J. bioso
Sci (1992) 24, 487^96
SECULAR TRENDS OF TWINNING RATE IN SWEDEN a
ULF HOGBERG* AND STIG WALLt * Department of Obstetrics and Gynaecology and ^Department of Epidemiology and Health Care Research, Umea University, Sweden Summary. The change in parity and maternal age in Sweden accounts for the decline in the twinning rate from the 19th century to the middle of the 20th century. The later decline in twinning rate cannot be explained by changes in maternal age and parity. Fecundity appears to be higher in mothers of twins than in other mothers. Introduction
The frequency of monozygotic twinning is nearly constant, with a rate of 3-5 per 1000, while the dizygotic twinning rate varies regionally between 5 and 49 per 1000 (Bulmer, 1970). The frequency of dizygotic twinning is subject to an intricate interaction between demographic, environmental, physiological and genetic components. A long-term temporal decline of twinning rate has been reported in developed countries (Eriksson, 1973; Allen, 1984). Family data and population differences suggest that dizygotic twin-proneness is inherited (Allen, 1984). It is hypothesised as a sex limited recessive trait. This would explain high twinning rates in endogamous populations, local breeding units, and declining rates with the break up of isolates (Eriksson, 1973). Such an effect could explain the secular decline in Finland and Sweden (Eriksson, 1973), although in France and Japan no correlation between inbreeding and high twinning rate has been reported. The twinning rate reaches a maximum at maternal age 37-38 (Bulmer, 1970; Hemon, Berger & Lazar, 1979). There is an upward trend of twinning rate with parity regardless of age. Further, parity and age amplify each other. Thus, a multiparous woman of 35-39 has a 4-5-fold higher rate than a primiparous teenage woman (Bulmer, 1970; Schneider, Bessis & Simmonet, 1979). Double or multiple ovulation is probably much more common than actual twinning. The early ultrasound diagnosis of twin pregnancy discloses that between one-third and one-half of those pregnancies end in singleton births (Schneider et al, 1979; Robinson & Caines, 1977; Levi, 1976). Twin-proneness seems to be related to high fecundity (Eriksson, 1973; Renkonnen, 1966; Rhine & Nance, 1976). Twinning rates could thereby indicate changes in fecundity. High number of motile spermatozoa is a risk factor for twin 487
488
U. Hogberg and S. Wall
pregnancy (Shelden et al, 1988). The decline in sperm counts, resulting in decreased fecundity, could be associated with the falling DZ twinning rate in developed countries (James, 1981). Twin-prone women are supposed to be more fecund. Thus, efficient contraception (i.e. the pill and the IUD) could have a negative impact on twinning rate (Allen, 1984). It is possible that pollution, toxic substances in air, water, food or tobacco, could also impair human reproduction (Allen, 1984). National and regional twinning rates from 18th and 19th century Sweden and Finland are the highest ever reported (Eriksson, 1973). The purpose of this study was to analyse the secular decline in twinning rates in Sweden in relation to changes of parity and maternal age. The study also assessed regional differences of fecundity and twinning rates in past Swedish populations.
Materials and method
Material from four sources has been used here. 1. Vital statistics from all deaneries in Sweden 1805-06 and 1855-56 (now in the Demographic Data Base at Umea University) were used to present the regional differences of twinning rate in 19th century Sweden. 2. Church books from seven Swedish parishes, (Nedertornea, Tuna, Svinnegarn. Trosa, Locknevi, Fleninge and Gullholmen), covering 0-27% of all births in Sweden during the 19th century, were used as a subsample. These parishes are not representative samples, but constitute the only information available for this period. The parishes are scattered throughout Sweden in rural areas where 90"/) of the population lived in that period. 3. For the period 1955-72, data on twin maternities by age and parity in the county of Vasterbotten were used. 4. For the period 1980-85, the Swedish Medical Birth Registry at the National Board of Health and Social Welfare was used. National data on birth order are available only for this period. Age and parity adjusted twinning rates, standardised by the direct method, were applied to describe time trends (Colton, 1974). The aetiologic fraction is defined as the difference between the number of observed cases (n0) and number of parity corrected cases (nc) divided by nc i.e. (n0 - nc)/nc (Kleinbaum, Kupper & Morgenstern, 1982; Walter, 1978; Brorsson & Wall, 1985). Fecundity in the seven parishes was analysed by the life table (density) method. Fecundity is defined as the incidence per month of first live births during the first five years of marriage. Results
The geographical variation of the twinning rate by diocese was small and no definite decline of twinning rate was ascertained during the first half of the 19th century (Table 1).
Twinning rates in Sweden
489
Table 1. Twinning rate by diocese in Sweden 1805-06 and 1855-56 1855-56
1805-06
Diocese
Sets of twins
Twinning rate
Sets of twins
Twinning rate
Uppsala Linkoping Skara Strangnas Vasteras Vaxjo Lund Goteborg Kalmar Karlstad Harnosand
275 261 181 174 231 153 353 227 93 165 171
180 170 15 2 15 9 169 13 6 161 147 17-5 139 156
377 308 270 225 264 239 546 330 133 297 287
21 0 14-4 136 16 3 15 2 13 7 14-9 13 2 17-4 13 5 14-4
Source: Demographic Data Base, Umea University.
