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Hum. Reprod. Advance Access originally published online on August 24, 2006
Human Reproduction 2006 21(12):3132-3136; doi:10.1093/humrep/del289
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© The Author 2006. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Time trends in ectopic pregnancies in a Norwegian county 1970–2004—a population-based study

I.J. Bakken1,3 and F.E. Skjeldestad1,2

1 Department of Epidemiology, SINTEF Health Research and 2 Department of Laboratory Medicine, Children’s and Women’s Health, Norwegian University of Science and Technology, Trondheim, Norway

3 To whom correspondence should be addressed at: Department of Epidemiology, SINTEF Health Research, N-7465 Trondheim, Norway. E-mail: inger.bakken{at}sintef.no


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
BACKGROUND: The study objective was to estimate temporal trends in ectopic pregnancy in a well-defined population. METHODS: We identified patients with ectopic pregnancy in hospital discharge registries in Sør-Trøndelag County, Norway, 1970–2004, and retrieved data from medical records. We calculated age-specific ectopic pregnancy incidence, proportions of patients with first ectopic pregnancy/prior infertility treatment, incidence of ectopic pregnancy by birth cohort and age and ratio of ectopic pregnancy to live births (extrauterine ratio) by age and parity. RESULTS: Age-adjusted ectopic pregnancy incidence rates increased from 4.3 to 16.0 per 10 000 women-years over the period 1970–1974 to 1990–1994 and declined to 8.4 per 10 000 women-years in 2000–2004. Incidences were highest among women aged 25–34 years throughout the study period. We observed decreases in proportions of women with previous ectopic pregnancy and with prior infertility treatment after 1990–1994. Incidence rates were the highest for women born between 1960 and 1964 in all age groups. Extrauterine ratio increased with age and was higher for women with two or more previous births compared with women with none or one prior birth. CONCLUSIONS: The epidemic increase in ectopic pregnancy towards 1990–1994 was followed by a marked decrease.

Key words: ectopic pregnancy/epidemiology/time trends


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
Ectopic pregnancy is a relatively common condition among women of childbearing age and comprises 1–3% of reported pregnancies (Farquhar, 2005Go). Women with ectopic pregnancy are at increased risk of repeat ectopic pregnancy and infertility (Sandvei et al., 1987Go; Skjeldestad et al., 1998Go; Ego et al., 2001Go).

During the 1970s and 1980s, considerable increases in the incidence of ectopic pregnancy were reported from several nations including Norway (Skjeldestad et al., 1997Go; Storeide et al., 1997Go) and the UK (Rajkhowa et al., 2000Go). Ectopic pregnancy rates have been reported to be stable during the 1990s in Australia (Boufous et al., 2001Go; Chen et al., 2005Go) and the UK (Rajkhowa et al., 2000Go). Declining trends in ectopic pregnancy incidence have been reported from Finland (a 12% decrease from 1988 to 1994) (Mäkinen, 2000Go), Sweden (a 21% decrease for women ≥25 years from 1990–1994 to 1997) (Kamwendo et al., 2000Go) and France (a 14% decrease from 1992 to 1997) (Coste et al., 2000Go). An observed decline in ectopic pregnancy relative to the total number of pregnancies during 1985–1995 was attributed to decreases in rates of chlamydial infection in Sweden (Egger et al., 1998Go), but a similar association was not confirmed in an Australian study (Chen et al., 2005Go).

The aim of this study was to study the incidence of ectopic pregnancy within a geographically defined population (Sør-Trøndelag County, Norway) over the period 1970–2004.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 Acknowledgements
 References
 
The study was approved by the Regional Committee for Medical Research Ethics and the Norwegian Data Inspectorate. Authorization for data retrieval from medical records was obtained from the Norwegian Ministry of Health and Social affairs.

Sør-Trøndelag County, Central Norway, has 270 000 inhabitants, with nearly 60% of the population living in the city of Trondheim. We included all cases of ectopic pregnancy 1970–2004 registered at the only two hospitals in the county—the Trondheim University Hospital and the Hospital of Orkdal. The Trondheim University Hospital serves as a regional hospital also for neighbouring counties.

