Increasing rates of prenatal testing among Jewish and Arab

women in Israel over one decade

Orly Romano-Zelekha, PHDa, Jenny Ostrovsky MScb, Tamy Shohat, MDa,b

aIsrael Center for Disease Control, Ministry of Health, Israel,

and bDepartment of Epidemiology and Preventive Medicine, Sackler School of

Medicine, Tel Aviv University, Israel.

Running head: Prenatal testing among Israeli Jewish and Arab women

Corresponding author: Orly Romano-Zelekha PHD, Israel Center for

Disease Control Gertner Institute, Sheba Medical Center, Tel Hashomer

52621, Israel. Tel: +972-3-7371500; Fax: +972-3-5349881; E-mail:

orly.romano@moh.health.gov.il

Key Words: amniocentesis, nuchal translucency, fetal ultrasound, Jewish,

Arab, prenatal testing, uptake

Abstract

Background/Aims/Objective: This study compares the use of prenatal tests

offered to pregnant women in Israel as reported in a national survey

conducted by the Israel Center for Disease Control in 2010 to that conducted

in 2001. Methods: Women who were 8-72 hours post-delivery of a live infant

were interviewed in 29 maternity wards in Israel on May 31, 2010. Results:

Of 768 women interviewed, 569 (72.3%) were Jewish and 197 (25.7%) were

Arabs. There was a significant increase in the uptake of nuchal translucency

and early ultrasound level 2 for both Jews and Arabs between 2001 and 2010.

The uptake of the biochemical triple marker test and amniocentesis did not

change. The uptake of nuchal translucency and early ultrasound level 2 was

significantly higher among Jews compared to Arabs (21.5% and 28.0% vs

2.9% and 13.7%, respectively in 2001, and 62.0% and 65.6% vs 30.1%, and

30.9%, respectively in 2010). Amniocentesis uptake among women age 35

and older was 47.6% and 47.5% in 2001 and 2010 in Jews, significantly

higher than among Arabs (18.5% vs 28.5%). The factors associated with

higher uptake of different prenatal tests were being secular, having a higher

income and having supplementary medical insurance for Jews, and having a

supplementary medical insurance and receiving printed information on

prenatal testing for Arabs. Conclusions: Prenatal testing rates rose over the

last decade in both population groups but there are still significant gaps. We

suggest that public funding of additional prenatal tests may increase the

uptake in both population groups.

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Introduction

In 2001, the Israeli Center for Disease Control conducted a national survey to

evaluate the uptake of prenatal testing among pregnant Jewish and Arab

women in Israel [1, 2]. The results of that survey revealed significant

differences between the two population groups. The uptake of amniocentesis,

nuchal translucency, late ultrasound level 2 and carrier screening for fragile X

and cystic fibrosis were significantly lower among Arabs than among Jews [1,

2].

The number of prenatal tests offered to pregnant women is constantly

increasing [3]. The national "health basket" in Israel covers amniocentesis at

no cost for women aged 35 years or older, carrier testing for cystic fibrosis for

all women at childbearing age, Tay Sachs for Jewish women, and familial

dysautonomia for Ashkenazi Jewish women. Biochemical triple marker tests

(TT) are performed at a minimal cost. Other tests such as nuchal

translucency, late ultrasound level 2, and genetic carrier screening for several

recessive diseases and for fragile X are partially covered by the

supplementary medical insurance.

The aims of the present study were to compare the uptake of prenatal testing

from 2001 and 2010 among Jewish and Arab women and to evaluate factors

associated with the uptake of these tests.

Methods

Study design

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A cross- sectional one day survey was conducted on May 31, 2010 in twenty-

nine of thirty maternity wards across Israel. One small hospital did not

participate due to technical problems.

Participants, Recruitments and Procedure

Women who were 8-72 hours post-delivery of a live infant were eligible for

participation and the compliant ones were interviewed on the same day.

Women who had received prenatal care outside of Israel or who had delivered

within 8 hours of the survey were excluded. The interviewers were nurses

from the same maternity wards in which the women delivered and who had

been trained to conduct this type of survey. Women were interviewed in their

mother tongue, Hebrew or Arabic"?. The study was approved by the supreme

ethics committee. Signed informed consent of the participants was obtained

prior to the collection of data.

