Schizophrenia

Time Trends in Schizophrenia: Changes in Obstetric Risk Factors with Industrialization


By Richard Warner
Schizophrenia Bulletin, Vol. 21, No. 3, 1995
National Institute of Mental Health

Abstract

The frequency of schizophrenia may have increased during the early stages of industrialization and may now be declining. Early in the process of development, the illness appeared to be more common among the upper classes and later, more common in the lower classes. As with certain other diseases, the occurrence of schizophrenia may be influenced by the transition from poverty to affluence. Explanations for such a pattern of occurrence include the combined effect of (1) variation in the rate of birth complications owing to cephalopelvic disproportion secondary to changes in nutrition, and (2) increased infant survival following improvements in obstetric and neonatal care. These effects help elucidate the pattern of occurrence of schizophrenia in immigrant groups.

Schizophrenia Bulletin, 21(3): 483-500, 1995.


There are indications of time trends in the occurrence of schizophrenia, which, if accurate, may offer clues to the etiology of the condition. Evidence presented below suggests that in the developed world, the illness increased in incidence with the advance of industrialization and has, in recent decades, been on the decline. Moreover, during the early stages of industrial development in the developing world, the illness appears to be more prevalent in the upper classes and may, only later, become more common in the lower classes. This article suggests that, if this changing pattern of occurrence is correct, neurodevelopmental factors provide a possible explanation. Data on the incidence of schizophrenia in immigrants are thus examined to test the accuracy of the hypothesis.

The Rise of Schizophrenia

Schizophrenia does not appear to be a recent disease: conditions resembling the illness were identified in ancient India and Rome and were distinguished from mania, depression, catatonic stupor, and delirium (Jeste et al. 1985). Schizophrenia-like syndromes, however, may have been much less common before the 18th century. The records of Napier, an English medieval physician who specialized in the care of the mentally ill, suggest that the condition closest to our modern category of schizophrenia, "mopishness," was not common in his day (Ellard 1987).

The total number of the identified insane in England grew dramatically throughout the Victorian era (Scull 1979), as did asylum admission rates (see figure 1). First admissions doubled between 1869 and 1900 (Hare 1983). An editorial in the Times (London) of 1877 quipped, "If lunacy continues to increase as at present, the insane will be in the majority, and, freeing themselves, will put the sane in asylums" (Scull 1979, p. 225). Many Victorian asylum superintendents argued that this trend was an artifact of the increasing recognition of those in need of treatment, while others believed that there was an actual increase in mental disorder. Hare (1983) suggests that increased recognition of insanity cannot explain a sustained growth rate on such a scale over several decades. If increasing numbers of mild cases were being admitted to the asylums, one would expect to find decreasing death rates and increasing recovery rates, and this was not the case.

The apparent increase in the occurrence of insanity was by no means confined to England. Tuke (1894) reported a 36-percent increase in the rate of first admissions to Irish asylums between 1875 and 1892, and similar increases were noted in the United States (Grob 1973), Italy (Tagliavini 1985), and elsewhere.

Hare (1988) argues that it was primarily early-onset schizophrenia (included in the contemporary term "melancholia") that increased during the 19th century and suggests that a new biological factor, such as the mutation of a virus or a change in the immunological defenses of the general population, occurred around 1800.

Even at the end of the 19th century schizophrenia appears to have been relatively rare. Jablensky (1986) reports that only 9 percent of men and 7 percent of women first admitted to the University Psychiatric Clinic in Munich in 1908 were diagnoses (some by Kraepelin himself) as suffering from dementia praecox. A substantial increase in schizophrenia, Jablensky suggests, occurred in the present century.

In summary, it seems possible that schizophrenia became more prevalent during the 19th and early 20th centuries, presumably in response to socioenvironmental changes associated with industrial growth. Possible biological mediating mechanisms include nutritional, obstetric, immunogical, and infectious causes, which will be discussed later.

The Fall of Schizophrenia

Several researchers have pointed out that the incidence of schizophrenia in developed countries appears to have declined in recent years (see figure 2). Studies examining changes in this rate since 1960 are listed in table 1. Three-quarters of these studies indicate a decrease in the incidence of the illness since 1960, and the remainder reveal no change or an increase. All of the studies rely on first-admission rates to some form of treatment service; the figures are age standardized in many instances. A study from rural Ireland with a somewhat different methodology found the morbid risk for schizophrenia to be constant for those born between 1920 and 1939 but to have fallen by 37 percent for those born between 1940 and 1969 (Waddington and Youssef 1994) - a change that would also be expected to produce a decrease in incidence beginning around 1960.

