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Guidelines-based indicators to measure quality ofantenatal carePaola Bollini MD DrPH1 and Katharina Quack-Ltscher MD MPH2

1Researcher of Services for Medical Research, Evolne, Switzerland2Projektleitung of Klinik fr Geburtshilfe, Universittsspital, Zrich, Switzerland

Keywordsantenatal care, evidence-based guidelines,indicators, migrants and ethnic minorities,quality of care, vulnerable groups

CorrespondenceDr. Paola BolliniServices for Medical ResearchforMed1983 EvolneSwitzerlandE-mail: [email protected]

Accepted for publication: 5 February 2013

doi:10.1111/jep.12027

AbstractRationale, aims and objectives No comprehensive measurement of quality of antenatalcare is available. Late booking or low number of checks are often used as surrogate for poorquality, leaving uncertainty on the actual content of the care received. In order to fill thisgap, we have reviewed two sets of clinical guidelines and developed corresponding indi-cators of quality.Method A group of clinicians and methodologists reviewed the National Institute forClinical Excellency Clinical Guidelines on antenatal care, and the list of prenatal careinterventions recommended by the Research and Development Group, both based onevidence of effectiveness of specific interventions. We identified single aspects in threedomains: (1) services utilization; (2) screening; and (3) interventions. For each indicator,we defined: (1) eligibility, that is the characteristics of the women to whom the indicatorapplies; (2) standard, that is the situation when the target is met; and (3) moderators, thatis all conditions which legitimately hamper the fulfilment of the standard.Results We developed four indicators of service utilization, 25 of screening and 17 ofintervention. The respective eligibility, standard and moderators criteria were described foreach indicator. While many indicators could be retrospectively evaluated from medicalcharts, quality of communication with provider, screening for sensible issues and counsel-ling on behaviours to be avoided could only be obtained with a prospective data collection.Conclusions The indicators of quality of antenatal care, complemented by measures ofsocial position, social support and immigrant/ethnic status, allow for a careful descriptionof the gaps in quality of care for specific groups of women.

IntroductionAntenatal care consists of screening and interventions aimed atensuring a harmonious and safe pregnancy development. There isagreement that adequate antenatal care correlates with satisfactoryand safe pregnancy outcomes [1,2]. Although overall antenatalcare in most developed countries is considered to be satisfactory,its quality may vary across groups: disadvantaged women (withlow socio-economic status, single mothers, adolescent mothers),women from minority/ethnic groups, immigrants and illegal resi-dents may experience various degrees of unsatisfactory care [35].Access to care, often considered non-problematic in countries thathave universal coverage, may hide specific barriers for the mostvulnerable groups. Some studies have highlighted late testing forcongenital malformations [6], non-execution of important tests [7],and inadequate communication with doctors and midwifes [811].

Usually, time of first visit and low number of antenatal checksare considered as satisfactory descriptors of the care received[4,5,12]. Late booking and few or no visits are proxies to inappro-priate care: they may indicate that necessary tests and interven-tions could not be performed, including screening for foetalconditions that may require treatment or warrant reproductivechoice. However, the actual content of antenatal care is seldomanalysed [13,14], not only in terms of tests and medical interven-tions performed, but also concerning the quality of the exchangebetween women and health care providers. To fill this gap, we havedeveloped a set of quality indicators of antenatal care, with refer-ence to clinical guidelines by the National Institute for ClinicalExcellency (NICE) in the UK [2] and to the summary provided theResearch and Development (RAND) group in the USA [15,16].Both sources are based on evidence of the effectiveness of screen-ing and interventions on pregnancy outcome, as well as on expert

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clinical judgment. This paper presents the list of quality indicatorsthat we have developed, together with the information necessary totheir measurement.

MethodsWe have developed a set of quality indicators on the basis of theNICE Clinical Guidelines [2], and on the list of prenatal careinterventions recommended by the RAND Group [16]. The twosources represent the best summaries of antenatal care based onevidence, as developed in the UK and the USA.

