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Prenatal exposure to influenza and schizophrenia in surinamese and Dutch Antillean immigrants to The Netherlands
SCHIZOPHRENIA RESEARCH ELSEVIER
Schizophrenia Research 30 ( 1998) 101- 103
Prenatal exposure to influenza and schizophrenia in Surinamese and Dutch Antillean immigrants to The Netherlands Jean-Paul Selten a,,, Joris Slaets b, Ren6 K a h n a a Department of Psychiatry, University of Utrecht, P.O. Box 85500, 3508 GA Utrecht, The Netherlands b Department of Geriatrics, Leyenburg Hospital, The Hague, The Netherlands
Received 14 April 1997; accepted 8 August 1997
Abstract
There is evidence of an increased incidence of schizophrenia in Afro-Caribbean immigrants to the UK and in Surinamese- and Dutch Antillean immigrants to The Netherlands. We tested the hypothesis that second-trimester exposure to the 1957 A2 influenza pandemic, which swept through the Caribbean in the same period as it affected Western Europe, contributes to this phenomenon. The dates of birth of immigrants, discharged from a Dutch psychiatric institute with a diagnosis of schizophrenia, were examined for any effect of the pandemic. Individuals who were in their second-trimester of fetal life at the peak of the pandemic were at no greater risk of developing schizophrenia than controls. © 1998 Elsevier Science B.V. Keywords: Schizophrenia; Influenza; Migration; Epidemiology
1. Introduction
The reports of a high incidence of schizophrenia in Caribbean immigrants to the U K (e.g., Harrison et al., 1988; King et al., 1994; Van Os et al., 1996) are supported by similar findings in The Netherlands. We examined data from the Dutch psychiatric registry and found that the risk of a first admission for schizophrenia was 3-4 times higher in young Surinamese and Dutch Antillean immigrants than in their Dutch-born peers (Selten and Sijben, 1994; Selten et al., 1997). The etiology of this phenomenon, however, is not known. A possible risk factor for schizophrenia is mater* Corresponding author. 0920-9964/98/$19.00 © 1998 ElsevierScience B.V. All rights reserved. PH S0920-9964(97)00105-9
nal exposure to influenza. The evidence supporting this hypothesis derives mainly from the 1957 A2 influenza pandemic. Mednick et al. (1988) noted an increase in schizophrenic births in people from Helsinki, who were in their second-trimester of fetal life during the epidemic. O'Callaghan et al. ( 1991 ) examined the dates of birth of schizophrenic inpatients in England and Wales and reported an increase in schizophrenic births in February and March 1958, 5 months after the peak of the pandemic. The results of several other studies, however, were negative (e.g., Selten and Slaets, 1994). Fahy et al. (1992) examined the possibility that maternal exposure to influenza contributes to the high incidence of schizophrenia in Caribbean immigrants to the UK. They collected data on
102
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patients hospitalized with a diagnosis of schizophrenia and found that an unusual proportion of the dates of birth of first-generation Caribbeans fell in March 1958. From a total of 33 patients born in the Caribbean in 1958, seven were born in March (data kindly provided by D r Fahy). The authors linked this finding to the 1957 pandemic, which swept through the Caribbean during the same months ( S e p t e m b e r - O c t o b e r 1957) as it affected Western Europe (Dunn, 1958; Payne, 1958). Only one patient of the second-generation was born in March 1958. We set out to examine whether the 1957 A2 influenza pandemic, which did not spare Surinam or The Netherlands Antilles (Dunn, 1958), was associated with an increased risk of schizophrenia for Surinamese- and Antillean-born immigrants to The Netherlands. Large-scale migration from Surinam and from the Netherlands Antilles occurred in the 1970s and 1980s. I f second-trimester exposure to A2 influenza is a risk factor for schizophrenia, one would expect an increase in schizophrenic births in the first four months of 1958. If the 5-month lag reported by O'Callaghan et al. (1991) occurs, one would expect an excess of such births in February and March 1958.
Numbers of livebirths on the islands of Curaqao and Aruba (where most Dutch Antilleans live) were available for most months of the 5-year period, but not for all months. There were no such data on the other islands of the Netherlands Antilles or on Surinam.