Patients diagnosed with ectopic pregnancy were identified from computerized hospital discharge registries by using the International Classification of Diseases (ICD) 8th Revision code 631 over the period 1970–1978, the ICD 9th Revision code 633 during 1979–1998 and the ICD 10th Revision codes O00.0–O00.9 over the years 1999–2004. No case was treated in an outpatient setting alone. Data on age, residency, pregnancy history, previous infertility treatment, diagnostic methods and findings, date and type of surgery and result of histological examination of removed tissue were retrieved from medical records and transferred to a standardized case report form. In this population, medical record data are a valid and complete source to determine previous infertility treatment because the Trondheim University Hospital is the regional centre for such treatment in Central Norway. Data retrieval started in 1983 and was subsequently updated at 3- to 5-year intervals. The last data retrieval was carried out in March 2005.

We identified 2051 possible ectopic pregnancies. We excluded 67 women not residing in Sør-Trøndelag County and two women >44 years at the time of the diagnosis. We also excluded 100 women for whom the diagnosis was not verified by ultrasound, histology or macroscopic inspection of the tubes. A total of 1883 ectopic pregnancies among 1619 women were included to the study.

Incidence was calculated as the number of ectopic pregnancies relative to the population at risk in 5-year intervals, starting with 1970–1974. Age was categorized into 10-year age groups. Population figures were provided by Statistics Norway.

We calculated the proportions of patients with first versus repeat ectopic pregnancy and the proportion of patients with first ectopic pregnancy and prior infertility treatment or intrauterine device (IUD) use at the time of the diagnosis.

The incidence of first ectopic pregnancy in 10-year age intervals was calculated for the birth cohorts from 1950–1954 to 1975–1979.

The extrauterine ratio was defined as the number of ectopic pregnancies divided by the number of births. The numbers of births by age and parity were provided by the Norwegian Medical Birth Registry.

Confidence intervals (95%) for proportions were calculated by using CIA software (Altman, 2000). We used chi-square tests for linear trend analysis and for proportions for the analysis of differences in incidence in age interval. SPSS for Windows version 12.0 (SPSS, Chicago, IL) was used in all analyses.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 Acknowledgements
 References
 
Age-adjusted ectopic pregnancy incidence rates increased from 4.3 to 16.0 per 10 000 women-years over the period 1970–1974 to 1990–1994 and declined to 8.4 per 10 000 in 2000–2004. The change in trends was the most marked among women aged 25–34 years, for whom incidence rates were the highest throughout the study period (Figure 1).


Figure 1
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  		Figure 1. Incidence of ectopic pregnancy per 10 000 women-years by age. Diamonds represent women aged 15–24 years, squares represent women aged 25–34 years and triangles represent women aged 35–44 years.

 
The proportion of patients with repeat ectopic pregnancy peaked at 20% in 1985–1989 and comprised 12% of all ectopic pregnancies in 2000–2004 (Table I).


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  		Table I. Number of ectopic pregnancies by first/repeat diagnosis and first ectopic pregnancy by prior infertility treatment/contraceptive failure from the use of an intrauterine device (IUD), 1970–2004

 
Among women presenting with their first diagnosis of ectopic pregnancy, 18% had been through prior infertility work-up/treatment in 1970–1974. This proportion peaked at 25% in 1985–1989 and fell thereafter to the same level as in 1970–1974 (18%) (Table I).

Most (97%, 319/330) women with an IUD present at the time of the diagnosis had had no previous ectopic pregnancy. The proportion of women presenting with their first ectopic pregnancy and using an IUD at the time of the diagnosis decreased from 21% in 1985–1989 to 10% in 2000–2004 (Table I).

Table II summarizes the incidence of ectopic pregnancy in 10-year age intervals by birth cohort. Women born during 1960–1964 had a high incidence of ectopic pregnancy, especially in the age interval 25–34 years, compared with other cohorts. By the age of 35, 3.3% of women in this birth cohort had experienced at least one hospitalization due to ectopic pregnancy.


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  		Table II. Number of women in birth cohort, number and incidence of first ectopic pregnancies in 10-year age intervals per 100 women (brackets) by age and birth cohort, 1970–2004

 
Within all time intervals, the extrauterine ratio was the highest for women aged 35–44 years (Figure 2). Age-specific extrauterine ratios increased until 1985–1989 and were stable until 1990–1994. Thereafter, decreasing extrauterine ratios were observed among women aged ≥25, whereas the ratios were constant in the younger age group.