Measure

Data were collected at face-to-face interviews that were based on a structured

questionnaire. The sociodemographic information accessed included age,

population group (Jewish/Arab), country of birth, place of residency,

educational level, religiousness, parental consanguinity, combined household

income, number of children and the holding of supplementary medical

insurance. Women were questioned about past terminations of pregnancy

due to abnormal prenatal findings and about prenatal testing.

Statistical analysis

The univariate analysis included a t-test for continuous variables and a chi-

squared test for categorical variables. Statistically significant variables in the

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univariate analysis were then included in the multivariate models. The odds

ratios (OR) and the 95% confidence intervals (95%CIs) were derived from

these models, controlling for confounding variables. The type 1 error was 5%.

All statistical analyses were performed using the SAS package (version 9.1,

SAS, Cary, NC).

Results

On the day of the survey 1,067 women were eligible for the study. The study

coordinators approached 996 women and 768 consented to participate

(77.1%). Seventy-one eligible women who were released from the hospital

before the study took place could not be recruited to participate. Among the

study participants, 569 (72.3%) were Jews and 197 (25.7%) Arabs. The

demographic data of the study population are represented in table 1. Jewish

women were significantly older, more educated, with a higher family income,

with fewer children, and more likely to have complementary medical

insurance.

The rates of nuchal translucency and early ultrasound level 2 uptake

increased significantly in both population groups (figure 1). However, in both

surveys the uptake of these tests was significantly higher among Jewish than

Arab women (21.5% and 28.0% vs 2.9% and 13.7%, respectively, in 2001,

and 62.0% and 65.6% vs 30.1% and 30.9%, respectively, in 2010 p<0.001).

The rates of TT were similar for both surveys among the Jewish women.

Significantly more Arab women underwent the TT than Jewish women in both

surveys (76.6% vs 61.5%, respectively in 2001, p<0.001, and 70.3% vs

61.0%, respectively in 2010, p=0.01). Also similar was the amniocentesis

uptake of women aged 35 years and older in 2010 and 2001 (figure 1). These 5

rates were significantly higher among Jews than Arabs (47.6% vs 28.5% in

2010 and 47.5% vs 18.5% in 2001, p<0.001).

An increase in carrier testing for fragile X and cystic fibrosis was observed for

both Jews and Arabs. However, this increase was more significant among

Jews. The corresponding rates for fragile X were 39.4 % among Jews in 2010

compared to 24.8% in 2001 (p<0.001). Among Arabs these rates were 5.6%

in 2010 compared to 1.6% in 2001 (p<0.001). Thirty-eight percent of the

Jewish women were tested for cystic fibrosis in 2010 compared to 19.9% in

2001 (p<0.001). Among Arabs women the rates were 11.7% in 2010 and

1.6% in 2001 (p<0.001) (figure 1).

Triple marker testing

The mean age of Jewish women who took the TT was significantly older than

among those who did not (30.8 ± 5.0 vs. 28.2 ± 5.7, respectively, p<0.001).

More who took the TT reported a total monthly income above $1765 (82.9%

vs. 37.0%, respectively, p<0.001) and more had fewer than 4 children (91.9%

vs. 59.5%, respectively, p<0.001). Religiousness was negatively associated

with uptake of the test: 89% of the secular women underwent TT, as did 88%

of the traditional women, 58.8% of the religious women and only 3.6% of the

ultra-religious women (p<0.001). The group who underwent the test had a

higher rate of previous pregnancy terminations due to abnormal prenatal test

findings in the fetus than did the group who did not undergo the test (8.9% vs.

3.3%, respectively, p=0.01), as well as a higher rate of planned pregnancies

(85.3% vs. 62.4%, respectively, p<0.001) and of first pregnancies (32.5% vs.

17.1%, respectively, p<0.001). In addition, more of those who underwent TT

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received printed information on prenatal testing during the index pregnancy

(76.9% vs. 57.2%, respectively, p<0.001). The multivariate model indicated

that age, monthly income above $1765, religious/ultra-religious observation

and first pregnancy, were significantly associated with TT uptake in the

Jewish group (table 2).

Compared to Arab women who did not take the TT, Arab women who took the

TT more frequently reported a total monthly income above $1765 (23.6% vs.