3. Results Results are shown in Table 1. From the 73 schizophrenic patients born in 1958, 57 were born in Surinam and 16 in the Netherlands Antilles. The number of schizophrenic births in March 1958 was lower than the mean for the same months in the four control years. The numbers of patients born in January, February or April 1958 were not significantly higher than the average numbers for the same months in the control years. When we analyzed data for both countries of birth and for both sexes separately, the results remained insignificant. As far as Curaqao and Aruba are concerned, our failure to find an increase in schizophrenic patients born in March 1958 is not explained by fluctuations in the population birth rate. The number of births in March 1958 ( n = 5 2 2 ) was higher than that for March 1956 ( n = 4 8 9 ) and
2. Method The Dutch psychiatric registry provided data on all Surinamese- and Dutch Antillean-born patients who were admitted to a Dutch psychiatric institute and discharged with a diagnosis of schizophrenia (ICD-8 or ICD-9) in the period 1970 1994. Details about the registry are given in Selten and Slaets (1994). We compared the numbers of patients born in each m o n t h of the period January-April 1958 to the numbers of patients born in the corresponding m o n t h of the previous and subsequent 2 years. For this purpose we calculated the mean for the monthly number of schizophrenic births in the four control months. We assumed a Poisson distribution and computed the 95% confidence interval for this mean. Next, we examined whether the numbers of schizophrenic births in any of the first four months of 1958 exceeded the upper limit of this 95% confidence interval.
Table 1 Surinamese and Dutch Antillean immigrants to The Netherlands, hospitalized with schizophrenia (1970-1994): monthly births in 1958, compared with average for control months. 1958
1956 57, 1959 60
Month of birth
n
Mean
(95%confidence interval)
January February March April May June July August September October November December
5 7 4 7 6 8 6 6 4 9 9 2
5.0 4.0 5.25 7.0 6.5 6.5 4.5 6.5 9.5 7.25 8.5 7.75
(1.6-11.7) (1.1-10.2) (1.8 12.0) (2.8 14.4) (2.5-13.7) (2.5-13.7) ( 1.4-11.0) (2.5-13.7) (4.5 17.7) (3.0-14.8) (3.8 16.4) (3.3 15.4)
J.-P. Selten et al. / Schizophrenia Research 30 (1998) 101 103
M a r c h 1959 ( n = 4 5 4 ) . D a t a o n M a r c h 1957 a n d M a r c h 1960 were n o t available.
4. Discussion There was n o significant rise in the n u m b e r s o f Surinamese- or D u t c h A n t i l l e a n - b o r n schizophrenic patients b o r n in the first four m o n t h s o f 1958. O n e l i m i t a t i o n o f o u r study was that m o n t h l y n u m b e r s o f livebirths in S u r i n a m a n d some o f the islands in the N e t h e r l a n d s Antilles were n o t available. A n o t h e r l i m i t a t i o n concerns the lack o f data o n the precise impact o f the p a n d e m i c in S u r i n a m a n d the N e t h e r l a n d s Antilles. The same limitations, however, applied to the F a h y et al. study, which was smaller t h a n ours. We conclude that there is insufficient evidence to s u p p o r t the claim that second-trimester exposure to the 1957 A2 influenza p a n d e m i c c o n t r i b u t e s to the high incidence o f schizophrenia in C a r i b b e a n - b o r n immigrants to Western Europe.
References Dunn, F., 1958. Pandemic influenza in 1957. Review of international spread of new Asian strain. JAMA 166, 1140-1148.
103
Fahy, T.A., Jones, P.B., Sham, P.C., Murray, R.M., 1992. Schizophrenia in Afro-Caribbeans in the UK following prenatal exposure to the 1957 A2 influenza epidemic. Schizophr. Res. 6, 98-99. Harrison, G., Owens, D., Holton, A., Neilson, D., Boot, D., 1988. A prospective study of severe mental disorder in AfroCaribbean patients. Psychol. Med. 18, 643-657. King, M., Coker, E., Leavey, G., Hoare, A., Johnson-Sabine, E., 1994. Incidence of psychotic illness in London: comparison of ethnic groups. Br. Med. J. 309, 1115 1119. Mednick, S.A., Machon, R.A., Huttunen, M.O., Bonett, D., 1988. Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch. Gen. Psychiatry 45, 189 192. O'Callaghan, E., Sham, P., Takei, N., Glover, G., Murray, R.M., 1991. Schizophrenia after prenatal exposure to 1957 A2 influenza epidemic. Lancet 337, 1248-1250. Payne, A.M., 1958. Some aspects of the epidemiology of the 1957 influenza epidemic. Proc. Royal Soc. Med. 51, 1009-1015. Selten, J.P., Sijben, A.E., 1994. First admission rates for schizophrenia in immigrants to the Netherlands. The Dutch national register. Soc. Psychiatry Psychiatr. Epidemiol. 29, 71-77. Selten, J.P., Slaets, J.P.J., 1994. Evidence against maternal influenza as a risk factor for schizophrenia. Br. J. Psychiatry 164, 674-676. Selten, J.P., Slaets, J.P.J., Kahn, R.S., 1997. Schizophrenia in Surinamese and Dutch Antillean immigrants to The Netherlands. Evidence of an increased incidence. Psychol. Med. 27, 807 811. Van Os, J., Castle, D.J., Takei, N., Der, G., Murray, R.M., 1996. Psychotic illness in ethnic minorities: clarification from the 1991 census. Psychol. Med. 26, 203-208.