Table 1. Temporal trends in the incidence of schizophrenia in the developed world since 1960
Author(s) and year Country Period Measure Change in frequency
Eagles & Whalley (1985) Scotland 1969-78 Age-standardized first-admission rate 49% decrease
Parker et al. (1985) New South Wales, Australia 1967-77 Number of first admissions 9% decrease
Dickson & Kendell (1986) Scotland 1970-81 Number of first admissions 48% decrease
Hafner & an der Heiden (1986) Mannheim, Germany 1963-80 First-contact rates 18% increase
Munk-Jorgensen (1986) Denmark 1970-84 Age-standardized first-admission rates 37% decrease
Munk-Jorgensen & Jorgensen (1986) Denmark 1970-84 Age-standardized first- admission rates 44% decrease (female)
Joyce (1987) New Zealand 1974-84 Number of first admissions 37% decrease
Eagles et al. (1988) Aberdeen, Scotland 1969-84 Age-standardized first- contact rates 54% decrease
de Alarcon et al. (1990) Oxford, England 1975-86 Age-standardized first-contact rates Age-standardized first-ever diagnosis rate 50% decrease (males & females)
Der et al. (1990) United Kingdom 1970-86 First-admission rates 40% decrease (males) 50% decrease (females)
Folnegovic et al. (1990) Croatia 1965-84 First-admission rates No change
Bamrah et al. (1991) Salford, England 1974-84 Age-standardized first-contact rates 64% increase
Castle et al. (1991) Camberwell, England 1965-84 Age-standardized first-contact rates 25% increase (ICD-9) 40% increase (RDC)
38% increase (DSM-III)
Harrison et al. (1991) Nottingham, England 1975-87 Age-specific first-contact rates No change
Munk-Jorgensen & Mortensen (1992) Denmark 1969-88 First-ever admission rates 50% decrease
Geddes et al. (1993) Scotland 1969-8 Age-standardized first admission rates 43% decrease (males) 57% decrease (females)
Kendell et al. (1993) Edinburgh, Scotland 1971-89 Age-standardized first-admission rates 38% decrease (males) 59% decrease (females)
D'Arcy et al. (1993) Saskatchewan, Canada 1979-90 First-contact rate 66% decrease
Note. -- ICD-9 = International Classification of Diseases (World Health Organization 1978); RDC = Research Diagnostic Criteria (Spitzer et al. 1978); DSM-III = Diagnositic and Statistical Manual of Mental Disorders, 3rd ed. (American Psychiatric Association 1980).

The decrease observed in these studies could be an artifact created by a number of factors, such as a diagnostic shift from schizophrenia to other categories. Mortensen and colleagues (1991) suggest that the decline in admissions for schizophrenia in Denmark was matched by an increase in borderline states, paranoid and "unspecified" psychoses. Parker et al. (1985) found that the decrease in the treated incidence of schizophrenia in New South Wales was accompanied by an increase in the diagnosis of manic-depressive illness following the introduction of lithium carbonate. Other studies (Dickson and Kendell 1986; Eagles et al. 1988) show a similar increase in the prevalence of affective psychoses. Kendell and coworkers (1993) found that the proportion of patients diagnosed with schizophrenia at first admission to the Royal Edinburgh Hospital in Scotland decreased by 22 percent between 1971 and 1989. No such decline was apparent, however, when the diagnosis was made using data from the patient records and a computer algorithm. A comparison of trends in France and Britain between 1973 and 1982 (van Os et al. 1993) led to the conclusion that a diagnostic drift occurred in opposite directions in the two countries, producing a diverging incidence of schizophrenia. In Britain, an increase in the use of standardized criteria may have led to an increase in "other psychoses" and a decrease in schizophrenia. In France, psychoanalytic influence produced a broadening of the concept of schizophrenia and may have increased the number of diagnosed cases (van Os et al. 1993). Yet, neither de Alarcon and associates (1990) looking at data from Oxfordshire, nor Der and colleagues (1990) examining British national data, nor Geddes and coworkers (1993) using Scottish figures could find evidence of a reciprocal rise in other diagnostic categories.

An artifact may result from cases being missed by traditional treatment-based statistics (Crow 1990; Munk-Jorgensen and Mortensen 1992). Since the introduction of antipsychotic drugs, greater numbers of psychotic patients can be treated successfully as outpatients and never admitted to inpatient care (Graham 1990). In Oxfordshire, however, it has been shown that schizophrenia at first contact, including outpatient contact, has been declining (de Alarcon et al. 1990). Some schizophrenia patients may be treated by general practitioners without referral to specialty psychiatric services (de Alarcon et al. 1990), and postwar changes in hospital admission policy may have led to more people with psychoses evading any kind of treatment. A recent incidence study of schizophrenia in Nottingham, England, for instance, found that 10 percent of the cases that were ultimately detected were missed by the original screening procedure because they were only fleetingly in contact with the treatment facilities (Cooper et al. 1987); other cases with no contact with the treatment system would have escaped detection altogether.