We have identified from both sources single relevant items ofantenatal care, either involving utilization of care, screening orinterventions. For each item, we have defined three quantities: (1)eligibility, that is the characteristics of the women to whom theindicator applies; (2) standard, that is the situation when the appro-priate target, either concerning timing of visit, screening or treat-ment, is met; and (3) moderators, that is all possible conditionswhich legitimately hamper the fulfilment of the standard.

As an example, both the NICE Guidelines and the RAND rec-ommendation (number 15) prescribe screening for HIV. Accord-ingly, we have defined the following quantities for the indicatorScreening for HIV:1 Eligibility applies to all pregnant women, at their first antenatalvisit;2 Standard is met when screening for HIV is performed; and3 Moderator is present when womans positivity to HIV status isalready known, or when she refuses the test.

The indicators developed have been discussed and reviewed bya group of gynaecologists of two large teaching hospitals in Swit-zerland. The discussion has allowed not only a more precise defi-nition of the indicators, but also their adaptation to the Swisshealth care context. For example, while the cut-off for Downssyndrome screen positivity recommended by the NICE Guidelinesis >1/250, the nationally agreed cut-off in Switzerland is >1/300 attime of testing; we adopted the latter to define screen positivity.Finally, we have added to the list three additional indicators basedon clinical consensus: screening for violence, counselling forwomen exposed to it, and screening for Streptococcus B. Exposureto violence has been recorded in a previous study on undocu-mented migrant women [7], and represents an important aspect ofcare according to local clinicians. Also, screening for Streptococ-cus B, although not recommended by NICE because evidence ofits clinical and cost-effectiveness remains uncertain, was consid-ered important by local clinicians.

We have developed a data collection form, containing all itemsnecessary to operationalize the indicators. In order to test thefeasibility of data collection, we have checked the possibility ofextracting all necessary information retrospectively from medicalcharts of 20 women who were followed at the Zurich MaternityHospital, and contrasted it with a prospective data collection on 20cases seen at the antenatal care clinic. Comparing the two methods,retrospective from hospital charts and prospective with data col-lected at the moment of the visit, we were able to appreciate thecontribution of different approaches to quality measurement.

ResultsOverall, we developed 46 indicators (Table 1), grouped in threecategories: (1) services utilization (N = 4); (2) screening

(N = 25); and (3) intervention (N = 17). Service utilizations indi-cators include the time of booking, as well as timing of subse-quent controls and communication with providers. Screeningindicators included all tests, clinical examinations, and inquirieson lifestyle and behaviours that have been shown to correlatewith good clinical outcome, or that are considered part of goodpractice by clinical consensus. Indicators of intervention includedboth treatment and advice concerning conditions revealed byscreening (such as hypertension and smoking) or concerning con-ditions present without any prerequisite (such as nutrition andwork during pregnancy). Counselling for reproductive choice incase of selected genetic diseases affecting the baby was also con-sidered to be part of indicators of intervention. Most indicatorscome from both sources of evidence, NICE Guidelines andRAND recommendations.

Tables 2, 3 and 4 describe the operationalization of the indica-tors, that is the data needed to evaluate each specific indicator inthe eligible population, assess whether the criterion was met or, ina number of cases, whether the presence of other circumstancesprevented the achievement of a given standard. It is worth notingthat the data needed to specify eligibility also give a completedescription of pregnancies at risk. Eligibility for indicators ofaccess to care often concerned a specific time of pregnancy, as wellas the presence of communication barriers. Eligibility for indica-tors of screening considered specific timing of pregnancy, but alsothe presence of selected risk factors. Concerning intervention,obviously most eligibility criteria selected women positive toscreening. Finally, for both screening and interventions, modera-tors mostly concerned refusal of test, which may occur albeitinfrequently, and in some cases late booking or subsequent visits,which rendered intervention ineffective (e.g. counselling for repro-ductive choice beyond the possibility to terminate pregnancy, oradministration of folic acid beyond the third trimester).