Schizophrenia Research 30 ( 1998) 101- 103
Prenatal exposure to influenza and schizophrenia in Surinamese and Dutch Antillean immigrants to The Netherlands Jean-Paul Selten a,,, Joris Slaets b, Ren6 K a h n a a Department of Psychiatry, University of Utrecht, P.O. Box 85500, 3508 GA Utrecht, The Netherlands b Department of Geriatrics, Leyenburg Hospital, The Hague, The Netherlands
Received 14 April 1997; accepted 8 August 1997
Abstract
There is evidence of an increased incidence of schizophrenia in Afro-Caribbean immigrants to the UK and in Surinamese- and Dutch Antillean immigrants to The Netherlands. We tested the hypothesis that second-trimester exposure to the 1957 A2 influenza pandemic, which swept through the Caribbean in the same period as it affected Western Europe, contributes to this phenomenon. The dates of birth of immigrants, discharged from a Dutch psychiatric institute with a diagnosis of schizophrenia, were examined for any effect of the pandemic. Individuals who were in their second-trimester of fetal life at the peak of the pandemic were at no greater risk of developing schizophrenia than controls. © 1998 Elsevier Science B.V. Keywords: Schizophrenia; Influenza; Migration; Epidemiology
1. Introduction
The reports of a high incidence of schizophrenia in Caribbean immigrants to the U K (e.g., Harrison et al., 1988; King et al., 1994; Van Os et al., 1996) are supported by similar findings in The Netherlands. We examined data from the Dutch psychiatric registry and found that the risk of a first admission for schizophrenia was 3-4 times higher in young Surinamese and Dutch Antillean immigrants than in their Dutch-born peers (Selten and Sijben, 1994; Selten et al., 1997). The etiology of this phenomenon, however, is not known. A possible risk factor for schizophrenia is mater* Corresponding author. 0920-9964/98/$19.00 © 1998 ElsevierScience B.V. All rights reserved. PH S0920-9964(97)00105-9
nal exposure to influenza. The evidence supporting this hypothesis derives mainly from the 1957 A2 influenza pandemic. Mednick et al. (1988) noted an increase in schizophrenic births in people from Helsinki, who were in their second-trimester of fetal life during the epidemic. O'Callaghan et al. ( 1991 ) examined the dates of birth of schizophrenic inpatients in England and Wales and reported an increase in schizophrenic births in February and March 1958, 5 months after the peak of the pandemic. The results of several other studies, however, were negative (e.g., Selten and Slaets, 1994). Fahy et al. (1992) examined the possibility that maternal exposure to influenza contributes to the high incidence of schizophrenia in Caribbean immigrants to the UK. They collected data on
102
J.-P. Selten et al. / Schizophrenia Research 30 (1998) 101 103
patients hospitalized with a diagnosis of schizophrenia and found that an unusual proportion of the dates of birth of first-generation Caribbeans fell in March 1958. From a total of 33 patients born in the Caribbean in 1958, seven were born in March (data kindly provided by D r Fahy). The authors linked this finding to the 1957 pandemic, which swept through the Caribbean during the same months ( S e p t e m b e r - O c t o b e r 1957) as it affected Western Europe (Dunn, 1958; Payne, 1958). Only one patient of the second-generation was born in March 1958. We set out to examine whether the 1957 A2 influenza pandemic, which did not spare Surinam or The Netherlands Antilles (Dunn, 1958), was associated with an increased risk of schizophrenia for Surinamese- and Antillean-born immigrants to The Netherlands. Large-scale migration from Surinam and from the Netherlands Antilles occurred in the 1970s and 1980s. I f second-trimester exposure to A2 influenza is a risk factor for schizophrenia, one would expect an increase in schizophrenic births in the first four months of 1958. If the 5-month lag reported by O'Callaghan et al. (1991) occurs, one would expect an excess of such births in February and March 1958.
Numbers of livebirths on the islands of Curaqao and Aruba (where most Dutch Antilleans live) were available for most months of the 5-year period, but not for all months. There were no such data on the other islands of the Netherlands Antilles or on Surinam.