Several reviewers have concluded that the case for the declining incidence of schizophrenia in the Western industrial world is to date unproven but merits further investigation (Castle 1993; Harrison and Mason 1993; Jablensky 1993). If there is a true decrease, the finding would be of considerable etiological significance. Proposed mechanisms include a decrease in the fertility of people with schizophrenia, a change in the population's immunity to an infectious agent, and a decrease in brain damage resulting from improvements in obstetric care.

A recent decrease in the fertility of people with schizophrenia is unlikely. For the incidence of schizophrenia to have decreased throughout the 1970s, it would have been necessary for a change in the fertility of such people to have been in effect through the 1950s. The decrease in the use of hospital confinement for the mentally ill since the mid-1950s makes it more likely that fertility has been increasing rather than decreasing in this group. The fertility of schizophrenia patients, moreover, is unlikely to have a major impact on the incidence of the illness because only 11 percent of people with schizophrenia have a parent with the condition (Gottesman 1991). Obstetric and infectious causes will be discussed later.

Caste and Class

As explained further on, certain diseases, such as thyrotoxicosis and coronary artery disease, initially increase in incidence among the upper classes as industrialization progresses and later become a predominantly lower class disease. There are indications that schizophrenia may fit this pattern of occurrence.

Schizophrenia is more common among the lower socioeconomic classes and more prevalent in lower class districts of many cities of the industrial world (Faris and Dunham 1939; Schroeder 1942; Gerard and Houston 1953; Hare 1956; Sundby and Nyhus 1963; Gardner and Babigian 1966; Klee et al. 1967; Giggs and Cooper 1987), as well as among the lower classes of a number of city population samples (Clark 1949; Odegard 1956; Stein 1957; Hollingshead and Redlich 1958; Srole et al. 1962; Leighton et al. 1963). The drift of individuals with schizophrenia or prepsychotic illnesses into lower status occupations may partly explain the concentration of schizophrenia in the poorer classes (Goldberg and Morrison 1963; Turner and Wagenfeld 1967; Jones et al. 1993). Further observations suggest, however, that a class-specific environmental factor is also involved: the social class gradient for schizophrenia is weak or absent in rural areas of the developed world (Leighton et al. 1971; Kohn 1973; Eaton 1974; Brown et al. 1977; Nielsen and Nielsen 1977) and slopes in the reverse direction in peasant cultures and nonindustrialized parts of the world.

Postwar Italy. In the early 1950s, in the Province of Lazio (largely rural at that time, even though it includes the city of Rome), schizophrenia was most commonly reported among the better educated, such as clerical workers and professionals (Rose 1964). However, this pattern could have been a result of differing referral rates between classes or diagnostic bias.

India. Several studies from India have found schizophrenia to be more common in high castes than in lower castes. First-admission rates for schizophrenia to the public mental hospital in Bihar State in 1959-60 were nearly 50 times greater among the highest caste than among the lowest (Rao 1966). A similar increased frequency of schizophrenia in higher socioeconomic groups in an Indian clinic has been reported by Varma and coworkers (1980).

As with the Italian data, these treatment-based statistics may be an artifact of higher referral rates in the more educated castes. However, field surveys in rural as well as urban areas, unaffected by referral patterns, confirm the greater occurrence of schizophrenia among the higher castes in India, sometimes by three or four times that found among the lower castes (Elnagar et al. 1971; Dube and Kumar 1972; Carstairs and Kapur 1976; Nandi et al. 1980). The statistics derived by these surveys are prevalence, not incidence, figures and could be affected by higher death and recovery rates among lower caste people with schizophrenia.

Taiwan. In a study from Taiwan, the Third World inverted social class gradient appeared to switch to the Western urban pattern of occurrence as the society became industrialized. In 1946-48, the prevalence of schizophrenia among the Chinese in Taiwan was high among the upper classes and merchants, increasing with higher levels of education. By 1961-63, however, after a period of dramatic industrial growth and urbanization, the patterns of illness had switched to those of the Western World (Lin et al. 1969). As table 2 indicates, the primary reason for the inverted gradient in 1946-48, is the unusually high prevalence in the upper classes, which dropped down to standard levels by 1961-63. Thus, it is not likely, in this case, that the inverted prevalence gradient was a result of higher death and recovery rates among the lower classes.