The last column of Table 1 indicates whether information foreach indicator could be retrieved from medical charts or onlyobtained prospectively. Important indicators such as the quality ofcommunication with provider, information on sensible issues, andcounselling on behaviours to be avoided could be reliably obtainedonly with a prospective data collection at the time of the antenatalvisit. In contrast, indicators of screening and intervention could bereconstructed from antenatal clinical records. All questions of thequestionnaire, including those on sensitive issues, were wellaccepted by the women interviewed.

DiscussionPregnancy is a relatively short and delicate period, during whichscreening, interventions and follow-up should follow a specifictiming. The publication of evidence-based summaries, such theones provided by NICE and by the RAND group, are very usefulbenchmarks against which to evaluate the delivery and acceptanceof antenatal care. Both share a core issue, namely evidence that thechosen approaches correlate with satisfactory pregnancy out-comes, such as birthweight, mortality or womens satisfaction. Inthis sense, the chosen indicators of quality imply content validity.Splitting antenatal care in a number of quality indicators allows fora detailed assessment of the care provided, including its timingand completeness. Surprisingly, no comprehensive instrumentmeasuring quality of antenatal care is available. Very often, time at

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Table 1 Quality indicators for antenatal care: source of evidence and data collection

Quality indicator

Source of evidence

Data collectionNICE2008

RAND Group2006

Clinicalconsensus

Services utilizationTime of first visit X X Chart reviewTime of subsequent visits (nulliparous and uncomplicated;

parous and complicated)X Chart review

Time of subsequent visits (parous and uncomplicated) X Chart reviewGood communication with provider X Prospective data collection

ScreeningRhesus status X X Chart reviewAtypical red cells antibodies X X Chart reviewMother screening for Sickle cell disease X X Chart reviewFather screening if Sickle cell trait X Chart reviewConfirmation of sickle cell disease X X Chart reviewThalassemia X Chart reviewHypertension and pre-eclampsia X X Chart reviewAnaemia X X Chart reviewUltrasound for foetal anomalies X Chart reviewDown syndrome combined test X Chart reviewDown syndrome confirmation X Chart reviewGestational diabetes X X Chart reviewHIV X X Chart reviewHepatitis B (HBsAg) X X Chart reviewRubella susceptibility X X Chart reviewChlamydia X X Chart reviewAsymptomatic bacteriuria X X Chart reviewStreptococcus B X Chart reviewSmoking X X Chart reviewUse of alcohol X X Prospective data collectionUse of recreational drugs X X Prospective data collectionPsychiatric disorders X Chart reviewSyphilis X X Chart reviewAssessing occupation X Prospective data collectionDomestic violence X Prospective data collection

InterventionImmunoprophylaxis for Rh-negative women X X Chart reviewCounselling for reproductive choice X Chart reviewTreatment of hypertension up to 36 weeks X X Chart reviewTreatment of hypertension at 37 weeks (and later) X X Chart reviewIron supplementation X Chart reviewFolic acid supplementation X Chart reviewAdvice concerning occupation X Prospective data collectionCounselling to stop smoking X X Prospective data collectionCounselling to stop alcohol X X Prospective data collectionDietary advice X Prospective data collectionTreatment of gestational diabetes X X Chart reviewAntiretrovirals to prevent HIV transmission to baby X X Chart reviewTreatment of Chlamydia infection X X Chart reviewTreatment of positive urine culture X X Chart reviewCounselling to stop recreational drugs X X Prospective data collectionTreatment of syphilis X X Chart reviewCounselling for domestic violence X Prospective data collection

NICE, National Institute for Clinical Excellency; RAND, Research and Development.

Measuring quality of antenatal care P. Bollini and K. Quack-Ltscher

2013 John Wiley & Sons, Ltd.1062

booking and the number of visits single or in combination approximate quality of antenatal care. However, we do not knowwhether the metric represented by the number of visits, a surrogatefor complete and correct execution of tests and interventions, isreally measuring it [13].