Two hundred sets of twins from the seven parishes provided information on age and parity of the mothers. Their twinning rate of 15-4 was close to the 19th century national average and these data were used as a standard for examining the secular decline of twinning rate. The crude twinning rate declined from 15-4 to 130 between the 19th century and 1955-60 (Fig. 1). This decline can mainly be explained by the change in age distribution and parity of mothers since the
1800-1899
1955-60
1961-66
1967-72
1980-85
Fig. 1. Crude twinning rate, twin sets per 1000 maternities, in Sweden, 1800-1985 (180099: seven Swedish parishes; 1955-72: county of VSsterbotten; 1980-85: national statistics).
U. Hogberg and S. Wall
490
1800-18991955-60 1961-66 1967-72 1980-85 Fig. 2. Twinning rate by maternal age, 1800-1985 (1800-99: seven Swedish parishes; 1955-72; county of Vasterbotten, Sweden; 1980-85; Swedish Medical Birth Registry.
standardised rate in the period 1955-60 was 15-6 (Fig. 3). However, the twinning rate continued to decline, by 38% in 1961-66 (compared with the 19th century) and by 48% in the period 1967-72 (Fig. 1). The decline of the twinning rate during the last 30 years cannot be explained by the changes in age and parity (Fig. 3). When standardising the rates for the whole period 1955-72 the changed
^Standardized rate rate 1800-99
1955-60
1961-66
1967-72
Fig. 3. Twinning rate in Sweden 1800-1972, standardized by direct method (1800-99: seven Swedish parishes; 1955-72: county of Vasterbotten, Sweden).
Twinning rates in Sweden
491
Table 2. Effects of changing age distribution on twinning rate, 1955-72, Sweden Twinning Parity ! Crude rate Age adjusted rate No. of twin sets Observed Age adjusted 'Prevented' by change in age distribution Parity 2-3 Crude rate Age adjusted rate No. of twin sets Observed Age adjusted 'Prevented' by change in age distribution Parity 4+ Crude rate Age adjusted rate No. of twin sets Observed Age adjusted 'Prevented' by change in age distribution Total no. of twin sets 'prevented' by change in age distribution
1800-99*
8-9 8-9
14-9 14 9
1955-60t
86 91
7-3 7-3
65 69 4
59 59
15 5 170
102 10-7
149 163 14 20-7 20 7
1961-66t
99 103 4
1967-72t
68 7-3 54 59 5 81 7-3 76 68
15-7 170
13 8 14-2
120 12 1
57 61 4
39 40 1
22 22
5 22 (31/644 = 4-8%)
4
* Data from seven parishes; used as standard for age distribution, t Data from county of Vasterbotten.
distribution by age and parity had separate effects on the twinning rate, 4-8% and 4 1% respectively (Tables 2, 3). However, the combined effect of age and parity is not only additive but amplified as the 'prevented' fraction was 15-3% with age and parity combined (Table 4). This corresponds to the highest relative risk of twins to be found in multiparous women aged 30-39 (Table 5). The twinning rate for the period 1980-85 (9-6), is slightly higher than in 1967-72 (Fig. 2). Whether age and parity changes have had any influence on the increase could not be calculated as age and parity specific twinning rates are not available for 1980-85. The highest twinning rate (23-2) is observed in the age group 30-39 combined with parity 4+, with relative risks of 3-3 during the 19th century and 2-3 during the years 1967-72 (Table 5). The age and parity specific twinning rate decline is most pronounced in the age group 30-39 with parity 2+. This represents the major part of the decline during the last 30 years.
492
U. Hogberg and S. Wall
Table 3. Effects of changing parity distribution on twinning rate, 1955-72, Sweden 1800-99* Age 15-29 Crude rate Parity adjusted rate No. of twin sets Observed Parity adjusted 'Due to' change in parity distribution Age 30-39 Crude rate Parity adjusted rate No. of twin sets Observed Parity adjusted 'Due to' change in parity distribution Age 40+ Crude rate Parity adjusted rate No. of twin sets Observed Parity adjusted 'Due to' change in parity distribution
6-4 6-4
1955-60t
103 10-7 134 138 4
21-7 21-7
Total no. of twin sets 'due to' change in parity distribution
8-2 7-8 113 107
1967-72t
7-7 70 109 59
12 3 13 5
83 102
74 81 7
38 46 8
9-4 160
12-5 109
111 118
10 17 7
10 9
5 5
7 11 (26/620 = 41%)
8
18 6 18 5 127 126
12-5 12 5
1961-66t
*, t : as Table 2.
Table 4. Combined effects of changing age and parity distribution on twinning rate, 1955-72, Sweden 1800-99* Overall crude rate Age and parity adjusted rate
154 15-4
No. of twin sets Observed Adjusted
1955-60t 130 156 271 324
Not born by change in combined age and id parity distribution *, t: as Table 2.