Table 2. Prevalence of schizophrenia per 1,000 of the Taiwanese Chinese population in 1946-48 and 1961-63
  1946-48 1961-63
Social class
    Upper 3.5 0.8
    Middle 1.2 1.1
    Lower 4.5 2.1
Occupation
    Professional 0.0 0.0
    Merchant 3.6 0.9
    Salaried worker 0.9 0.4
    Laborer 1.7 1.9
    Farmer and fisherman 1.7 1.1
    Unemployed 3.8 5.5
Education
    College 18.2 0.0
    Senior high school 13.0 1.9
    Junior high school 5.7 0.0
    Elementary education 1.1 1.2
    No formal education 3.8 3.7
Source of data. -- Lin et al. (1969).

Japan. A similar switch from an inverted social class gradient to a Western pattern can be identified in industrializing Japan. In contrast to European and American studies of the period (Brugger 1931, 1933; Hyde and Kingsley 1944; Bremer 1951), Japanese epidemiological surveys published in the early 1940s failed to find a higher prevalence of schizophrenia in the lowest social class (Tsugawa et al. 1942; Akimoto et al. 1943). For example, in the town of Komoro at that time, the prevalence of schizophrenia was more than four times greater in the highest class than in the lowest (Akimoto et al. 1943). More recent research indicates that the Japanese social class gradient for schizophrenia has since shifted to the usual Western pattern (Nakane et al. 1992; Ohta et al. 1992). Many changes in postwar Japanese society, including altered patterns of nutrition leading to a substantial increase in children's height and weight, have accompanied this shift (Reischauer 1977).

The high prevalence rates among high-caste Indians, higher class Japanese, and well-educated Taiwanese cannot be the result of social drift. Caste is immutable, and mentally impaired people will not drift up the class scale or into higher education. The high rates could be due to a tendency of psychiatrists to overdiagnose schizophrenia selectively in higher class/caste patients early in the process of industrialization, but there are no prior reasons to suppose this to be true. As in the case of the rising and falling incidence of schizophrenia, possible biological mediating factors include differences in nutritional, obstetric, infectious, and immunological factors related to affluence.

19th-Century British Isles. Was schizophrenia more common in the upper classes in the early stages of Western industrial development? There are few data to answer this question. Dementia praecox was not defined as an entity until late in the 19th century, and systematic information on the class or occupation of patients is not available for the early phases of the industrial revolution, when the higher classes were first exposed to the effects of affluence (Taylor 1975). We know that the increase in the number of paupers in asylums in England and Wales between 1844 and 1900 was substantially greater than the increase in private patients (Parry-Jones 1972), but the private/pauper distinction may not accurately reflect the patients' social class. Many pauper patients came from "respectable" classes and fell upon public support because, as the Commissioners of Lunacy pointed out in 1855, "Any protracted attack of insanity ... seldom fails to reduce its immediate victims, and generally also their families with them, to poverty, and ultimately to pauperism" (Scull 1979, p. 242). Moreover, since upper- and middle-class families regarded the asylum as a place of last resort (MacKenzie 1985), many mentally ill relatives were kept at home, and the number of affluent insane may have been far greater than admission figures suggest. Some sources suggest that the lower classes, in fact, may not have been over-represented in the asylum population of the mid-19th century. In Ireland in 1865, for example, there was no apparent social class gradient: according to the asylum inspectors, the class background of the insane was similar to that of Irish society outside the asylum (Finnane 1981).

Etiological Significance

It seems likely that the occurrence of schizophrenia in the West increased during the last century and possible that it has peaked and has been decreasing over the past two or three decades. In preindustrial settings, the illness appears to be more prevalent in the upper castes and classes, but in the postindustrial West, the illness is more common in the poorer urban classes. The epidemiology of other diseases offers clues to explain this pattern of occurrence.

Some illnesses, such as breast cancer, are diseases of affluence. They tend to rise in incidence with the advance of industrialization and to be more prevalent among the upper classes. Other illnesses, such as rheumatic heart disease, are diseases of poverty. Their incidence declines as industrial development progresses, and they are more common in the lower classes (Barker 1989). There is yet a third category: illnesses that are influenced by both affluence and poverty and that rise in incidence early in the process of development and fall in frequency later (see figure 3). These illnesses, which include thyrotoxicosis, peptic ulcer, poliomyelitis, appendicitis, and coronary artery disease (Barker 1989), are initially more common among the rich but later become more common among the poor. The reasons for the rise and fall in incidence vary from condition to condition but are generally related to a change in hygiene or diet, which acts in childhood to modify individual susceptibility to the same factor or a different one, exerting an effect later in life to produce illness. For example, people whose dietary iodine is deficient in youth appear less able to adapt to an increase in iodine intake later in life and thus are more likely to develop thyrotoxicosis (Barker and Phillips 1984). Gupta and Murray (1991) have previously noted that schizophrenia fits some features of this third pattern of occurrence. The evidence presented above suggests that schizophrenia may conform to this pattern in all respects. Neuro-developmental factors are prominent among the potential causes.

