to a Survey of Reproductive-Aged Michigan Anglers, 1993–1995
Men (%)
Women (%)
Ever conceived Yes No
77.9 22.1
82.7 17.3
Conception delay Yes No
12.9 87.1
13.3 86.7
— — — —
10.6 22.5 1.2 3.7
Men
Prior reproductive events (In females who have conceived) No live birth 51 miscarriage 51 stillbirth 51 child with birth defects
namely region of residence, age, race, education, income, smoking, and alcohol were included in the model. In women, the odds ratio for the highest sport fish consumption group was 1.4 relative to nonconsumers. In men, the comparable odds ratio was 2.4 (Table 4). We further tested whether the effect of one’s own sport-caught fish consumption persisted once knowledge of one’s partner’s consumption was taken into account. When the partner’s fish consumption was entered into the model for women, any association between her own sport-caught fish consumption and conception delay completely disappeared. However, when the partner’s fish consumption was entered into the model for men, the association between his sport-caught fish consumption and conception delay did not change (Table 4). DISCUSSION
Alternative explanations for our findings need to be considered. Our data are cross sectional, and we do not know whether the reported period of conception delay followed, coincided with, or preceded the critical period of fish consumption. Nor do we know whether the current partner, from whom we obtained fish consumption data, was indeed the partner during the period of attempted conception. We have controlled in our analysis for several potential confounders that we assessed in our survey. However, other unmeasured variables may possibly explain the association we describe. In our study, increased sport fish consumption is strongly associated with increased fishing activity in both males and females (P:0.001). If increased fishing
Women
OR (95% C.I.)
OR
(95% C.I.)
Age 425 years 26—30 years 31#years
(—) b 1.6 1.6
(0.5—4.5) (0.5—4.6)
(—) 3.0 2.1
(1.2—7.2) (0.8—5.1)
Race Caucasian Non-Caucasian
(—) 2.2
(1.0—5.0)
(—) 1.9
(0.8—4.6)
Income :$20,000/year $20,000—39,999/year 5$40,000/year
(—) 1.1 1.0
(0.5—2.4) (0.5—2.3)
(—) 0.9 1.0
(0.4—2.0) (0.5—2.1)
Regiona West Michigan Saginaw Bay SE Michigan Wayne County
(—) 0.5 1.1 1.2
(0.3—1.0) (0.5—2.2) (0.7—2.1)
(—) 0.6 0.9 1.1
(0.3—1.1) (0.5—1.9) (0.6—2.0)
Education 4High school Some college College graduate
(—) 0.9 0.8
(0.5—1.5) (0.4—1.5)
(—) 0.8 1.2
(0.5—1.4) (0.6—2.1)
Smoking Never smoked Former smoker Current smoker
(—) 1.5 1.0
(0.8—2.6) (0.6—1.7)
(—) 1.5 1.6
(0.8—2.6) (0.9—2.7)
Alcohol in past year None 41 drink/month 1—3 drinks/month 51 drink/week
(—) 1.4 1.1 1.3
(0.5—3.9) (0.4—3.3) (0.5—3.5)
(—) 0.9 1.0 1.0
(0.4—1.8) (0.5—2.4) (0.4—2.3)
a West Michigan—Muskegon, Ottawa, Allegan; Saginaw Bay— Bay, Midland, Saginaw; SE Michigan—St. Clair, Macomb, Monroe; Wayne County—Wayne County. b (—) denotes reference category.
activity is, in turn, associated with increased time away from the spouse, an alternative explanation for our findings could be that increased fishing activity results in reduced opportunity for conception to occur. We think this is unlikely to be the case because recreational anglers in the regions we surveyed are thought to do most of their fishing in lakes and streams near their residences, which would not require time away from home. In the screening survey we do not have information on whether couples were truly ‘‘at risk’’ for conception during their 12 months of trying, that is, we do not know whether there were
SPORT FISH CONSUMPTION AND CONCEPTION DELAY
TABLE 4 Associations between Conception Delay and Lifetime Sport Fish Consumption in 626 Currently Married Couples Responding to a Survey of Reproductive-Aged Michigan Anglers, 1993–1995 Men a
Lifetime sport-caught fish meals
Womenb
Unadjusted odds ratios None Low Medium High
OR (—) 1.2 1.3 2.0
(95% C.I.) OR (—) (0.5—2.9) 0.9 (0.6—3.1) 1.0 (0.9—4.5) 1.4
(95% C.I.)