Figure 2
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  		Figure 2. Extrauterine ratio (ectopic pregnancies per 1000 births) by age. Diamonds represent women aged 15–24 years, squares represent women aged 25–34 years and triangles represent women aged 35–44 years.

 
Extrauterine ratios increased strongly within all parity groups during the first part of the study period (Figure 3). Within all time periods, extrauterine ratios were the highest for women with two or more children. For women who were nulliparous at the time of the diagnosis, age-adjusted extrauterine ratio increased 3-fold from 1970–1974 to 1990–1994. From 1990 to 1994, a strong decrease in age-adjusted extrauterine ratio was observed in all parity groups.


Figure 3
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  		Figure 3. Extrauterine ratio (ectopic pregnancies per 1000 births) by parity. Diamonds represent nulliparous women, squares represent women with parity 1 and triangles represent women with parity 2+.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
Acknowledgements
 References
 
Our study shows a strong, sustained declining trend in ectopic pregnancy by all outcome measures from the early 1990s. This population-based study includes all cases of ectopic pregnancy treated at the only two hospitals in a defined geographical area (county) over a period of 35 years.

In Norway, ectopic pregnancy is treated in public hospitals only. Cases are easily identifiable through hospital registries by using the 11-digit personal identifier unique to each Norwegian citizen. The Trondheim University Hospital serves as a regional hospital for neighbouring counties. Treatment of residents from Sør-Trøndelag County for ectopic pregnancy in hospitals located outside the county is very uncommon (one to two cases annually, data from Norwegian Patient Registry). By using data on residency, we were able to restrict our study population to residents of the county. All medical records were reviewed, and only women with a verified diagnosis were included in the study.

In addition to incidence rates by age, this study reports ectopic pregnancy by first or repeat diagnosis, ectopic pregnancy with prior infertility treatment, extrauterine ratios for age- and parity-specific groups and incidence of ectopic pregnancy by birth cohort and age group. Compared with studies only reporting incidence rates and/or extrauterine ratios by age (Hockin et al., 1984Go; Flett et al., 1988Go; Storeide et al., 1997Go; Egger et al., 1998Go; Mäkinen, 2000Go; Rajkhowa et al., 2000Go; Boufous et al., 2001Go; Irvine and Setchell, 2001Go; Chen et al., 2005Go), the present study provides more detailed information and more comprehensive analysis of the epidemiology of ectopic pregnancy.

In concordance with our study, increasing ectopic pregnancy rates from the early 1970s to the late 1980s were reported from several countries including Norway (Storeide et al., 1997Go), England and Wales (Rajkhowa et al., 2000Go), Finland (Mäkinen, 2000Go), Scotland (Flett et al., 1988Go), Sweden (Weström et al., 1981Go; Kamwendo et al., 2000Go) and Canada (Hockin et al., 1984Go). The incidence of ectopic pregnancy has been particularly high in the Scandinavian countries, but recent decreasing trends have been observed in Sweden from the mid-1980s to the mid-1990s (Egger et al., 1998Go; Kamwendo et al., 2000Go) and in Finland from 1988 to 1994 (Mäkinen, 2000Go). Ectopic pregnancy rates reported from a large US-managed care organization during 1997–2000 (Van Den Eeden et al., 2005Go) were similar to our rates.

Our data show that the proportion of patients with repeat ectopic pregnancy was at its highest when the total incidence peaked in the late 1980s. During the 1980s, tubal extirpation became the primary choice for the treatment of ectopic pregnancy, whereas tubal resection was less commonly used. Probably, at least part of the reduction in repeat ectopic pregnancy after the 1980s can be explained by better primary treatment, including the introduction of laparoscopic technique. Only a few patients were medically treated by methotrexate during the study period.

Our data also show that the proportion of patients with a history of infertility treatment at first ectopic pregnancy has been decreasing since 1985–1989. The indications and methods for infertility treatment have changed radically over the study period. From the late 1980s, tubal surgery has been reduced to a minimum, and assisted reproduction is now the primary treatment for women with tubal infertility. At the same time, the volume of infertility treatment has increased strongly (data from the Medical Birth Registry of Norway, not shown). Thus, some of the decrease in the number of ectopic pregnancies from the late 1980s can probably be explained by better treatment options for women with infertility problems.