Industrialization and the Hazards of Childbirth. Obstetric complications are related to the subsequent development of schizophrenia (McNeil 1987), the risk for people born with complications being two to three times greater than that for people born without (Goodman 1988). Complications of delivery, rather than of pregnancy, are more likely to occur with increased frequency in schizophrenia samples; and oxygen deprivation, especially owing to prolonged labor, appears to be the common denominator among these complications (McNeil 1988). In four studies cited by McNeil (1988), prolonged labor occurred in 17 to 40 percent of schizophrenia samples compared with 8 to 19 percent of control subjects. Some argue that those who develop schizophrenia following obstetric trauma tend to be people without a genetic vulnerability to the illness (Wilcox and Nasrallah 1987; Schwarzkopf et al. 1989). Others suggest, in contrast, that the genetic predisposition to schizophrenia may be a nervous system fragility that renders brain tissue more sensitive to the effects of oxygen deprivation or intracranial bleeding (Cannon et al. 1989; Fish et al. 1992). On balance, it is likely that obstetric complications are a risk factor for people with or without genetic vulnerability (McNeil 1988).

Changes associated with industrialization alter the risk of obstetric complications differentially in the various classes. Delivery complications due to pelvic contraction (diminished pelvic size), for example, are more common in women who suffered childhood rickets secondary to vitamin D deficiency. In the 1960s, pelvic contraction owing to rickets was reported in only 2 percent of white women in the United States but in 15 percent of black women (Eastman and Hellman 1961). Improvements in nutrition during industrial development reach the upper classes first, but the first generation of women who gain this benefit will be relatively small in stature and at risk for bony deformities because, as children, their nutrition was inferior. Consequently, the first generation of more affluent women will tend to have relatively small pelvic dimensions and, when pregnant, will carry large, well-nourished fetuses. In a series of Third World studies, birthweights of infants born to prosperous women were 6 to 26 percent greater than those of infants born to poor women (Siegel and Morris 1970). The result for the newly affluent will be an increase in cephalopelvic disproportion (the fetal head being disproportionately larger than the birth canal), prolonged labor, and brain damage in the new generation of infants.

Another consequence will be increased infant mortality in the upwardly mobile classes. As figure 4 shows, infant mortality, despite a progressive downward trend, rose in concert with the rate of industrial growth in Victorian Britain, suggesting that periods of affluence at that time exerted an adverse effect on neonatal health. An increase in obstetric complications could lead to a rise in both perinatal deaths and numbers of surviving brain-damaged infants; as neonatal care improves, the proportion of surviving brain-damaged infants will increase even though infant mortality may continue to be high.

Improvements in neonatal care in the early phase of industrialization become available sooner to the upper classes. This bias increases the tendency for children born with obstetric complications to high-income women to survive infancy with brain damage while similar low-income children die early in life. The increased rates of both brain damage and survival could, in turn, lead to higher schizophrenia rates in the upper classes.

In the later phases of industrial development, women of higher socioeconomic standing and with good nutrition from birth will have relatively well-formed pelvic cavities. Additionally, further advances in obstetric care that decrease the risk of fetal brain trauma, such as the more frequent use of cesarean section, tend to be selectively available to the upper classes. Both of these factors will eventually lead to lower brain damage rates and a subsequent decrease in the incidence of schizophrenia in the upper classes. In the 1958 British Perinatal Mortality Survey, maternal height was substantially greater and perinatal mortality was less in the higher social classes compared to the lower ones (Butler and Bonham 1963). Women of low socioeconomic status do not realize the benefits of improved obstetric care as soon. Low birthweight, an indicator of delayed intrauterine development, premature delivery, and other obstetric complications, is more common among black infants in the United States than among white infants (North and MacDonald 1977). Like children born after prolonged labor, these low-birthweight infants are at greater risk for schizophrenia (Lane and Albee 1966; Stabenau and Pollin 1967) and have more periventricular brain damage (a common finding in schizophrenia) (Cannon et al. 1989). The risk of schizophrenia in the contemporary low-income population, moreover, is not moderated by poor survival rates of affected infants; black low-birthweight infants have higher survival rates than white ones (North and MacDonald 1977).