10.9%, respectively, p=0.07); fewer than 4 children (79.9% vs. 64.8%,

respectively, p<0.001), planned pregnancies (64.2% vs. 40.7%, respectively,

p=0.003), a first pregnancy (32.1% vs. 14.8%, respectively, p=0.02) and

having supplementary medical insurance (74.1% vs 55.6% p=0.01). In

addition, more of them had received printed information on prenatal testing

during the current pregnancy (73.4% vs. 38.9%, respectively, p<0.001).

Religiousness was not associated with TT uptake. The multivariate model

indicated that receiving printed information on prenatal testing during the

current pregnancy and having supplementary medical insurance were

significantly associated with TT uptake (table 3).

Amniocentesis in women aged 35 and above

Compared to Jewish women who did not undergo amniocentesis, a higher

proportion of those who underwent amniocentesis reported a total monthly

income >$1765 (95.2% vs. 45.7%, respectively, p<0.001), planned pregnancy

(87.2% vs. 68.6%, respectively, p=0.03) and having fewer than 4 children

(14.9% vs. 57.7%, respectively, p<0.001). Religious observation was

negatively associated with uptake of the test. None of the ultra-religious

women underwent the test. Seventy-one percent of the secular women took

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the test, 42.0% of the traditional women, 33.3% of the religious women and

none of the ultra-religious women (p<0.001). The multivariate model indicated

that a higher income was a significant factor associated with uptake of

amniocentesis in this group, while being religious was negatively associated

with it (table 2).

Only 10 Arab women (5.1%) underwent amniocentesis and only 4 of them

(28.5% of all women aged 35 and above) were older than 35 years. The

sample was too small to analyze the factors associated with uptake of the test

by age.

Nuchal Translucency

The univariate model revealed a higher mean age for Jewish women who

underwent nuchal translucency than for those who did not (31.3 ± 4.7 vs 28.8

± 5.7, respectively, p<0.001). Compared to women who did not undergo the

test, more of those who underwent the test reported a total monthly income

above $1765 (83.9% vs. 33.0%, p<0.001), having a supplementary medical

insurance (67.7% vs 19.7%, respectively, p<0.001), a previous pregnancy

termination due to abnormal prenatal test findings in the fetus (10.0% vs.

1.5%, p<0.001), planned pregnancy (84.9% vs. 61.4%, respectively,

p<0.001), a first pregnancy (33.5% vs. 15.2%, respectively, p<0.001), having

undergone fertility treatments (11.4% vs. 4.3%, p=0.004) and fewer than 4

children (91.7% vs. 60.2% respectively, p<0.001). In addition, more of them

had received printed information on prenatal testing during the index

pregnancy than did those who did not take nuchal translucency (77.7% vs.

55.7%, respectively, p<0.001). Religiousness was significantly associated with

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low uptake of the test: 91.9% of the secular women, 88.9% of the traditional

women, 62.5% of the religious women and only 1.4% of the ultra-religious

women underwent this test (p<0.001). In the multivariate model older age,

monthly income above $1765, having supplementary medical insurance, first

pregnancy and religiousness were significant factors associated with uptake

of nuchal translucency in the Jewish group (table 2).

Compared to Arab women who did not undergo the test, more of those who

underwent the test reported a total monthly income above $1765 (30.8% vs.

14.7% respectively, p=0.02), having supplementary medical insurance (81.0%

vs. 18.9%, respectively p=0.01), fewer than 4 children (89.7% vs. 71.2%,

respectively p=0.006) and having received printed information on prenatal

testing (81.0% vs. 55.3%, respectively, p<0.001). Religiousness was

significantly associated with low uptake of the test: 52.1% of the secular

women, 30.7% of the traditional women, and 19.3% of the religious women

underwent this test.

In multivariate analysis, having a supplementary medical insurance and

receiving printed information on prenatal testing during the index pregnancy

were significantly associated with uptake of this test (table3).