3. Results Results are shown in Table 1. From the 73 schizophrenic patients born in 1958, 57 were born in Surinam and 16 in the Netherlands Antilles. The number of schizophrenic births in March 1958 was lower than the mean for the same months in the four control years. The numbers of patients born in January, February or April 1958 were not significantly higher than the average numbers for the same months in the control years. When we analyzed data for both countries of birth and for both sexes separately, the results remained insignificant. As far as Curaqao and Aruba are concerned, our failure to find an increase in schizophrenic patients born in March 1958 is not explained by fluctuations in the population birth rate. The number of births in March 1958 ( n = 5 2 2 ) was higher than that for March 1956 ( n = 4 8 9 ) and
2. Method The Dutch psychiatric registry provided data on all Surinamese- and Dutch Antillean-born patients who were admitted to a Dutch psychiatric institute and discharged with a diagnosis of schizophrenia (ICD-8 or ICD-9) in the period 1970 1994. Details about the registry are given in Selten and Slaets (1994). We compared the numbers of patients born in each m o n t h of the period January-April 1958 to the numbers of patients born in the corresponding m o n t h of the previous and subsequent 2 years. For this purpose we calculated the mean for the monthly number of schizophrenic births in the four control months. We assumed a Poisson distribution and computed the 95% confidence interval for this mean. Next, we examined whether the numbers of schizophrenic births in any of the first four months of 1958 exceeded the upper limit of this 95% confidence interval.
Table 1 Surinamese and Dutch Antillean immigrants to The Netherlands, hospitalized with schizophrenia (1970-1994): monthly births in 1958, compared with average for control months. 1958
1956 57, 1959 60
Month of birth
n
Mean
(95%confidence interval)
January February March April May June July August September October November December
5 7 4 7 6 8 6 6 4 9 9 2
5.0 4.0 5.25 7.0 6.5 6.5 4.5 6.5 9.5 7.25 8.5 7.75
(1.6-11.7) (1.1-10.2) (1.8 12.0) (2.8 14.4) (2.5-13.7) (2.5-13.7) ( 1.4-11.0) (2.5-13.7) (4.5 17.7) (3.0-14.8) (3.8 16.4) (3.3 15.4)
J.-P. Selten et al. / Schizophrenia Research 30 (1998) 101 103
M a r c h 1959 ( n = 4 5 4 ) . D a t a o n M a r c h 1957 a n d M a r c h 1960 were n o t available.
4. Discussion There was n o significant rise in the n u m b e r s o f Surinamese- or D u t c h A n t i l l e a n - b o r n schizophrenic patients b o r n in the first four m o n t h s o f 1958. O n e l i m i t a t i o n o f o u r study was that m o n t h l y n u m b e r s o f livebirths in S u r i n a m a n d some o f the islands in the N e t h e r l a n d s Antilles were n o t available. A n o t h e r l i m i t a t i o n concerns the lack o f data o n the precise impact o f the p a n d e m i c in S u r i n a m a n d the N e t h e r l a n d s Antilles. The same limitations, however, applied to the F a h y et al. study, which was smaller t h a n ours. We conclude that there is insufficient evidence to s u p p o r t the claim that second-trimester exposure to the 1957 A2 influenza p a n d e m i c c o n t r i b u t e s to the high incidence o f schizophrenia in C a r i b b e a n - b o r n immigrants to Western Europe.
References Dunn, F., 1958. Pandemic influenza in 1957. Review of international spread of new Asian strain. JAMA 166, 1140-1148.
103
Fahy, T.A., Jones, P.B., Sham, P.C., Murray, R.M., 1992. Schizophrenia in Afro-Caribbeans in the UK following prenatal exposure to the 1957 A2 influenza epidemic. Schizophr. Res. 6, 98-99. Harrison, G., Owens, D., Holton, A., Neilson, D., Boot, D., 1988. A prospective study of severe mental disorder in AfroCaribbean patients. Psychol. Med. 18, 643-657. King, M., Coker, E., Leavey, G., Hoare, A., Johnson-Sabine, E., 1994. Incidence of psychotic illness in London: comparison of ethnic groups. Br. Med. J. 309, 1115 1119. Mednick, S.A., Machon, R.A., Huttunen, M.O., Bonett, D., 1988. Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch. Gen. Psychiatry 45, 189 192. O'Callaghan, E., Sham, P., Takei, N., Glover, G., Murray, R.M., 1991. Schizophrenia after prenatal exposure to 1957 A2 influenza epidemic. Lancet 337, 1248-1250. Payne, A.M., 1958. Some aspects of the epidemiology of the 1957 influenza epidemic. Proc. Royal Soc. Med. 51, 1009-1015. Selten, J.P., Sijben, A.E., 1994. First admission rates for schizophrenia in immigrants to the Netherlands. The Dutch national register. Soc. Psychiatry Psychiatr. Epidemiol. 29, 71-77. Selten, J.P., Slaets, J.P.J., 1994. Evidence against maternal influenza as a risk factor for schizophrenia. Br. J. Psychiatry 164, 674-676. Selten, J.P., Slaets, J.P.J., Kahn, R.S., 1997. Schizophrenia in Surinamese and Dutch Antillean immigrants to The Netherlands. Evidence of an increased incidence. Psychol. Med. 27, 807 811. Van Os, J., Castle, D.J., Takei, N., Der, G., Murray, R.M., 1996. Psychotic illness in ethnic minorities: clarification from the 1991 census. Psychol. Med. 26, 203-208.