Recent developments in obstetric and neonatal care may account for the putative decrease in the incidence of schizophrenia. The postwar decline in early perinatal mortality rates in England and Wales was paralleled by the subsequent fall, 20 years later, in the first-admission rates for schizophrenia in the 1960s and 1970s (Gupta and Murray 1991). The differential impact of these advances on various socioeconomic groups may explain why the apparent decrease in schizophrenia has been greatest in the more prosperous regions of the United Kingdom (Gupta and Murray 1991), and why the districts that show no decrease in schizophrenia have large immigrant populations with high rates of poverty (Eagles 1991a).

The nutritional/obstetric hypothesis is supported by Hare's (1988) observation that it was the early onset form of schizophrenia -- the type most likely to have a neurodevelopmental origin (Murray et al. 1992) that appears to have increased most dramatically during the 19th century. The theory also gains support from Geddes and coworkers (1993), who found that Scottish schizophrenia rates after 1969 appear to have declined to a greater extent in younger age groups, suggesting a birth cohort effect.

It has been argued that if obstetric complications were crucial to the etiology of schizophrenia, the incidence of the illness would be substantially higher in the Third World, where obstetric care is worse (Gureje et al. 1994). In fact, this appears to be the case. Among modern studies listed by Eaton (1991) as using reliable diagnostic criteria, broad case finding, and adequate sample size, all three of the Third World studies included are among the four with the highest rates. For example, in the 10-country World Health Organization Determinants of Outcome study (Jablensky et al. 1992), which provides standardized, comparable incidence data, the age-corrected incidence of broadly diagnosed schizophrenia is roughly twice as great in the two developing world samples reporting such data (rural and urban Chandigarh, India) (0.42 and 0.35 per 1,000) as in the developed world centers (0.16 to 0.28 per 1,000). A study from Madras (Eaton 1991) confirms the impression of an elevated incidence of schizophrenia in India (0.58 per 1,000, age corrected). Two factors may prevent the Third World incidence of schizophrenia from reaching greater heights. First, brain-damaged infants have a lower rate of survival in the Third World. Second, widespread pregnancy food taboos restrict the consumption of protein by pregnant women in the developing world: these have the effect, and sometimes the explicit intent, of limiting the size of the fetus and the risk of cephalo-pelvic disproportion during delivery (Wood 1979; Ferro-Luzzi 1980; Harris 1985). The disruption of this nutritional pattern by industrialization or emigration may be partly responsible for changes in the incidence of schizophrenia.

Immigration. Patterns of occurrence of schizophrenia in immigrants provide a test of the theory that obstetric complications arising from social change affect schizophrenia rates. Immigrants to the industrial world have a higher incidence of schizophrenia than native-born citizens (Warner and de Girolamo 1995). Frequently cited explanations include a selective tendency for individuals to immigrate who are constitutionally predisposed to develop schizophrenia; and the stress of migration or of living in an alien culture, which increases the risk of developing the illness (Leff 1988; Warner and de Girolamo 1995). Other possible explanations are that immigrants entering the developed world encounter a change of immunity or a risk of infection by novel viruses (Wing 1989) or, as argued above, greater obstetric difficulties (owing, in part, to changes in maternal nutrition), which, coupled with better perinatal care, result in the survival of increased numbers of affected offspring.

If the last explanation is accurate,

  1. The frequency of schizophrenia will be elevated more in immigrants from countries where nutrition is less adequate than in the new country.
  2. The incidence of schizophrenia will be greater in immigrants than in the population of their country of origin.
  3. The rate of both obstetric complications and perinatal survival will be elevated among immigrants.
  4. The incidence of schizophrenia will be greater in second-generation immigrants than the first-generation.

Migration to improved conditions. There is substantial evidence that immigrants from poor countries to rich show high rates of schizophrenia. In the United States and Canada in the first half of the 20th century, successive waves of poor migrants -- Greeks, Poles, Irish, Russians, and Swedes -- many of whom were escaping privation, exhibited first-admission rates for schizophrenia that were considerably higher than those of the general population (Malzberg 1969). Refugees entering Norway were 10 times more likely than the native population to suffer from psychosis (Eitinger 1959). A succession of studies has demonstrated that the Afro-Caribbean and (to a lesser extent) Asian immigrant rate of schizophrenia is substantially elevated in Britain (Hems) 1967; Bagley 1971; Cochrane 1977; Rwegellera 1977; Carpenter and Brockington 1980; Bebbington et al. 1981; Dean et al. 1981; Cochrane and Bal 1987; McGovern and Cope 1987; Harrison et al. 1988; Glover 1989; Wessely et al. 1991; Thomas et al. 1993).