Adjusted odds ratiosc None Low Medium High
(—) 1.3 1.5 2.4
(0.5—3.2) (0.6—3.5) (1.0—5.7)
(—) 0.9 1.0 1.4
(0.4—1.8) (0.5—2.0) (0.7—3.0)
Adjusted odds ratiosd None Low Medium High
(—) 1.4 1.8 2.8
(0.5—3.9) (0.6—5.0) (1.0—8.0)
(—) 0.8 0.8 1.0
(0.4—1.9) (0.4—1.8) (0.4—2.4)
(0.5—1.8) (0.5—1.9) (0.7—2.7)
a
Men: low, 1—114 meals; medium, 115—270 meals; high, 271—1127 meals. b Women: low, 1—54 meals; medium, 55—138 meals; high, 139—1127 meals. c Adjusted for region, age, race, education, income, smoking, alcohol. d Also adjusted for partner’s sport-caught fish consumption.
separations from the spouse, nor do we have any idea of the frequency and timing of intercourse during this time. In our prospective reproductive cohort study (Courval et al., 1999) we will be able to address these issues more fully. This analysis provides only indirect evidence that environmental contaminants are associated with human reproductive health outcomes. We did not attempt to measure serum environmental contaminant levels in the screening survey population, and therefore cannot directly relate PCB or other contaminant burden to risk of conception delay. From other data, it is known that serum PCB levels are elevated in consumers of Great Lakes sportcaught fish, increase with reported amount of sport fish consumed, and are higher in males (Humphrey 1988; Hovinga et al., 1993). As in all surveys, there is always the concern that respondents may differ from nonrespondents, and that any association may be an artifact. We have examined this possibility in a substudy in which 268 of our nonrespondents were contacted by telephone about 2 years after the initial mailings. We were not able to repeat our exact analysis in these nonresponders because we did not ask about the number of
S187
years since 1970 that a person had consumed sport fish in the nonresponder substudy. Instead, we examined the association between sport fish consumption and conception delay using reported sport fish consumption levels in the previous fishing year. The strength and direction of the association in currently married men between sport fish consumption in the past 12 months and conception delay were similar in respondents to the original survey and in the sample of nonrespondents we contacted (Stein et al., 1999). We conclude that nonresponse bias is unlikely to be the explanation for the association seen in our current study. A particular strength of our study is that we attempted to examine the contributions of sportcaught fish consumption of both members of the couple simultaneously. Estimates of both sportcaught fish consumption and reproductive histories of partners are highly correlated. This might explain the similar trends that were observed in men and women. To separate out these effects, we further tested whether the effect of one’s own sport-caught fish consumption persisted once knowledge of one’s partner’s consumption was taken into account. When the partner’s fish consumption was entered into the model for women, any association between her own sport-caught fish consumption and conception delay completely disappeared. However, the effect persisted among men. This suggests that any effect of sport-caught fish consumption on conception delay is restricted to men only. We wish to emphasize that, in our view, these findings are only suggestive. We will be very interested to see whether we are able to replicate these results in our prospective reproductive health study which addresses many of the limitations described (Courval et al., 1999).
REFERENCES Allen, J. R., Barsotti, D. A., Lambrecht, L. K., and Van Miller, J. P. (1979). Reproductive effects of halogenated aromatic hydrocarbons on nonhuman primates. Ann. NY Acad. Sci. 419—425. Aulerich, R. J., and Ringer, R. K. (1977). Current status of PCB toxicity to mink, and effect on their reproduction. Arch. Environ. Contam. Toxicol. 6, 279—292. Courval, J. M., DeHoog, J. V., and Holzman, C. et al. (1996). Fish consumption and other characteristics of reproductive-aged Michigan anglers—a potential population for studying the effects of consumption of Great Lakes fish on reproductive health. Toxicol. Ind. Health. 12, 347—359. Courval, J. M., DeHoog, J. V., and Wirth, J. et al. (1999). Recruitment of males, females, and couples as participants for a multioutcome prospective study of human reproductive health. Submitted for publication.