1961-66t 9-6 113 197 231
34 53 (112/732 = 15-3%)
1967 72t 80 93 152 177 25
Twinning rates in Sweden
493
Table 5. Age and parity as risk factors for twinning rate, 1800-99 and 1955-72 Age and parity 15-29
40+
30-39
1
2-3
4+
1800-99* Twinning rate Relative risk Aetiologic cases Aetiologic fraction
70 10 0
4-6 0-7 0
— — 0
23-2 20 1 170 2-9 3-3 2-4 28-8 71 680 111 •6/200 = 56%
1955-72t Twinning rate Relative risk Aetiologic cases Aetiologic fraction
7-2 10 00
10 2 1-4 550
110 1-5 60
13 1 164 10 7 1-8 1-5 2-3 590 8-3 48-2 186 5/602 = 30 1%
1
2-3
4+
1
2-3
4+
18 5 2-6 06
13 8 20 1-5
120 17 6-2
13 8 1-9 50
10 3 1-4 50
*, t: as Table 2.
Only 23 sets of twins were observed among the 2499 first births in the seven parishes, too few to permit life table analysis. However, the cumulative pregnancy rate within 1 year of marriage was 0-82 and 0-67 for those mothers having twin and singleton births, respectively, at first delivery, which implies a higher fecundity for the twin mothers. Discussion
This study can be criticised for using different subsamples and national data. However, age and parity distributions of the mothers do not differ from national fertility data and therefore the methodology is considered appropriate and the results consistent. It has been proposed that parity and maternal age effects could only partly account for the secular decline of the twin rate in Sweden (Eriksson, 1973). Studies from Italy, the US and UK also suggest only a slight influence of age and parity on the secular decline of the twinning rate (James, 1975, 1980; Jeanneret & McMahon, 1962). However, results of this study suggest that the slow decline of twinning rate from the 19th century to 1960 in Sweden can be explained mainly by the changed distribution by age and parity of the mothers. The present study cannot explain the further decline in twinning rate during the years 1961-72 as only a minor part of the decline is caused by the changed age and parity distribution. The reasons for this decline are not clear (Allen, 1981, 1984). An increasing twinning rate is observed for the period 1980-85, mainly in the age group 30-39 years. This increase has been noticed since 1975, and could be caused by postponement of births to higher maternal ages, but
494
U. Hogberg and S. Wall
also by an increase in MZ twinning rate. Another explanation could be gonadotrophin stimulation. Furthermore, this study indicates that fecundity could be higher among women giving birth to twins than among those having a singleton first birth (Philippe & Roy, 1989). Although not statistically significant, the same tendency is shown in other studies (Bulmer, 1959; Allen, 1981). Is the further decline of twinning rate during the 1960s and 1970s associated with a decline in fecundity, caused either by a change in the human environment or by a change in human behaviour? A radical change in reproductive behaviour has occurred. During the 19th century, with a fertility rate of 4-2 children per woman, 44% of the married women produced two-thirds of the children (Hogberg & Ackerman, 1990). The pattern today, with a fertility rate of 1-6-20, is that reproduction is evenly distributed among the women. The fertility rate is thus more true for the individual woman of today than during the 19th century (Hogberg & Ackerman, 1990; Hogberg, Nilsson & Sandstrom, 1992). This is accomplished by efficient family planning (liberal abortion practice, oral contraceptives, IUD), introduced during the mid-1960s in Sweden (Hogberg, 1985). The small family norm from that time should have had an impact on the decline in twinning rate (Allen, 1981). The environmental pollution influence on twinning rate is under debate (James, 1981; Allen, 1981). Increased incidence of miscarriages is claimed to be one cause of the declining twin rate (Hemon et ai, 1979). However, when comparing Swedish women born in 1936-45 and 1946-60, no cohort differences in fecundability could be ascertained (Hogberg et ai, 1992). This does not support the theories that declining fecundity is the precursor of a declining twinning rate. To conclude, the study found independent effects of age and parity on twinning rates, but also an interaction implying that they amplify each other. Furthermore, there are indications of an association between high fecundity and risk of twin pregnancy. The changed distribution of mothers by age and parity explains the secular decline of twinning rate until the 1960s, while the continued decline thereafter remains unexplained. References ALLEN, G. (1981) Twinning and fertility paradox. Progr. din. biol. Res. 69A, 1. ALLEN, G. (1984) Multiple births. In: Perinatal, pp. 152-189. Edited by M. B. Brecker. Oxford University Press, Oxford. BRORSSON, B. & WALL, S. (1985) Assessment of Medical Technology—Problems and Methods. Swedish Medical Research Council, Stockholm. BULMER, M. G. (1959) The effect of parental age, parity and duration of marriage on the twinning rate. Ann. hum. Genet. 23, 454. BULMER, M. G. (1970) The Biology of Twinning in Man. Clarendon Press, Oxford. COLTON, T. (1974) Statistics in Medicine. Little Brown, Boston. ERIKSSON, A. (1973) Human twinning in and around the Aland Islands. Commentat. Biol. 64, 1. HEMON, D., BERGER, C. & LAZAR, P. (1979) The etiology of human dizygotic twinning with special reference to spontaneous abortions. Ada Genet, med. Gemell. 28, 253. HOGBERG, U. (1985) Maternal Mortality in Sweden. Umea University Medical Dissertations, New Series 156. Umea.