Eligibility criteria define to which women each indicator wouldapply. The two most frequent eligibility criteria were weeks ofpregnancy, which varied according to the type of screening per-formed, and positivity to screening test, which was the prelimi-nary step prior to intervention. At times, as for instance forscreening for gestational diabetes or chlamydia, positivity to oneor more risk factors was considered as eligibility criterion forscreening. For moderators, we have allowed for womens refusalof tests, which may occur on different grounds, as well as latecare, which could explain why certain interventions, such asadministration of folic acid or counselling on reproductive choice,were not performed. The latter is a rather delicate issue, which hasbeen explored in other European countries, confirming the lack ofequal opportunities for reproductive choice for native and immi-grant women [6]. It is worth noting that a review of studiesconducted in European countries showed that differences in con-genital malformations between native and immigrant women dis-appeared where active integration policies were implemented,suggesting that attention to the reproductive health of specificvulnerable groups could actually improve screening and counsel-ling for congenital malformations [17].

Quality indicators are essentially developed to improve thequality of clinical care delivered, by identifying aspects requiringchange (in the structure or process of care delivery) for the entirepopulation, or for specific groups [18]. Certainly many indicatorsmay be measured retrospectively from clinical charts, or fromhospital information systems. However, two limitations exist: (1)hospital information systems are rarely conceived to measurequality; and (2) information characterizing the patients is seldomcollected. For the first aspect, as our study in a large universityhospital in Switzerland has confirmed, clinical advice on preven-tive behaviours, possible difficulties in screening for sensitiveproblems, and counselling for reproductive choice cannot be cap-tured with a retrospective data collection based on clinical records.Other studies have confirmed that medical records are a poorvehicle for collecting data on preventive care [19]. In addition, thequality of communication between patient and provider is seldomreported, although both quantitative and qualitative studies indi-cate that it is a central issue for immigrant women [10,11,20].Secondly, measures of vulnerability, such as socio-economic posi-tion, immigrant status and social support, which reveal the mainbarriers possibly hampering access to care and effective uptake ofpreventive measures for specific groups, are partially reported inmedical charts, and can be obtained only with a targeted datacollection [2123]. Accordingly, although it is feasible to retro-spectively define a large number of quality indicators fromclinical charts, for a genuine and complete effort aimed at quality

Table 2 Services utilization: operationalization of quality indicators for antenatal care.

Quality indicator Eligibility Standard Moderators

Time of first visit All pregnant women at theirfirst antenatal visit

First antenatal visit within 10 weeks of pregnancy,US dated

Two-week delay

Time of subsequent visits(nulliparous anduncomplicated; parousand complicated)

First and uncomplicatedpregnancy

Second or subsequentpregnancy, complicated*

2nd visit at 16 weeks of pregnancy3rd visit at 20 weeks4th visit at 25 weeks5th visit at 28 weeks6th visit at 31 weeks7th visit at 34 weeks8th visit at 36 weeks9th visit at 38 weeks10th visit at 40 weeks

Hospitalization in theprevious month

Twoweek delay

Time of subsequentvisits (parous anduncomplicated)

Second or subsequentpregnancy, uncomplicated

2nd visit at 16 weeks of pregnancy3rd visit at 28 weeks4th visit at 34 weeks5th visit at 36 weeks6th visit at 38 weeks7th visit at 41 weeks

Hospitalization in theprevious month

Two-week delay

Good communicationwith provider

All pregnant women Good understanding between woman and obstetrician/midwife, without intermediaries or with a professionalinterpreter, rated by the health professional

Good communication between woman and healthprofessional, rated by the woman

*A list of conditions requiring additional care include previous pregnancies with complications (recurrent miscarriage, preterm births, pre-eclampsia,Hemolysis, Elevated Liver Enzymes, Low Platelets syndrome, eclampsia, uterine surgery, antenatal or postpartum haemorrhage on two occasions,puerperal psychosis, grand multiparity (four or more), stillbirth or neonatal death, SGA or LGA infant, low birthweight baby, macrosomic baby, a babywith congenital abnormality (structural or chromosomal), or the presence of specific conditions (cardiac disease including hypertension, renal disease,endocrine disorders or diabetes requiring insulin, psychiatric disorder treated with medication, haematologic disorders, autoimmune disorders,epilepsy requiring antiepileptic drugs, malignant disease, severe asthma, use of recreational drugs, HIV or HBV infection, obesity or underweight,smoking, age above 40 years, vulnerable women as teenagers or women lacking social support). HBV, hepatitis B virus; LGA, large for gestational age;SGA, small for gestational age.