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Gray, L.E., Jr., Ostby, J., Marshall, R., and Andrews, J. (1993). Reproductive and thyroid effects of low-level polychlorinated biphenyl (Aroclor 1254) exposure . Fundam. Appl. Toxicol. 20, 288—294. Hovinga, M., Sowers, M., and Humphrey, H. E. B. (1993). Environmental exposure and lifestyle predictors of lead, cadmium, PCB, and DDT levels in great lakes fish eaters. Arch. Environ. Health 48, 98—104. Humphrey, H. E. B. (1988). Chemical contaminants in the Great Lakes In ‘‘The Human Health Aspect of Toxic Contaminants
and Ecosystem Health; A Great Lakes Focus.’’ Wiley, New York. Krishnan, V., and Safe, S. (1993). Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PDDs), and dibenzofurans (PCDFs) as anti-estrogens in MCF-7 human breast cancer cells: Quantitative structure—activity relationships. Toxicol Appl. Pharmacol. 120, 55—61. Stein, A. D., Tay, E., and Courval, J. M. (1999). Absence of nonresponse bias in a study of sport-caught Great Lakes fish consumption and conception failure. Environ. Res. 80.
Sport-Caught Fish Consumption and Conception Delay in Licensed Michigan Anglers1 Jeanne M. Courval,* 2 Jane V. DeHoog,* Aryeh D. Stein,* Eugene M. Tay,* Jianping He,* Harold E. B. Humphrey,- and Nigel Paneth* *Department of Epidemiology, College of Human Medicine, Michigan State University, East Lansing, Michigan 48824-1316; and -Bureau of Epidemiology, Michigan Department of Community Health, Lansing, Michigan, 48809 Received January 9, 1998
woman’s partner included in the model, the OR were 0.8, 0.8, and 1.0, respectively. These data suggest a modest association, in men only, of sportcaught fish consumption with risk of conception delay. 1999 Academic Press Key Words: fish consumption; conception delay; Great Lakes.
Between 1993 and 1995, we surveyed 4931 licensed anglers aged 17–34 years residing in 10 Michigan counties bordering a Great Lake. Responses were received from 1443 anglers and 844 of their partners. Lifetime sport-caught fish consumption was estimated as the number of sport-caught fish meals consumed in the previous 12 months times years since 1970 in which sport-caught fish were consumed. Analysis was restricted to currently married couples (n ⴝ 626). Lifetime sport-caught fish consumption was categorized in men as 0 (14%); 1–114 (27%); 115–270 (30%); 271–1127 (29%) meals; and in women as 0 (28%); 1–54 (26%); 55–138 (27%); fand 139–1127 (19%) meals, respectively. Conception delay (ever having failed to conceive after 12 months of trying) was reported by 13% of both men and women. Among men, the unadjusted odds ratios (OR) for conception delay were 1.2, 1.3, and 2.0 across the three increasing levels of sport-caught fish consumption compared to none (trend test P ⴝ 0.06). After adjustment for age, race, region of Michigan, household income, educational attainment, smoking, alcohol consumption, and partner’s sport fish consumption, the OR for conception delay in men were 1.4, 1.8, and 2.8, respectively. In women, unadjusted OR for conception delay were 0.9, 1.0, and 1.4 with increasing sport-caught fish consumption (trend test P ⴝ 0.35). With the same covariates and the sport-caught fish consumption of the
INTRODUCTION
Polychlorinated biphenyls (PCBs) and organic pesticides, such as DDT and DDE, are widespread industrial contaminants in the Great Lakes basin. Although production and discharge of these compounds ceased in the 1970s, they persist in the environment and bioaccumulate in the food chain. Several studies in animals have suggested that elevated PCB levels may cause reproductive problems, including reproductive failure and effects on sexual development (Auerlich and Ringer, 1977; Allen et al., 1979; Gray et al., 1993; Krishnan and Safe, 1993). It has been hypothesized that these reproductive problems may be related to the tendency of this class of compounds to disrupt normal endocrine development. Few large human populations are chronically exposed to detectable levels of PCB. One group of people potentially at higher risk of PCB exposure is recreational anglers who consume their catch (Humphrey 1988). We are currently recruiting a population for a cohort study in which we will investigate associations between sport-caught fish consumption and human reproductive health. The analysis described here is based upon data from the baseline screening survey used to identify potential participants for the cohort study (Courval et al., 1996).
