International Journal of Gynecology and Obstetrics 121 (2013) 78–81

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International Journal of Gynecology and Obstetrics

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CLINICAL ARTICLE

Errors in the treatment of hypertensive disorders of pregnancy and their impact onmaternal mortality

John J. Zuleta-Tobón a,b,⁎, Heleodora Pandales-Pérez a, Sandra Sánchez a,Gladis A. Vélez-Álvarez a,b, Jesús A. Velásquez-Penagos b

a Department of Obstetrics and Gynecology, University of Antioquia, Medellín, Colombiab NACER, Sexual and Reproductive Health, University of Antioquia, Medellín, Colombia

⁎ Corresponding author at: Calle 70 nro. 52–72 of. 504050010. Tel.: +57 4 2635600, +57 4 2195400; fax: +5

E-mail address: jjzuleta@une.net.co (J.J. Zuleta-Tobó

0020-7292/$ – see front matter © 2012 International Fedhttp://dx.doi.org/10.1016/j.ijgo.2012.10.031

a b s t r a c t

a r t i c l e i n f o

Article history:

Received 9 July 2012Received in revised form 11 October 2012Accepted 18 December 2012

Keywords:Maternal mortalityPre-eclampsiaSubstandard care

Objective: To describe the patients' characteristics and the factors that contributed to the maternal deaths asso-ciated with hypertensive disorders of pregnancy that occurred in the department of Antioquia, Colombia, from2004 through 2011. Methods: A committee of experts conducted a retrospective descriptive study to analyzethe information obtained from both mandatory reports of health facilities to the Public Health SurveillanceSystem and interviews with family members. Results: From 2004 through 2011, there were 720 170 birthsand 389 maternal deaths in the Department of Antioquia, and 70 of the deaths were due to hypertensivedisorder of pregnancy. The factors that most contributed to the deaths were a lack of emergency adminis-tration of antihypertensive drugs (64.6%); the inadequate administration of antihypertensive drugs

(58.8%); retaining the patient at a health facility ill equipped to treat her appropriately for her clinicalstate (54.7%); untimely referral or inadequate conditions for transfer (50.8%); and an error in classifyingthe severity of the disorder, which prevented appropriate management (49.1%). Conclusion: A substandardquality of care was the determining factor in the deaths of women who presented with hypertensive disordersof pregnancy.© 2012 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction

The incidence of pre-eclampsia varies between 3% and 10% amongpregnant women in high-income countries, and the global number ofmaternal deaths due to pre-eclampsia is estimated to exceed 63 000each year [1]. Pre-eclampsia is the major cause of maternal death inLatin America and the Caribbean, with an incidence of 25.7% [2].

In Colombia, pre-eclampsia was the second-leading cause of ma-ternal deaths in 2010, accounting for 37% of the 416 that occurred[3]. In the department of Antioquia, between 2004 and 2007, theleading cause was obstetric hemorrhage. However, by 2008, owingto a decrease in the number of deaths from hemorrhage, hypertensivedisorder of pregnancy (HDP) became the leading cause, with an inci-dence rate of 27% [4]. Identifying risk factors that could be controlled,and enacting control, may have significantly contributed to the reduc-tion in maternal mortality from hemorrhage in the department ofAntioquia [5]. The success of the intervention later prompted the de-sign and implementation of both an evaluation strategy and a trainingprogram for medical personnel, and resulted in the improved man-agement of this complication [6].

Medellín, Antioquia, Colombia7 4 2191031.n).

eration of Gynecology and Obstetrics.

Maternal death can be associated with inadequate care as well aswith risks of pregnancy and childbirth [7]. The objective of the pres-ent study was to analyze the personal characteristics and the factorsrelated to inadequate care contributing to the deaths of womenwith HDP in the department of Antioquia from 2004 through 2011.In an approach similar to that developed for obstetric hemorrhage,the objective was also to identify critical benchmarks in the manage-ment of women with HDP, develop management criteria for each ofthese benchmarks, and implement training interventions.

2. Materials and methods

A retrospective descriptive study was conducted by an investigat-ing committee of the Department of Antioquia, Colombia. Althoughthe healthcare delivery system of Antioquia comprises 184 facilities,some of the residents of the 126 municipalities can have difficultyaccessing health services. In Antioquia, 98.8% of deliveries are institu-tional, 93.7% of the women have at least 1 prenatal visit, and 84.7%have at least 4 prenatal visits. All institutional births are attendedby physicians.

All maternal deaths with HDP as the underlying cause that oc-curred in the department from 2004 through 2011 were analyzed.Maternal death was defined as in the International Statistical Classi-fication of Diseases and Related Health Problems, 10th Revision [8].

Published by Elsevier Ireland Ltd. All rights reserved.

79J.J. Zuleta-Tobón et al. / International Journal of Gynecology and Obstetrics 121 (2013) 78–81

The cases were collected by reviewing the Population Registry,which contains the mandatory reports from health facilities to thePublic Health Surveillance System, and death certificates for allwomen of childbearing age. The sources of information concerningthe deaths included medical records, interviews with the families,analyses performed at the health facilities and/or by the departmentalepidemiologic surveillance committee, and autopsy reports (whenavailable). Permission for publication was obtained from the RegionalHealth and Social Protection Secretary of Antioquia.