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Table 3 Screening: operationalization of quality indicators for antenatal care


Rhesus status All pregnant women at their firstantenatal visit

Rhesus status determined

Atypical red cells antibodies All pregnant women at their firstantenatal visit (to be repeated at 28thweek if Rh negative)

Atypical red cells antibodies measured

Mother screening for sicklecell disease

All pregnant women at their firstantenatal visit, ideally within 10 weeks

Screening for sickle cell trait Second or subsequentpregnancy followed inSwitzerland

Father screening if motherwith sickle cell trait

Women with sickle cell trait Partner screened Partner refusal of test orpartner not available

Confirmation of sickle celldisease

Mother and partner with sickle cell trait Sickle cell disease confirmed by chorionicvilli sampling or amniocentesis

Refusal of test

Thalassemia All pregnant women with red blood cellanomalies at their first antenatal visit,ideally within 10 weeks

Screening for thalassemia Refusal of testSecond and subsequent

pregnancies followed inSwitzerland

Hypertension andpre-eclampsia

All pregnant women at every visit Blood pressure measured, urine testedfor proteinuria, clinical symptomschecked

Anaemia All pregnant women at the first visit and28th -30th week

Haemoglobin and ferritin (the latter onlyat booking) are measured

Ultrasound for foetalanomalies

All pregnant women between 20 and 22weeks

Ultrasound testing to screen for fetalanomalies

Refusal of test

Down syndrome combinedtest

All pregnant women, either between 11and 13 weeks+6 days, or between 15and 20 weeks

Combined test is performed (between 11and 13 weeks+6 days)

Triple or quadruple serum test (between15 and 20 weeks)

Refusal of testSchedule of visits not

respected (e.g. late bookingor subsequent visits)

Down syndrome confirmation Women who tested positive, with aprobability >1/300, or >35 years old

Chorionic villi sampling or amniocentesisperformed

Refusal of test

Assessing occupation All pregnant women at their firstantenatal visit

Occupation is assessed for possibleexposure to risk factors

Gestational diabetes Pregnant women at any appointmentwith pre-pregnancy obesity (body massindex > 30 kg m-2), advanced maternalage (>40), prior gestational diabetes,family history of diabetes in firstdegree relatives, prior macrosomicbaby 4.5 kg), South Asian, BlackCaribbean and Middle Easternbackground

A glucose tolerance test is performed Refusal of test

HIV All pregnant women at their firstantenatal visit

Screening for HIV Refusal of HIV testHIV status already known

Hepatitis B (HbsAg) All pregnant women at their firstantenatal visit

Screening for Hepatitis B performed Refusal of test

Rubella susceptibility All pregnant women early in pregnancy Rubella susceptibility screeningperformed

Refusal of testOfficial record of

immunisations performed inSwitzerland available

Chlamydia Pregnant women less than 25 years oldat their first antenatal visit

Screening for Chlamydia infectionperformed

Refusal of test

Asymptomatic bacteriuria All pregnant women, early in pregnancy Screening for asymptomatic bacteriuriaperformed (nitrite or culture)

Streptococcus B All pregnant women at 36 weeks Screening for Streptococcus B performedSmoking All pregnant women at their first

antenatal visitAssessment of past and current smoking

Use of alcohol All pregnant women at their firstantenatal visit

Assessment of past and current use ofalcohol

Use of recreational drugs All pregnant women at their firstantenatal visit

Assessment of past and current use ofrecreational drugs

Psychiatric disorders All pregnant women at their firstantenatal visit

Questions about past or present mentalillness, with special attention todepression, previous or currenttreatment

Syphilis All pregnant women at their firstantenatal visit

Screening test for syphilis performed

Domestic violence All pregnant women at their firstantenatal visit

Risk for domestic violence assessed byspecific questions



improvement ad hoc prospective studies are needed. Furthermore,quality improvement is an incremental process, requiring a pro-gressive adaptation of the system to a given target. In this process,quality indicators are useful tools to monitor progress.