1 The Fisheaters Family Health Project is funded by the Great Lakes Human Health Effects Program, Agency for Toxic Substances and Disease Registry. Eugene Tay was recipient of a Science to Achieve Results (STAR) Graduate Fellowship from the Environmental Protection Agency. This study was approved by the Michigan State University Committee on Research Involving Human Subjects and was conducted according to the approved protocol. 2 To whom reprint requests should be addressed at Department of Epidemiology, Rollins School of Public Health, 1518 Clifton Road, NE, Atlanta, Georgia 30322.
S183 0013-9351/99 $30.00 Copyright 1999 by Academic Press All rights of reproduction in any form reserved.
S184
COURVAL ET AL.
MATERIALS AND METHODS
Screening Survey The methods and results of the screening survey have been previously described (Courval et al., 1996). Between 1993 and 1995, we surveyed a population of reproductive-aged (17—34 years old) Michigan anglers who lived in one of 10 Michigan counties bordering a Great Lake (Fig. 1). These anglers were identified from computerized fishing license information or from copies of fishing licenses, both of which were provided to us by the Michigan Department of Natural Resources. Licensed anglers were sent two questionnaires, one to be completed by the angler and one to be completed by their spouse or partner. The questionnaire solicited information concerning fishing habits and fish consumption, pregnancy and reproductive history, and selected demographic characteristics. Repeat mailings and a variety of small incentives were used to increase participation. We mailed surveys to 4931 households. The Post Office returned 505 surveys as undeliverable, and an additional 44 were returned uncompleted. A total of 1443 questionnaires were completed by licensed anglers, for a crude response rate of 29%. An additional 844 questionnaires were completed by other household members, usually
a partner, but occasionally a parent or an unrelated individual. In total, 2287 questionnaires were received. Population We defined a couple for this analysis as a male and a female returning their questionnaires together; 803 such couples were identified. Since we did not expect substantial numbers of unmarried people in this age range to have previously attempted to achieve pregnancy, we restricted the analysis to currently married couples. The sample for the present analysis thus consists of 626 married couples. Outcome of Interest We defined conception delay as a positive response to the question ‘‘Was there ever a period of 12 months or more during which you tried to conceive a child but were unable to?’’ Men were asked about attempts to father a child. Exposure Assessment We computed an index of lifetime fish consumption by multiplying the reported number of fish meals consumed in the previous 12 months by the number of years since 1970 in which any sportcaught fish was consumed. This method assumes that fish consumption patterns are relatively consistent across years that any fish is consumed. This index was then divided into four sex-specific consumption categories, with the lowest group including all those reporting no sport fish consumption. Statistical Methods
FIG. 1. Target counties for the Fisheaters Family Health Project, Michigan.