Early Ultrasound Level 2

Compared to Jewish women who did not undergo this test, the mean age of

Jewish women who did undergo it was older (31.3 ± 4.8 vs 28.6 ± 5.1,

p<0.001). They more frequently reported a total monthly income above $1765

(83.1% vs. 29.4%, p<0.001), holding supplementary medical insurance

(71.2% vs 21.3%, p<0.001) and a previous pregnancy termination due to

abnormal prenatal test findings in the fetus (8.6% vs. 3.2%, p=0.02); more 9

reported planned pregnancy (85.4% vs. 58.2%, respectively, p<0.001), a first

pregnancy (32.5% vs. 15.5%, respectively, p<0.001), and having undergone

fertility treatments (11.6% vs. 3.1%, p<0.001). More of them had received

printed information on prenatal testing during the index pregnancy (77.0% vs.

54.4%, p<0.001) and had fewer than 4 children (88.9% vs. 37.8%,

respectively, p<0.001). Religiousness was significantly associated with low

uptake of the test: 91.8% of the secular women, 94.0% of the traditional

women, and 68.1% of the religious women underwent it compared to only

7.8% of the ultra-religious women (p<0.001). The multivariate model showed

that age, having a total monthly income above $1765, having supplementary

medical insurance, planned pregnancy, having printed information about

prenatal testing, and religiousness were significant factors associated with

uptake of early ultrasound level 2 in this group (table 2).

None of the factors analyzed in the univariate analysis were significant in

determining the uptake of early ultrasound level 2 testing among Arab women.

Discussion

Prenatal testing has gained much public attention and popularity in the Israeli

population in recent years. It is often discussed in the written and the

electronic media (Mordechai Shohat, Director Medical Genetics, Rabin

Medical Center, Israel). The present study compares the uptake of prenatal

tests by Jewish and Arab women in Israel at two points in time (in 2001 and in

2010). For 2001, we reported great differences in the uptake of all prenatal

tests (except TT) between Jews and Arabs. Some of the genetic screening

tests have since been funded by the Israeli Ministry of Health and other

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prenatal tests have been partially subsidized by complementary health

insurance. Therefore, the study during a period of changing health policy of

changes in the uptake of prenatal tests among two population groups residing

in the same country but with different cultures and customs is interesting.

The present study was conducted on the same day in practically all the

maternity wards in Israel. The uptake rates of the TT and amniocentesis did

not change between 2001 and 2010. The TT rates remained high in both

population groups, and were higher among Arab than Jewish women in both

surveys. The rate of amniocentesis among Jewish women 35 years and older

was 47.5% in 2010 and 47.6% in 2001. This non- significant drop in

amniocentesis uptake was observed for secular women in this age group

(82.8% in 2001 and 71.4% in 2010, p=0.3) [2]. This might be related to the

introduction of nuchal translucency and new serum biochemical markers, and

to the fact that amniocentesis is no longer recommended solely on the basis

of a woman’s age. The uptake of amniocentesis among Arab women aged 35

and older (who are eligible for the test free of charge) was only 28.5% in 2010

and 18.5% in 2001 (p=0.7). This is higher than reported for this group in 2005-

2007 (13.5%) [4]. Consistent with this low uptake, the prenatal detection rate

of Down syndrome was only 34.6% in women 35 years and older in 2010-

2011 [5]. The low uptake of amniocentesis in face of a high uptake of TT

suggests that Arab women are ready to undergo non- invasive tests earlier in

pregnancy but not other tests, especially not those done from the fourth

month, since results at that stage will not affect decisions regarding the

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pregnancy. Most Israeli Muslim Arabs have been reported not to be willing to

terminate a pregnancy even in the event of a severely affected fetus [6].

The nuchal translucency rates increased almost 3 fold between 2001 and

2010 among Jews and 10 fold among Arabs. The rates of early ultrasound

level 2 more than doubled among Jews as well as among Arabs. The

increase in the uptake rates of these two tests can be attributed to changes in

the financing practices between 2001 and 2010, with most supplementary

medical insurance plans currently covering the costs.

Screening rates for fragile X and cystic fibrosis increased among both Jews

and Arabs; however, they remained significantly higher among Jews. Cystic

fibrosis screening was offered free of charge since 2008 and fragile X testing

was partially covered by the supplementary insurance at the time of the study.

The Israel Society of Medical Genetics recommends screening for fragile X

and cystic fibrosis for the entire population [7, 8]. Since the prevalence rates

of fragile X and cystic fibrosis are similar among Jews and Arabs in Israel, the

differences in uptake are not due to differences in the frequency of the

disease. In the case of fragile X it could be due to the cost [8].