One issue relating to indicators of quality is their transferabilityacross countries. Studying a set of quality indicators for commonconditions in primary care, developed in the USA and in the UKwith the same methodology, it has been shown that 56% of theindicators were identical, while many others appeared to relate todifferences in clinical practice or norms of professional behaviourin the two countries [24]. In contrast, the quality indicators that wehave developed for antenatal care are largely coincident between

the UK and USA, some differences being attributable to the factthat there is a few years gap between the two. Accordingly, theywould probably apply with minimal modifications across high-income countries, and could represent a good basis for intra- andinter-country comparisons. Another relevant issue is whether indi-cators based on evidence from developed countries would apply todeveloping ones. In principle, pregnancy is similar for all women,and the core content should obviously be the same. A preliminaryretrospective study of quality of antenatal care in India, on arandom sample of 5% of women delivering in a rural hospital(Dangoria D, Swarna Late, personal data), has shown that theindicators of quality of antenatal care which we have developed

Table 4 Intervention: operationalization of quality indicators for antenatal care


Immunoprophylaxis forRh-negative women

All pregnant women who tested negativeat the screening for Rh status

Rh-negative women should be offered appropriateantenatal (and postnatal) immunoprophylaxis

Counselling for reproductivechoice

Women whose babies have Downsyndrome, thalassemia, sickle celldisease or other malformationsconfirmed

Counselling on possibility of reproductive choice Confirmation ofdiagnosis too latefor reproductivechoice

Treatment of hypertension/pre-eclampsia up to 36weeks

All pregnant women with systolic BP>140 mmHg at 20 weeks or later, orwith diastolic BP >90, or with a systolicrise >30 mmHg, or diastolic rise>15 mmHg, proteinuria and peripheraloedema

Bed rest and follow-up within 1 week; possibletreatment with antihypertensive drugs

Hospitalization

Treatment of hypertension/pre-eclampsia at 37 weeks(and later)

All pregnant women at 37 weeks andlater with systolic BP >140 mmHg, orwith diastolic BP >90, or with a systolicrise >30 mmHg, or diastolic rise>15 mmHg, proteinuria and peripheraloedema

Hospital referral for labour induction or caesareansection

Iron supplementation All pregnant women with

apply without modifications. However, the list should beenriched with additional indicators, such as tetanus toxoidadministration, administration of multivitamins, and dewormingas part of treatment of severe anaemia, because of the often pre-carious conditions of delivery and the malnutrition of manyexpectant mothers [25,26]. In addition, we found that someuseful, but expensive tests, such as nuchal translucency in thefirst trimester to screen for Down syndrome, were seldom per-formed, because of lack of trained specialists, especially in ruralareas, or inability of patients to pay for the services. A compara-tive study of quality of antenatal care would allow the identifi-cation of specific patterns of perinatal health inequalitiesbetween developed and developing countries.

In summary, the indicators of quality of antenatal care proposedin this paper, based on evidence-based summaries, allow for adetailed description of care provided to pregnant women. Thequality indicators should be complemented by measures of socialposition, social support and immigrant status, which may have adifferent impact on quality of antenatal care. This is particularlyimportant whenever specific barriers, be it economic, linguistic orcultural, may hamper the correct development of prevention andcare, and warrant appropriate remedies.

AcknowledgementsWe wish to thank Manuella Epiney, Beat Zimmermann, Jean-Franois Delaloye, Philippe Wanner and Sandro Pampallona forthoughtful suggestions to the first version of this manuscript.

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