Initial analyses examined the distributions of all variables. Subsequently, we used logistic regression to investigate the impact of the consumption of sport-caught Great Lakes fish on conception delay among couples who responded to our screening survey. Analyses were conducted using SPSS (SPSS, Inc., Chicago, IL). Initial descriptive analyses, and unadjusted and adjusted logistic regression analyses, were stratified by sex. Conception requires contributions from both members of a couple. We tried to separate the male and female effects of sport fish consumption on conception delay in the logistic regression models by examining whether the association between an individual’s sport-caught fish consumption and conception delay persisted once information on their
S185
SPORT FISH CONSUMPTION AND CONCEPTION DELAY
partner’s sport fish consumption was taken into account. RESULTS
TABLE 1 Demographic, Health Behavior, and Sport Fish Related Characteristics of 626 Currently Married Couples Responding to a Survey of Reproductive-Aged Michigan Anglers, 1993–1995
Characteristics of Our Population Over 80% of women and over 90% of men were aged 25 years or older. Overall, the men in our study were slightly older than the women; 60% of men were at least 31-years old compared to 41% of the women. The overwhelming majority (greater than 94%) of respondents were Caucasian. A few identified themselves as Black, Hispanic, or Native American. About 40% of respondents had no postsecondary education. About 38% of men, and 15% of women, reported drinking alcohol at least weekly. In addition, 40% of men, and almost half of the women, reported never having smoked, while an additional 22% reported that they were former smokers. Men were more likely to have consumed any sport-caught fish than women and, among sport fish consumers, men ate more fish meals than women (Table 1). Approximately 80% of men had fathered a child, and a similar proportion of women had been pregnant (ever conceived). As would be expected, prevalence of prior conception increased with age (data not shown). About 13% of both men and women reported failing to conceive after 12 months of trying. Among women who reported a period of conception delay, over 75% also reported having at least one birth. We do not know whether the reported births followed episodes of reported delayed conception or occurred at a different period in life. Among women who had ever conceived, just over 10% had never had a live birth, and almost 25% had experienced one or more miscarriages. A small proportion had experienced a stillbirth or had had a child with a birth defect (Table 2). Logistic Regression Analyses We examined associations between selected demographic and behavioral characteristics, and prevalence of conception delay. Increased age, particularly among women, and non-Caucasian race were associated with increased prevalence of conception delay. A regional variation in conception delay was also noted. Current smoking was moderately associated with conception delay among women but not men, while former smoking was associated with conception delay in both sexes. Income, educational attainment, and alcohol intake were not associated with conception delay in either sex (Table 3).
Men
Women
Age (years)
425 years 26—30 years 31#years
% 7.6 32.2 60.2
% 15.6 43.0 41.4
Income
:$20,000/year $20,000—39,999/year 5$40,000/year
12.1 41.9 45.9
12.4 41.3 46.3
Region a
West Michigan Saginaw Bay SE Michigan Wayne county
34.5 27.7 13.8 24.0
34.5 27.5 13.8 24.0
Education
4High school Some college College graduate
43.8 34.7 21.4
38.7 39.7 21.6
Race/ethnicity
Caucasian Non-Caucasian
94.2 5.8
94.7 5.3
Alcohol use
None 41 drink/month 1—3 drinks/month 51 drink/week
7.8 33.7 19.5 38.2
12.2 54.6 17.3 15.1
Smoking
Never smoked Former smoker Current smoker
41.2 22.2 35.9
47.2 23.3 29.2
14.2 27.0 30.3 28.5
28.1 26.0 26.9 19.0
Lifetime consumption of sport-caught fish b None Low Medium High
a West Michigan—Muskegon, Ottawa, Allegan; Saginaw Bay— Bay, Midland, Saginaw; SE Michigan—St. Clair, Macomb, Monroe; Wayne County—Wayne County. b Men: low, 1—114 meals; medium, 115—270 meals; high, 271—1127 meals. Women: low, 1—54 meals; medium, 55—138 meals; high, 139—1127 meals.
In unadjusted logistic regression analyses, a modest association between high lifetime sport-caught fish consumption and conception delay was observed for women. A slightly stronger association was noted among men, with those in the highest consumption group having an odds ratio of 2.0 relative to those with no consumption (Table 4). For women, the test for trend was not significant (P"0.35). For men, the test for linear trend was of marginal significance, with a P value of 0.06. In women, the odds ratios were unaltered after adjustment for potential confounders, but in men, the associations were strengthened when several potential confounders,
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TABLE 2
TABLE 3
Reproductive History of 626 Currently Married Couples Responding to a Survey of Reproductive-Aged Michigan Anglers, 1993–1995
Unadjusted Odds Ratios (95% Confidence Intervals) for the Associations between Conception Delay and Potential Confounders in 626 Currently Married Couples Responding to a Survey of Reproductive-Aged Michigan Anglers, 1993–1995
Men (%)
Women (%)
Ever conceived Yes No
77.9 22.1
82.7 17.3
Conception delay Yes No
12.9 87.1
13.3 86.7
— — — —
10.6 22.5 1.2 3.7
Men
Prior reproductive events (In females who have conceived) No live birth 51 miscarriage 51 stillbirth 51 child with birth defects
namely region of residence, age, race, education, income, smoking, and alcohol were included in the model. In women, the odds ratio for the highest sport fish consumption group was 1.4 relative to nonconsumers. In men, the comparable odds ratio was 2.4 (Table 4). We further tested whether the effect of one’s own sport-caught fish consumption persisted once knowledge of one’s partner’s consumption was taken into account. When the partner’s fish consumption was entered into the model for women, any association between her own sport-caught fish consumption and conception delay completely disappeared. However, when the partner’s fish consumption was entered into the model for men, the association between his sport-caught fish consumption and conception delay did not change (Table 4). DISCUSSION
Alternative explanations for our findings need to be considered. Our data are cross sectional, and we do not know whether the reported period of conception delay followed, coincided with, or preceded the critical period of fish consumption. Nor do we know whether the current partner, from whom we obtained fish consumption data, was indeed the partner during the period of attempted conception. We have controlled in our analysis for several potential confounders that we assessed in our survey. However, other unmeasured variables may possibly explain the association we describe. In our study, increased sport fish consumption is strongly associated with increased fishing activity in both males and females (P:0.001). If increased fishing
Women
OR (95% C.I.)