Religiousness remained significantly associated with low uptake of prenatal

testing after controlling for other covariates in Jews. According to the Jewish

law, termination of pregnancy is forbidden after the first 40 days of gestation;

therefore, termination of a pregnancy because of an abnormal finding is

essentially impossible. As a result, the highest rates of live-born Jewish

children with Down syndrome in Israel are in cities with large ultra-orthodox

representation [9]. The association between uptake of prenatal testing and

religiousness among Jews has been reported in other studies [6,10].

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In the current study, religiousness was significantly associated with low

uptake in Arabs in all the univariate analyses but not in the multivariate

analysis. Other studies have found associations between religiousness and

uptake of prenatal tests among Arabs. Shoham-Vardi [11] reported that the

main reasons for avoiding prenatal diagnosis in the Bedouin population were

opposition to termination of pregnancy because of religious reasons, and

mistrust of the diagnosis of an existing abnormality. Muhsen et al [4] reported

that underutilization of amniocentesis among women aged 35 and older was

significantly associated with age, being religious, perceiving amniocentesis as

a risky procedure, spouse's opposition to termination of pregnancy and not

being employed outside the home. These latter factors were not included in

the present study.

.Receiving printed information on prenatal tests was significantly associated

with higher rates of uptake of early ultrasound level 2 in the Jewish

population, and uptake of more nuchal translucency in the Arab one. This

finding supports an earlier report in which preliminary knowledge about

prenatal testing was associated with increased uptake rates [12]. The authors

of that study found that women who underwent elective amniocentesis were

more knowledgeable about prenatal diagnostics and the risks and probability

of abnormality than those who were referred to but did not undergo medically

indicated amniocentesis.

The printed information about the recommended prenatal tests that is

disseminated mostly by the family healthcare centers appears to have

contributed to growing awareness of the importance of prenatal diagnosis,

especially in the Arab communities; in the current study, 60% of the pregnant

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Arab women reported that they chose to conduct the pregnancy care in the

family care centers. Therefore, it is important to disseminate information on

prenatal tests especially to Arab women at those centers.

Family income was significantly associated with the rates of nuchal

translucency and early ultrasound level 2 among Jews, and having

supplementary medical insurance was a significant factor among Jews and

Arabs. Payment for prenatal care and attaining transportation to the providers

of such care were found to be the most common barriers to prenatal care in

low-income women in a previous study [13]. Economic reasons were also

suggested as an explanation for the low uptake of genetic testing among

Israeli Arabs in another recent study [8]. Given that low income and not

having a supplementary medical insurance are associated with low uptake of

prenatal tests, it is possible that funding assistance will increase the rate of

uptake.

The current study has some limitations. Data for 228 (22.9%) women who

refused to participate is not available. It is possible that those who opposed

prenatal testing were less willing to participate, resulting in selection bias. We

could also not compare women with healthy infants to those with affected

infants, due to the low number of affected infants in the study (12 Jewish

infants and 11 Arab infants). We had no information about previous

malformations in the family. Individuals with such a family history might be

more motivated to undergo prenatal tests. However, we did ask about

previous pregnancy termination due to abnormal findings in the fetus. A one

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day survey, although done across the country, represents women who

delivered at that time. Those who deliver more often, such as the Jewish

religious women, are more likely to be represented in the study than those

with fewer deliveries.

Conclusions

Over the course on one decade, uptake rates of prenatal tests increased

among Jews and Arabs, but significant differences continue to exist between

these two population groups. Given that the provision of written information

and having a supplementary medical insurance are associated with increased

uptake among Arab women, the provision of more detailed explanations and

funding assistance may achieve higher rates. Doctors and nurses who

provide prenatal care services should inform their patients about the

availability of prenatal tests, and support their making suitable decisions,

considering their beliefs and values.

Further research should access more detailed and accurate information about

the reasons for not undergoing prenatal testing, including attitudes towards

termination of pregnancy, trust in the diagnosis and in the health services,

accessibility to health care services, and history of malformations in the

family, in order to plan equitable prenatal genetic services for each population

group.

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