Twinning rates in Sweden
495
HOGBERG, U. & AKERMAN, S. (1990) Reproductive pattern among women in 19th century Sweden. / . biosoc. Sci. 22, 13. HOGBERG, U., NILSSON, N. G. & SANDSTR0M, A. (1992) Reproductive pattern among Swedish women born 1935-1960. In press. JAMES, W. (1975) The secular decline in dizygotic twinning rates in Italy. Ada Genet, med. Gemmell. 24, 9. JAMES. W. (1980) Secular changes in twinning rates in England and Wales. Ann. hum. Biol. 7, 485. JAMES. W. (1981) Has fecundability been declining in recent years in developed countries? J. biosoc. Sci. 13, 419. JEANNERET, G. & MCMAHON, B. (1962) Secular changes in rates of multiple births in the United States. Am. J. hum. Genet. 14, 410. KLEINBAUM, D. G., KUPPER, L. L. & MORGENSTERN, H. (1982) Epidemiologic Research,
Principles and Quantitative Methods. Van Nostrand Reinhold, New York. LEVI, S. (1976) Ultrasonic assessment of the high rate of human multiple pregnancy in the first trimester. J. din. Ultrasound. 4, 3. PHILIPPE, P. & ROY, R. (1989) Conceptive delays of twin-prone mothers: a demographic epidemiologic approach. Hum. Biol. 61, 599. RENKONNEN. K. (1966) The mothers of twins and their fertility. Ann. Med. e.xp. Fenn. 44. 322. RHINE, S. & NANCE, W. (1976) Familial twinning: a case for superfetation in man. Actu Genet. med. Gemmell. 25, 66. ROBINSON, H. & CAINES, J. (1977) Sonar evidence of early pregnancy failure in patients with twin conceptions. Br. J. Obstet. Gynaec. 84, 22. SHELDEN, R., KEMMAN, E.. BOHRER, M. & PASUALE. S. (1988) Multiple gestation is associated
with the use of high sperm numbers in the intrauterine insemination specimen in women undergoing gonadotropin stimulation. Fert. Steril. 49, 607. SCHNEIDER, L.. BESSIS, R. & SIMMONET. T. (1979) The frequency of uvular resorption during the first trimester of twin pregnancy. Acta Genet, med. Gemmell. 28, 271. WALTER. S. (1978) Calculation of attributable risks from epidemiological data. Int. J. Epidemiol. 7. 175. Received 20th February 1991
12 44 97 153
1 3 15 19
36
52
112
200
706 2,185 4,174 7,065
54 218 1,250 1,522
4,057
1 2-3 4+ Crude rate Parity adj
1 Crude rate Age adj
2-3 Crude rate 3,492 Age adj
4+ Crude rate 5,424 Age adj
12,973
30-39 1 2-3 4+ Crude rate Parity adj
40+
Overall crude rate Age and parity adj
20,488
20,813
130 156
15 4 15-4
2,817
15 7 170
3.632
20-7 20-7 271 202
57 92-7
9.669
15-5 170
149 59-5
9.604
14 9 14 9
8,002
8-6 91
65 37
39 262 498 799
762 3,499 1,746 6,007
7,203 5,980 573 13,756
7,577
10 6 9-7 9-4 160
12 6 197 19-3 18 6 18-5
81 131 9-5 10 3 *
8-9 8-9
3 7 10 24
12 71 44 127 131
53 75 6 134
58 284 723 1,065
951 3,609 2,275 6,835
6,568 5,711 634 12,913
18 5 13-8 120 12 5 12 5
170 20 1 23-2 21 7 21 7
6-4 6-4
70 4-6
1967-72
120 121 22 656 1,833 19,073
13-8 14 2 96 11-3
39 77-2 197 146-6
80 9-3
81 7-3 76 25-8 9,361 10-2 10 7 990 37-5
152 121-2
6-8 7-3
54 29-8 7,879
11-2 12 5 111 11-8
129 5-2 120 8-3 10 2
7-3 7-3
2 3 5 18
8 16 14 38 72-7
6-3 90 116 7.7 *
590 29
32 178 239 449
620 2,763 1,164 4,547
46 58 5 109
19 1 100 12-5 109
6-6 120 15 5 12 3 13 5
5 42 27 74 95-7
7,227 6,420 430 14,077
5 5 10 16 7
7-5 8-7 12-2 8-2 *
54 52 7 113
Twin Twinning Twinning Twin Twinning Maternities sets Maternities; sets rate rate rate
1961-66
Not calculated since no cases occurred in the standard group 15 29 of age and parity 4+.