Reports of immigrant groups from more affluent countries stand in contrast. British immigrants to Victoria, Australia, in 1959 60, for example, demonstrated an incidence of treated schizophrenia that was similar to the native-born rate but was only a quarter of the incidence found among immigrants from southern and eastern Europe (Cede and Krupinski 1962). European Jews settling in Israel in the 1950s had a lower incidence of schizophrenia than Jewish immigrants from the Middle East (Halevi 1963). American-born residents of England and Wales experienced rates of hospitalization for schizophrenia in 1971 that were lower than those for most other immigrants and close to those for native-born residents (Cochrane 1977). English-born immigrants to New York State in 1949-51 exhibited a strikingly lower first-admission rate for schizophrenia than immigrants from other nations or native-born, white Americans (Malzberg 1969). Immigrants were not over-represented in a Canadian schizophrenia sample unless they were coming from Eastern Europe and entering a disadvantaged minority population (Bland and Orn 1981). Thus, the occurrence of schizophrenia among immigrants from countries with similar nutritional and health care standards does not appear to be elevated.

Greater incidence than in country of origin. Several studies indicate that the elevated incidence of schizophrenia among immigrants from poor countries is greater than that among the population of the immigrants' countries of origin. Arieti (1974) reports that, in 1949, the treated incidence rate among Italian immigrants to New York was three times greater than the highest incidence in Italy. 0degard (1932) found that treated schizophrenia among Norwegian immigrants to Minnesota before the 1930s was twice as common a that among native-born Americans or the general population of Norway. The incidence of schizophrenia in Jamaica appears to be substantially lower than that among Afro-Caribbeans in Britain (Royes 1962; Burke 1974). On the other hand, immigrants to London from Ireland, where nutrition is not substantially worse, do not show an increased prevalence of illness when compared to the Irish who remain in Eire (Clare 1974; Walsh et al. 1980).

Elevated obstetric complications and perinatal survival rates. The risk of obstetric complications in immigrant women from poor countries may be greater than that in the general population because of (1) cephalo-pelvic disproportion secondary to the move from poverty in the home country to relative affluence, and (2) social disadvantage relative to the majority population in the host country. Afro-Caribbean and Asian women in England and Wales are more likely to die from complications of childbirth than are women in the general population (Adelstein and Marmot 1989). Asian-born women in Bradford, England, are shorter in stature, receive less prenatal care, and suffer more complications of pregnancy than British-born women (Lumb et al. 1981); and Afro-Caribbean babies are two or three times more likely than European infants to have a very low birthweight (indicating possible obstetric complications) (Terry et al. 1987; Griffiths et al. 1989).

The infants of immigrants, nevertheless, have high rates of survival. The children of black women in a British study did not have higher perinatal mortality rates than those born to white mothers although the black mothers experienced more obstetric complications and required more emergency cesarean sections (Tuck et al. 1983). Although perinatal mortality in the Carribbean is about five times greater than that in Britain (World Health Organization 1968), perinatal death rates are no higher for the Afro-Caribbean infants in Britain than for European babies (Terry et al. 1980). As with black low-birthweight infants in the United States, neonatal survival for Afro-Caribbean low-birthweight infants in the United Kingdom is higher than that for white low-birthweight infants (Terry et al. 1987; Griffiths et al. 1989).

Greater incidence in second-generation immigrants. An increase in obstetric complications and infant survival in immigrant women would produce an elevation in schizophrenia rates among second-generation immigrants but would not contribute to the rate among first-generation immigrants. A number of recent studies have shown that second-generation Afro-Caribbean immigrants to Britain have higher rates of schizophrenia than Afro-Caribbean immigrants who were born in the West Indies. Harrison and coworkers (1988) demonstrated the incidence of schizophrenia among this ethnic population in Nottingham to be at least six times greater than that among the indigenous population and found the large majority of cases to be second generation. A study in Birmingham showed the schizophrenia rate to be substantially greater in British-born Afro-Caribbeans than among first-generation immigrants or non-Caribbeans (McGovern and Cope 1987), and a study in south London (Wessely et al. 1991) confirms that the risk of schizophrenia is substantially greater in second-generation Afro-Caribbean immigrants. Thomas and colleagues (1993) established that the rate of first admission for schizophrenia among young second-generation Afro-Caribbeans in Manchester is nine times greater than that among Europeans, but that the first-admission rate for mental disorder among the same age group of first-generation Afro-Caribbeans is a quarter of the rate among the native British population. The higher rate of schizophrenia in second-generation immigrants undermines the argument that there is a selective tendency for individuals who are predisposed to develop schizophrenia to immigrate, but it does not eliminate the possibility that carriers of an unexpressed gene for schizophrenia may be more likely to become migrants.