In 1993, a hormonal IUD was introduced in the Norwegian market. Based on sales and continuation rates, hormonal devices were as often in use as copper-containing devices by the year 2000. The observed 50% reduction in the proportion of patients experiencing a contraceptive failure while using an IUD over the last 10 years may be explained by a decrease in the use of copper-containing devices and a shift towards more use of hormonal devices of higher efficacy. From France, differing trends for ectopic pregnancy following ‘reproductive failure’ (increasing) and ‘contraceptive failure’ (mostly IUD failure, decreasing) have been described (Coste et al., 2004Go). We were however not able to study such trends, because we did not have access to population data on contraception use.

Smoking is considered a major risk factor for ectopic pregnancy (Bouyer et al., 2003Go; Farquhar, 2005Go). In the present study, we did not have data on smoking available. However, throughout the study period, the proportion of daily smokers among Norwegian women aged 16–74 years has been ~30% (The Norwegian Directorate for Health and Social Affairs, 2004Go), and in 1994–1995, 34% of pregnant women had been daily smokers 3 months before the pregnancy (Eriksson et al., 1998Go). Thus, it seems unlikely that changing smoking habits to any degree can explain the marked changes in ectopic pregnancy incidence described in this study.

Genital infections caused by Neisseria gonorrheae and Chlamydia trachomatis are considered as major risk factors for ectopic pregnancy (Pisarska et al., 1998Go). In Sweden, the observed decrease in fertility problems over the period 1983–1993 has been attributed to the eradication of gonorrhoea (Akre et al., 1999Go). However, in our study, ectopic pregnancy increased strongly during the 1970s and 1980s, whereas genital infections caused by N. gonorrheae decreased. In Norway, gonococcal infections were nearly eradicated by the late 1980s when ectopic pregnancy rates were at their highest (Norwegian Institute of Public Health, 2005Go). It seems likely, however, that some of this discrepancy can be explained by a time lag between trends in N. gonorrheae and ectopic pregnancy.

Women born after 1965 have to a low degree been exposed to N. gonorrheae and have also benefited from the extensive opportunistic screening for C. trachomatis that was introduced in Norway in the early 1980s. We observed lower incidence of ectopic pregnancy by age for women born during 1965–1969 and later compared with women born during 1960–1964 and proposed that part of this decrease in incidence may be attributed to the early diagnosis and treatment of chlamydial infections.

The risk of adverse pregnancy outcomes including ectopic pregnancy increases with increasing maternal age (Nybo Andersen et al., 2000Go). Our data showed the increased ratio of ectopic pregnancies to births with age within all time periods. The average age at first birth has been increasing for Norwegian women born after 1950 (data from the Medical birth registry, not shown). It is however difficult to estimate to what degree the increase in maternal age has contributed to the increases in ectopic pregnancy observed during the first two decades of our study period, especially because maternal age has increased further after 1990, when ectopic pregnancy incidence was sharply declining.

Our data showed that the extrauterine ratio for women with two or more prior births (para-2+) was considerably higher than that for women without children or with just one child (para-01). After excluding women who experienced a contraceptive failure while using an IUD from analyses, the parity difference in extrauterine ratio between para-2+ and para-01 women was reduced (data not shown). Thus, part of the parity effect can be explained by differences in contraceptive practice among para-2+ and para-01 women.

In summary, this study shows a strong reduction in ectopic pregnancy from 1990 to 1994 and onwards.


   Acknowledgements
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
References
 
The study has been financed with the aid of EXTRA funds from the Norwegian Foundation for Health and Rehabilitation, Oslo, Norway (grant number 2003/2/0250), through the Norwegian Support Organization for Infertility.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Acknowledgements
 References
 
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Chen MY, Fairley CK, Donovan B. (2005) Discordance between trends in chlamydia notifications and hospital admission rates for chlamydia related diseases in New South Wales, Australia. Sex Transm Infect 81:318–322.[Abstract/Free Full Text]

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Submitted on March 6, 2006; resubmitted on May 12, 2006; resubmitted on June 15, 2006; accepted on June 26, 2006.


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