28
4,386
15-29 1 2-3 4+ Crude rate Parity adj
1955-60
Twin Twin Twinning Maternities i sets rate Maternities sets
23 5
Parity
3,297 1,089
Age
1800-99
Table A. Background data
Appendix
§ a. •
Q-
Cto :
Sci (1992) 24, 487^96
SECULAR TRENDS OF TWINNING RATE IN SWEDEN a
ULF HOGBERG* AND STIG WALLt * Department of Obstetrics and Gynaecology and ^Department of Epidemiology and Health Care Research, Umea University, Sweden Summary. The change in parity and maternal age in Sweden accounts for the decline in the twinning rate from the 19th century to the middle of the 20th century. The later decline in twinning rate cannot be explained by changes in maternal age and parity. Fecundity appears to be higher in mothers of twins than in other mothers. Introduction
The frequency of monozygotic twinning is nearly constant, with a rate of 3-5 per 1000, while the dizygotic twinning rate varies regionally between 5 and 49 per 1000 (Bulmer, 1970). The frequency of dizygotic twinning is subject to an intricate interaction between demographic, environmental, physiological and genetic components. A long-term temporal decline of twinning rate has been reported in developed countries (Eriksson, 1973; Allen, 1984). Family data and population differences suggest that dizygotic twin-proneness is inherited (Allen, 1984). It is hypothesised as a sex limited recessive trait. This would explain high twinning rates in endogamous populations, local breeding units, and declining rates with the break up of isolates (Eriksson, 1973). Such an effect could explain the secular decline in Finland and Sweden (Eriksson, 1973), although in France and Japan no correlation between inbreeding and high twinning rate has been reported. The twinning rate reaches a maximum at maternal age 37-38 (Bulmer, 1970; Hemon, Berger & Lazar, 1979). There is an upward trend of twinning rate with parity regardless of age. Further, parity and age amplify each other. Thus, a multiparous woman of 35-39 has a 4-5-fold higher rate than a primiparous teenage woman (Bulmer, 1970; Schneider, Bessis & Simmonet, 1979). Double or multiple ovulation is probably much more common than actual twinning. The early ultrasound diagnosis of twin pregnancy discloses that between one-third and one-half of those pregnancies end in singleton births (Schneider et al, 1979; Robinson & Caines, 1977; Levi, 1976). Twin-proneness seems to be related to high fecundity (Eriksson, 1973; Renkonnen, 1966; Rhine & Nance, 1976). Twinning rates could thereby indicate changes in fecundity. High number of motile spermatozoa is a risk factor for twin 487
488
U. Hogberg and S. Wall
pregnancy (Shelden et al, 1988). The decline in sperm counts, resulting in decreased fecundity, could be associated with the falling DZ twinning rate in developed countries (James, 1981). Twin-prone women are supposed to be more fecund. Thus, efficient contraception (i.e. the pill and the IUD) could have a negative impact on twinning rate (Allen, 1984). It is possible that pollution, toxic substances in air, water, food or tobacco, could also impair human reproduction (Allen, 1984). National and regional twinning rates from 18th and 19th century Sweden and Finland are the highest ever reported (Eriksson, 1973). The purpose of this study was to analyse the secular decline in twinning rates in Sweden in relation to changes of parity and maternal age. The study also assessed regional differences of fecundity and twinning rates in past Swedish populations.
Materials and method
Material from four sources has been used here. 1. Vital statistics from all deaneries in Sweden 1805-06 and 1855-56 (now in the Demographic Data Base at Umea University) were used to present the regional differences of twinning rate in 19th century Sweden. 2. Church books from seven Swedish parishes, (Nedertornea, Tuna, Svinnegarn. Trosa, Locknevi, Fleninge and Gullholmen), covering 0-27% of all births in Sweden during the 19th century, were used as a subsample. These parishes are not representative samples, but constitute the only information available for this period. The parishes are scattered throughout Sweden in rural areas where 90"/) of the population lived in that period. 3. For the period 1955-72, data on twin maternities by age and parity in the county of Vasterbotten were used. 4. For the period 1980-85, the Swedish Medical Birth Registry at the National Board of Health and Social Welfare was used. National data on birth order are available only for this period. Age and parity adjusted twinning rates, standardised by the direct method, were applied to describe time trends (Colton, 1974). The aetiologic fraction is defined as the difference between the number of observed cases (n0) and number of parity corrected cases (nc) divided by nc i.e. (n0 - nc)/nc (Kleinbaum, Kupper & Morgenstern, 1982; Walter, 1978; Brorsson & Wall, 1985). Fecundity in the seven parishes was analysed by the life table (density) method. Fecundity is defined as the incidence per month of first live births during the first five years of marriage. Results
The geographical variation of the twinning rate by diocese was small and no definite decline of twinning rate was ascertained during the first half of the 19th century (Table 1).
Twinning rates in Sweden
489
Table 1. Twinning rate by diocese in Sweden 1805-06 and 1855-56 1855-56
1805-06
Diocese
Sets of twins
Twinning rate
Sets of twins
Twinning rate
Uppsala Linkoping Skara Strangnas Vasteras Vaxjo Lund Goteborg Kalmar Karlstad Harnosand
275 261 181 174 231 153 353 227 93 165 171
180 170 15 2 15 9 169 13 6 161 147 17-5 139 156
377 308 270 225 264 239 546 330 133 297 287
21 0 14-4 136 16 3 15 2 13 7 14-9 13 2 17-4 13 5 14-4
Source: Demographic Data Base, Umea University.