Infection and Immunity. It has been argued that the higher rate of schizophrenia among second-generation immigrants may be due to maternal exposure to novel viruses during pregnancy (Wing 1989; Harrison 1990; Eagles 1991b). A similar explanation is advanced for the rising incidence of schizophrenia during the industrial revolution (Hare 1983) and for the elevated rates of infantile autism (Gillberg et al. 1987; Wing 1989) and multiple sclerosis (Elian and Dean 1987; Stevens 1988; Harrison 1990) in immigrant groups. It is doubtful, however, that immigrants often encounter a novel virus. Are the Caribbean islands, for example, so isolated that the population is protected from the viruses that affect the British population? The rapid global spread of acquired immunodeficiency syndrome (a relatively difficult disease to communicate) suggests that there are few national barriers to contagion.

It is questionable, moreover, that exposure to viral infection is sufficient to account for the scale of variation in schizophrenia rates reported in this article. Current theories of viral influence on the incidence of schizophrenia based on seasonal variation in the birthdate of people with schizophrenia ascribe no more weight to this factor, at the most liberal extreme, than a 10-percent increase in frequency (Eaton 1991). Sham and associates (1992) estimate that no more than 1 to 2 percent of schizophrenia births in England are attributable to influenza, and Adams and coworkers (1993) concluded in a recent three-nation study that "only a small fraction in the variance in the 'incidence' of schizophrenia is explained by exposure to maternal influenza" (p. 533). A history of obstetric complications, on the other hand, occurred in a third to more than a half of schizophrenia patients in recent studies (Eagles et al. 1990; O'Callaghan et al. 1992; Gunther-Genta et al. 1994).

Changes in immunity or in the timing of exposure to infection, however, might produce some of the observed pattern of occurrence of schizophrenia. Changes in hygiene have produced alterations in the general population's immunity to various infectious agents. Poliomyelitis is an example of an illness whose prevalence increased with industrialization as a result of changes in hygiene (see figure 3): improvements in sanitation delayed exposure to the poliovirus until later in life, when the central nervous system is more vulnerable to its effects (Barker 1989). A similar delay in exposure to enteric infection with advances in hygiene explains the 20th-century rise in acute appendicitis (see figure 3): continued improvements in sanitation led to further delay in exposure and to the eventual fall in the incidence of the illness (Barker et al. 1988). Similar changes in the timing of exposure to an infection agent to coincide with a window of vulnerability might account for an increase in schizophrenia accompanying industrial development and affecting different classes in sequence. It is not likely, however that this process would explain an increase in schizophrenia in second-generation immigrants since the children of immigrants and the children of the native population are unlikely to encounter grossly dissimilar sanitation conditions.

Social Stress. Some have suggested that social stress increases the risk of immigrants developing schizophrenia (Warner 1985; Leff 1988), a hypothesis that is supported by the observation, outlined above, that only immigrants from poor countries who enter the lower classes in the host country demonstrate elevated rates of schizophrenia. Do the stresses of urban poverty, menial employment, and unemployment provoke the development of the illness? This hypothesis is now open to doubt, as we would not expect the stresses of migration to be greater on second-generation migrants than on those of the first generation. Another reasonable objection is that, although we know that stress can influence the course of schizophrenia (Kavanagh 1992), we cannot easily explain how it can cause the illness. Stress, for example, increases dopamine release and, by exacerbating dopamine supersensitivity, could theoretically exacerbate the symptoms of schizophrenia (Haracz 1982). There is good evidence that stress can trigger the onset of an episode of schizophrenia and influence its timing (Dohrenwend and Egri 1981). However, there is no clear biological mechanism that would allow stress to cause new cases of the illness, and there is little reason to believe that stress will precipitate the illness in someone who would otherwise have stayed healthy.

Conclusion

It is possible that schizophrenia has risen and fallen in incidence over the past two centuries in the industrial world and has switched from being a disease of affluence to one of poverty. The development of industry may affect the rate of occurrence of schizophrenia over time differentially in the social classes by bringing about changes in maternal nutrition, obstetric complications, and perinatal survival. This pattern of occurrence could also be the result of changes in hygiene, which affect the timing of exposure and immunity to infectious agents. The nutritional/obstetric influence, but not the timing of exposure to infection, can also explain the elevated incidence of schizophrenia in second-generation immigrants .

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The Author

Richard Warner, M.B., D.P.M., D.Obst.R.C.O.G., is Medical Director, Mental Health Center of Boulder County, and Associate Professor-Adjunct, University of Colorado, Boulder, CO.


This article, originally from the Schizophrenia Bulletin, is in the public domain and may be reproduced or copied without requesting the author's permission.

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