OR
(95% C.I.)
Age 425 years 26—30 years 31#years
(—) b 1.6 1.6
(0.5—4.5) (0.5—4.6)
(—) 3.0 2.1
(1.2—7.2) (0.8—5.1)
Race Caucasian Non-Caucasian
(—) 2.2
(1.0—5.0)
(—) 1.9
(0.8—4.6)
Income :$20,000/year $20,000—39,999/year 5$40,000/year
(—) 1.1 1.0
(0.5—2.4) (0.5—2.3)
(—) 0.9 1.0
(0.4—2.0) (0.5—2.1)
Regiona West Michigan Saginaw Bay SE Michigan Wayne County
(—) 0.5 1.1 1.2
(0.3—1.0) (0.5—2.2) (0.7—2.1)
(—) 0.6 0.9 1.1
(0.3—1.1) (0.5—1.9) (0.6—2.0)
Education 4High school Some college College graduate
(—) 0.9 0.8
(0.5—1.5) (0.4—1.5)
(—) 0.8 1.2
(0.5—1.4) (0.6—2.1)
Smoking Never smoked Former smoker Current smoker
(—) 1.5 1.0
(0.8—2.6) (0.6—1.7)
(—) 1.5 1.6
(0.8—2.6) (0.9—2.7)
Alcohol in past year None 41 drink/month 1—3 drinks/month 51 drink/week
(—) 1.4 1.1 1.3
(0.5—3.9) (0.4—3.3) (0.5—3.5)
(—) 0.9 1.0 1.0
(0.4—1.8) (0.5—2.4) (0.4—2.3)
a West Michigan—Muskegon, Ottawa, Allegan; Saginaw Bay— Bay, Midland, Saginaw; SE Michigan—St. Clair, Macomb, Monroe; Wayne County—Wayne County. b (—) denotes reference category.
activity is, in turn, associated with increased time away from the spouse, an alternative explanation for our findings could be that increased fishing activity results in reduced opportunity for conception to occur. We think this is unlikely to be the case because recreational anglers in the regions we surveyed are thought to do most of their fishing in lakes and streams near their residences, which would not require time away from home. In the screening survey we do not have information on whether couples were truly ‘‘at risk’’ for conception during their 12 months of trying, that is, we do not know whether there were
SPORT FISH CONSUMPTION AND CONCEPTION DELAY
TABLE 4 Associations between Conception Delay and Lifetime Sport Fish Consumption in 626 Currently Married Couples Responding to a Survey of Reproductive-Aged Michigan Anglers, 1993–1995 Men a
Lifetime sport-caught fish meals
Womenb
Unadjusted odds ratios None Low Medium High
OR (—) 1.2 1.3 2.0
(95% C.I.) OR (—) (0.5—2.9) 0.9 (0.6—3.1) 1.0 (0.9—4.5) 1.4
(95% C.I.)