Two hundred sets of twins from the seven parishes provided information on age and parity of the mothers. Their twinning rate of 15-4 was close to the 19th century national average and these data were used as a standard for examining the secular decline of twinning rate. The crude twinning rate declined from 15-4 to 130 between the 19th century and 1955-60 (Fig. 1). This decline can mainly be explained by the change in age distribution and parity of mothers since the
1800-1899
1955-60
1961-66
1967-72
1980-85
Fig. 1. Crude twinning rate, twin sets per 1000 maternities, in Sweden, 1800-1985 (180099: seven Swedish parishes; 1955-72: county of VSsterbotten; 1980-85: national statistics).
U. Hogberg and S. Wall
490
1800-18991955-60 1961-66 1967-72 1980-85 Fig. 2. Twinning rate by maternal age, 1800-1985 (1800-99: seven Swedish parishes; 1955-72; county of Vasterbotten, Sweden; 1980-85; Swedish Medical Birth Registry.
standardised rate in the period 1955-60 was 15-6 (Fig. 3). However, the twinning rate continued to decline, by 38% in 1961-66 (compared with the 19th century) and by 48% in the period 1967-72 (Fig. 1). The decline of the twinning rate during the last 30 years cannot be explained by the changes in age and parity (Fig. 3). When standardising the rates for the whole period 1955-72 the changed
^Standardized rate rate 1800-99
1955-60
1961-66
1967-72
Fig. 3. Twinning rate in Sweden 1800-1972, standardized by direct method (1800-99: seven Swedish parishes; 1955-72: county of Vasterbotten, Sweden).
Twinning rates in Sweden
491
Table 2. Effects of changing age distribution on twinning rate, 1955-72, Sweden Twinning Parity ! Crude rate Age adjusted rate No. of twin sets Observed Age adjusted 'Prevented' by change in age distribution Parity 2-3 Crude rate Age adjusted rate No. of twin sets Observed Age adjusted 'Prevented' by change in age distribution Parity 4+ Crude rate Age adjusted rate No. of twin sets Observed Age adjusted 'Prevented' by change in age distribution Total no. of twin sets 'prevented' by change in age distribution
1800-99*
8-9 8-9
14-9 14 9
1955-60t
86 91
7-3 7-3
65 69 4
59 59
15 5 170
102 10-7
149 163 14 20-7 20 7
1961-66t
99 103 4
1967-72t
68 7-3 54 59 5 81 7-3 76 68
15-7 170
13 8 14-2
120 12 1
57 61 4
39 40 1
22 22
5 22 (31/644 = 4-8%)
4
* Data from seven parishes; used as standard for age distribution, t Data from county of Vasterbotten.
distribution by age and parity had separate effects on the twinning rate, 4-8% and 4 1% respectively (Tables 2, 3). However, the combined effect of age and parity is not only additive but amplified as the 'prevented' fraction was 15-3% with age and parity combined (Table 4). This corresponds to the highest relative risk of twins to be found in multiparous women aged 30-39 (Table 5). The twinning rate for the period 1980-85 (9-6), is slightly higher than in 1967-72 (Fig. 2). Whether age and parity changes have had any influence on the increase could not be calculated as age and parity specific twinning rates are not available for 1980-85. The highest twinning rate (23-2) is observed in the age group 30-39 combined with parity 4+, with relative risks of 3-3 during the 19th century and 2-3 during the years 1967-72 (Table 5). The age and parity specific twinning rate decline is most pronounced in the age group 30-39 with parity 2+. This represents the major part of the decline during the last 30 years.
492
U. Hogberg and S. Wall
Table 3. Effects of changing parity distribution on twinning rate, 1955-72, Sweden 1800-99* Age 15-29 Crude rate Parity adjusted rate No. of twin sets Observed Parity adjusted 'Due to' change in parity distribution Age 30-39 Crude rate Parity adjusted rate No. of twin sets Observed Parity adjusted 'Due to' change in parity distribution Age 40+ Crude rate Parity adjusted rate No. of twin sets Observed Parity adjusted 'Due to' change in parity distribution
6-4 6-4
1955-60t
103 10-7 134 138 4
21-7 21-7
Total no. of twin sets 'due to' change in parity distribution
8-2 7-8 113 107
1967-72t
7-7 70 109 59
12 3 13 5
83 102
74 81 7
38 46 8
9-4 160
12-5 109
111 118
10 17 7
10 9
5 5
7 11 (26/620 = 41%)
8
18 6 18 5 127 126
12-5 12 5
1961-66t
*, t : as Table 2.
Table 4. Combined effects of changing age and parity distribution on twinning rate, 1955-72, Sweden 1800-99* Overall crude rate Age and parity adjusted rate
154 15-4
No. of twin sets Observed Adjusted
1955-60t 130 156 271 324
Not born by change in combined age and id parity distribution *, t: as Table 2.
1961-66t 9-6 113 197 231
34 53 (112/732 = 15-3%)
1967 72t 80 93 152 177 25
Twinning rates in Sweden
493
Table 5. Age and parity as risk factors for twinning rate, 1800-99 and 1955-72 Age and parity 15-29
40+
30-39
1
2-3
4+
1800-99* Twinning rate Relative risk Aetiologic cases Aetiologic fraction
70 10 0
4-6 0-7 0
— — 0
23-2 20 1 170 2-9 3-3 2-4 28-8 71 680 111 •6/200 = 56%
1955-72t Twinning rate Relative risk Aetiologic cases Aetiologic fraction
7-2 10 00
10 2 1-4 550
110 1-5 60
13 1 164 10 7 1-8 1-5 2-3 590 8-3 48-2 186 5/602 = 30 1%
1
2-3
4+
1
2-3
4+
18 5 2-6 06
13 8 20 1-5
120 17 6-2
13 8 1-9 50
10 3 1-4 50
*, t: as Table 2.
Only 23 sets of twins were observed among the 2499 first births in the seven parishes, too few to permit life table analysis. However, the cumulative pregnancy rate within 1 year of marriage was 0-82 and 0-67 for those mothers having twin and singleton births, respectively, at first delivery, which implies a higher fecundity for the twin mothers. Discussion
This study can be criticised for using different subsamples and national data. However, age and parity distributions of the mothers do not differ from national fertility data and therefore the methodology is considered appropriate and the results consistent. It has been proposed that parity and maternal age effects could only partly account for the secular decline of the twin rate in Sweden (Eriksson, 1973). Studies from Italy, the US and UK also suggest only a slight influence of age and parity on the secular decline of the twinning rate (James, 1975, 1980; Jeanneret & McMahon, 1962). However, results of this study suggest that the slow decline of twinning rate from the 19th century to 1960 in Sweden can be explained mainly by the changed distribution by age and parity of the mothers. The present study cannot explain the further decline in twinning rate during the years 1961-72 as only a minor part of the decline is caused by the changed age and parity distribution. The reasons for this decline are not clear (Allen, 1981, 1984). An increasing twinning rate is observed for the period 1980-85, mainly in the age group 30-39 years. This increase has been noticed since 1975, and could be caused by postponement of births to higher maternal ages, but
494
U. Hogberg and S. Wall
also by an increase in MZ twinning rate. Another explanation could be gonadotrophin stimulation. Furthermore, this study indicates that fecundity could be higher among women giving birth to twins than among those having a singleton first birth (Philippe & Roy, 1989). Although not statistically significant, the same tendency is shown in other studies (Bulmer, 1959; Allen, 1981). Is the further decline of twinning rate during the 1960s and 1970s associated with a decline in fecundity, caused either by a change in the human environment or by a change in human behaviour? A radical change in reproductive behaviour has occurred. During the 19th century, with a fertility rate of 4-2 children per woman, 44% of the married women produced two-thirds of the children (Hogberg & Ackerman, 1990). The pattern today, with a fertility rate of 1-6-20, is that reproduction is evenly distributed among the women. The fertility rate is thus more true for the individual woman of today than during the 19th century (Hogberg & Ackerman, 1990; Hogberg, Nilsson & Sandstrom, 1992). This is accomplished by efficient family planning (liberal abortion practice, oral contraceptives, IUD), introduced during the mid-1960s in Sweden (Hogberg, 1985). The small family norm from that time should have had an impact on the decline in twinning rate (Allen, 1981). The environmental pollution influence on twinning rate is under debate (James, 1981; Allen, 1981). Increased incidence of miscarriages is claimed to be one cause of the declining twin rate (Hemon et ai, 1979). However, when comparing Swedish women born in 1936-45 and 1946-60, no cohort differences in fecundability could be ascertained (Hogberg et ai, 1992). This does not support the theories that declining fecundity is the precursor of a declining twinning rate. To conclude, the study found independent effects of age and parity on twinning rates, but also an interaction implying that they amplify each other. Furthermore, there are indications of an association between high fecundity and risk of twin pregnancy. The changed distribution of mothers by age and parity explains the secular decline of twinning rate until the 1960s, while the continued decline thereafter remains unexplained. References ALLEN, G. (1981) Twinning and fertility paradox. Progr. din. biol. Res. 69A, 1. ALLEN, G. (1984) Multiple births. In: Perinatal, pp. 152-189. Edited by M. B. Brecker. Oxford University Press, Oxford. BRORSSON, B. & WALL, S. (1985) Assessment of Medical Technology—Problems and Methods. Swedish Medical Research Council, Stockholm. BULMER, M. G. (1959) The effect of parental age, parity and duration of marriage on the twinning rate. Ann. hum. Genet. 23, 454. BULMER, M. G. (1970) The Biology of Twinning in Man. Clarendon Press, Oxford. COLTON, T. (1974) Statistics in Medicine. Little Brown, Boston. ERIKSSON, A. (1973) Human twinning in and around the Aland Islands. Commentat. Biol. 64, 1. HEMON, D., BERGER, C. & LAZAR, P. (1979) The etiology of human dizygotic twinning with special reference to spontaneous abortions. Ada Genet, med. Gemell. 28, 253. HOGBERG, U. (1985) Maternal Mortality in Sweden. Umea University Medical Dissertations, New Series 156. Umea.