Adjusted odds ratiosc None Low Medium High
(—) 1.3 1.5 2.4
(0.5—3.2) (0.6—3.5) (1.0—5.7)
(—) 0.9 1.0 1.4
(0.4—1.8) (0.5—2.0) (0.7—3.0)
Adjusted odds ratiosd None Low Medium High
(—) 1.4 1.8 2.8
(0.5—3.9) (0.6—5.0) (1.0—8.0)
(—) 0.8 0.8 1.0
(0.4—1.9) (0.4—1.8) (0.4—2.4)
(0.5—1.8) (0.5—1.9) (0.7—2.7)
a
Men: low, 1—114 meals; medium, 115—270 meals; high, 271—1127 meals. b Women: low, 1—54 meals; medium, 55—138 meals; high, 139—1127 meals. c Adjusted for region, age, race, education, income, smoking, alcohol. d Also adjusted for partner’s sport-caught fish consumption.
separations from the spouse, nor do we have any idea of the frequency and timing of intercourse during this time. In our prospective reproductive cohort study (Courval et al., 1999) we will be able to address these issues more fully. This analysis provides only indirect evidence that environmental contaminants are associated with human reproductive health outcomes. We did not attempt to measure serum environmental contaminant levels in the screening survey population, and therefore cannot directly relate PCB or other contaminant burden to risk of conception delay. From other data, it is known that serum PCB levels are elevated in consumers of Great Lakes sportcaught fish, increase with reported amount of sport fish consumed, and are higher in males (Humphrey 1988; Hovinga et al., 1993). As in all surveys, there is always the concern that respondents may differ from nonrespondents, and that any association may be an artifact. We have examined this possibility in a substudy in which 268 of our nonrespondents were contacted by telephone about 2 years after the initial mailings. We were not able to repeat our exact analysis in these nonresponders because we did not ask about the number of
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years since 1970 that a person had consumed sport fish in the nonresponder substudy. Instead, we examined the association between sport fish consumption and conception delay using reported sport fish consumption levels in the previous fishing year. The strength and direction of the association in currently married men between sport fish consumption in the past 12 months and conception delay were similar in respondents to the original survey and in the sample of nonrespondents we contacted (Stein et al., 1999). We conclude that nonresponse bias is unlikely to be the explanation for the association seen in our current study. A particular strength of our study is that we attempted to examine the contributions of sportcaught fish consumption of both members of the couple simultaneously. Estimates of both sportcaught fish consumption and reproductive histories of partners are highly correlated. This might explain the similar trends that were observed in men and women. To separate out these effects, we further tested whether the effect of one’s own sport-caught fish consumption persisted once knowledge of one’s partner’s consumption was taken into account. When the partner’s fish consumption was entered into the model for women, any association between her own sport-caught fish consumption and conception delay completely disappeared. However, the effect persisted among men. This suggests that any effect of sport-caught fish consumption on conception delay is restricted to men only. We wish to emphasize that, in our view, these findings are only suggestive. We will be very interested to see whether we are able to replicate these results in our prospective reproductive health study which addresses many of the limitations described (Courval et al., 1999).
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Gray, L.E., Jr., Ostby, J., Marshall, R., and Andrews, J. (1993). Reproductive and thyroid effects of low-level polychlorinated biphenyl (Aroclor 1254) exposure . Fundam. Appl. Toxicol. 20, 288—294. Hovinga, M., Sowers, M., and Humphrey, H. E. B. (1993). Environmental exposure and lifestyle predictors of lead, cadmium, PCB, and DDT levels in great lakes fish eaters. Arch. Environ. Health 48, 98—104. Humphrey, H. E. B. (1988). Chemical contaminants in the Great Lakes In ‘‘The Human Health Aspect of Toxic Contaminants
and Ecosystem Health; A Great Lakes Focus.’’ Wiley, New York. Krishnan, V., and Safe, S. (1993). Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PDDs), and dibenzofurans (PCDFs) as anti-estrogens in MCF-7 human breast cancer cells: Quantitative structure—activity relationships. Toxicol Appl. Pharmacol. 120, 55—61. Stein, A. D., Tay, E., and Courval, J. M. (1999). Absence of nonresponse bias in a study of sport-caught Great Lakes fish consumption and conception failure. Environ. Res. 80.