Twinning rates in Sweden
495
HOGBERG, U. & AKERMAN, S. (1990) Reproductive pattern among women in 19th century Sweden. / . biosoc. Sci. 22, 13. HOGBERG, U., NILSSON, N. G. & SANDSTR0M, A. (1992) Reproductive pattern among Swedish women born 1935-1960. In press. JAMES, W. (1975) The secular decline in dizygotic twinning rates in Italy. Ada Genet, med. Gemmell. 24, 9. JAMES. W. (1980) Secular changes in twinning rates in England and Wales. Ann. hum. Biol. 7, 485. JAMES. W. (1981) Has fecundability been declining in recent years in developed countries? J. biosoc. Sci. 13, 419. JEANNERET, G. & MCMAHON, B. (1962) Secular changes in rates of multiple births in the United States. Am. J. hum. Genet. 14, 410. KLEINBAUM, D. G., KUPPER, L. L. & MORGENSTERN, H. (1982) Epidemiologic Research,
Principles and Quantitative Methods. Van Nostrand Reinhold, New York. LEVI, S. (1976) Ultrasonic assessment of the high rate of human multiple pregnancy in the first trimester. J. din. Ultrasound. 4, 3. PHILIPPE, P. & ROY, R. (1989) Conceptive delays of twin-prone mothers: a demographic epidemiologic approach. Hum. Biol. 61, 599. RENKONNEN. K. (1966) The mothers of twins and their fertility. Ann. Med. e.xp. Fenn. 44. 322. RHINE, S. & NANCE, W. (1976) Familial twinning: a case for superfetation in man. Actu Genet. med. Gemmell. 25, 66. ROBINSON, H. & CAINES, J. (1977) Sonar evidence of early pregnancy failure in patients with twin conceptions. Br. J. Obstet. Gynaec. 84, 22. SHELDEN, R., KEMMAN, E.. BOHRER, M. & PASUALE. S. (1988) Multiple gestation is associated
with the use of high sperm numbers in the intrauterine insemination specimen in women undergoing gonadotropin stimulation. Fert. Steril. 49, 607. SCHNEIDER, L.. BESSIS, R. & SIMMONET. T. (1979) The frequency of uvular resorption during the first trimester of twin pregnancy. Acta Genet, med. Gemmell. 28, 271. WALTER. S. (1978) Calculation of attributable risks from epidemiological data. Int. J. Epidemiol. 7. 175. Received 20th February 1991
12 44 97 153
1 3 15 19
36
52
112
200
706 2,185 4,174 7,065
54 218 1,250 1,522
4,057
1 2-3 4+ Crude rate Parity adj
1 Crude rate Age adj
2-3 Crude rate 3,492 Age adj
4+ Crude rate 5,424 Age adj
12,973
30-39 1 2-3 4+ Crude rate Parity adj
40+
Overall crude rate Age and parity adj
20,488
20,813
130 156
15 4 15-4
2,817
15 7 170
3.632
20-7 20-7 271 202
57 92-7
9.669
15-5 170
149 59-5
9.604
14 9 14 9
8,002
8-6 91
65 37
39 262 498 799
762 3,499 1,746 6,007
7,203 5,980 573 13,756
7,577
10 6 9-7 9-4 160
12 6 197 19-3 18 6 18-5
81 131 9-5 10 3 *
8-9 8-9
3 7 10 24
12 71 44 127 131
53 75 6 134
58 284 723 1,065
951 3,609 2,275 6,835
6,568 5,711 634 12,913
18 5 13-8 120 12 5 12 5
170 20 1 23-2 21 7 21 7
6-4 6-4
70 4-6
1967-72
120 121 22 656 1,833 19,073
13-8 14 2 96 11-3
39 77-2 197 146-6
80 9-3
81 7-3 76 25-8 9,361 10-2 10 7 990 37-5
152 121-2
6-8 7-3
54 29-8 7,879
11-2 12 5 111 11-8
129 5-2 120 8-3 10 2
7-3 7-3
2 3 5 18
8 16 14 38 72-7
6-3 90 116 7.7 *
590 29
32 178 239 449
620 2,763 1,164 4,547
46 58 5 109
19 1 100 12-5 109
6-6 120 15 5 12 3 13 5
5 42 27 74 95-7
7,227 6,420 430 14,077
5 5 10 16 7
7-5 8-7 12-2 8-2 *
54 52 7 113
Twin Twinning Twinning Twin Twinning Maternities sets Maternities; sets rate rate rate
1961-66
Not calculated since no cases occurred in the standard group 15 29 of age and parity 4+.
28
4,386
15-29 1 2-3 4+ Crude rate Parity adj
1955-60
Twin Twin Twinning Maternities i sets rate Maternities sets
23 5
Parity
3,297 1,089
Age
1800-99
Table A. Background data
Appendix
§ a. •
Q-
Cto :