The 3-delays model proposed byMaine et al. [9] was used: delay 1,delay in deciding to seek care; delay 2, delay in reaching a treatmentfacility; and delay 3, delay in receiving adequate treatment at thefacility. There is no official guideline for pre-eclampsia manage-ment in Antioquia, and each facility has its own management pro-tocol; however, the local recommendations for the management ofpre-eclampsia were consistently based on the best available scien-tific evidence [10–12]. The effect of the lack of adherence to therecommendations was graded by consensus.

Prenatal care was defined as receiving at least 1 complete visit.The following information was recorded during family interviews,which were the primary information source: Whether the deceasedwoman had received any treatments from nonmedical persons;whether any financial, administrative, or transportation difficultiesdelayed access to medical care; and whether the woman decided toforgo a consultation owing to a negative perception of healthcare fa-cilities or personnel. A delay in the identification of HDP was definedas the recording of high blood pressure values or premonitory signsor symptoms of HDP in the medical chart without HDP being consid-ered as a diagnosis.

The treatment of the patient was evaluated to determine whether,after initial stabilization, the personnel retained the care of the pa-tient even though her clinical state required treatment at ahigher-complexity medical facility. The referral process was gradedwith respect to timeliness and the necessity for prompt action, themeans of transportation used, and the suitability of such transporta-tion for transferring sick patients.

The physical examinations, interviews, and laboratory tests wereevaluated to determine whether their omission or misinterpretationdelayed decision making or elicited inappropriate treatment.

The non-administration of an antihypertensive agent wasrecorded if an emergency medication was not ordered or administrat-ed when a patient's blood pressure reached or exceeded 160/110 mmHg. An inadequate use of an antihypertensive agent was recorded iflabetalol, nifedipine, hydralazine, or sodium nitroprusside was notused at the proper time or dosage. An absence of magnesium sulfateprophylaxis was recorded if an initial intravenous bolus of 4 to 6 gmagnesium sulfate was not ordered for patients with symptoms ofcortical irritation before the presumptive or confirmed diagnosis ofsevere pre-eclampsia was reached, or if a maintenance dose of 1 to2 g per hour of magnesium sulfate was not ordered for these patientsafter they received the initial bolus. An absence of prophylaxis in thepostpartum was recorded if the administration of the chosen hyper-tensive agent was not continued for at least 24 hours postpartum.The non-administration of an additional intravenous bolus of magne-sium sulfate in patients with eclampsia was also recorded, as was thelack of strict monitoring for signs of toxicity in these patients. The ad-ministration, and frequency of administration, of medications such asα-methyldopa, captopril, and diazepam, which are not recommendedfor use in the management of pre-eclampsia, hypertensive crises, oreclampsia, were also recorded. Finally, the unavailability of a requiredtreatment at a healthcare facility with the appropriate self-declaredlevel of complexity was recorded as a lack of resources.

A database was created using Microsoft Access 2007 (Microsoft,Redmond, WA, USA) and the data were analyzed using SPSS version19 (IBM, Armonk, NY, USA). Maternal age and gestational age arepresented as mean and standard deviation; discrete quantitative

variables are presented as median and interquartile percentiles; andqualitative variables are presented as number and percentage. De-nominators indicate the number of patients known as having hadthe relevant characteristic.

Research information is at the basis of the epidemiologic surveil-lance system of the department, which is supported and financed bythe Regional Health and Social Protection Office. Family membersprovided informed consent before being interviewed, and the healthfacilities provided consent prior to the review of clinical records.

3. Results

According to the national vital statistics system, 707 018 livebirths occurred in Antioquia from January 1, 2004, through December31, 2011 (official data for 2004–2010 and preliminary data for 2011)[4]. Of the 389 maternal deaths that occurred in the same period, 70(18.0%) were due to HDP, making HDP the second-leading cause ofmaternal death after obstetric hemorrhage. The overall maternalmortality ratio in Antioquia was 55.01 per 100 000 live births, andthe ratio for deaths caused by HDP was 9.9 per 100 000 live births.Two patients were excluded from analysis because of insufficient in-formation. Among the 68 remaining patients, the main complicationsassociated with HDP were eclampsia (n=45 [66.1%]); hemolysis, el-evated liver enzyme levels, and low platelet count (HELLP) syndrome(n=39 [57.3%]); cerebrovascular disease (n=34 [50%]); acute kid-ney failure (n=21 [30.9%]); acute pulmonary edema (n=19[28.0%]); hemorrhagic complication (n=13 [19.1%]); and placentalabruption (n=8 [11.8%]). Table 1 presents the characteristics of thestudy population.

Women sought care for the following: premonitory symptoms (n=27 [39.7%]); eclampsia (n=19 [27.9%]); labor (n=9 [13.2%]); andother (n=11 [16.2%]). Two more women (2.9%) were dead on arrival.Eleven of the 63 women (17.5%) for whom information was availablewere hospitalized for hypertension during their pregnancy and thendischarged. The mean±SD gestational age at the onset of symptomswas 34±4.5 weeks, and the median time between the onset of symp-toms and consultation with a physician was 23.5 hours (interquartilerange, 4.8–48.0 hours). The family interviews revealed that the preg-nancy was not intended in 53.7% of cases (the information was missingfor 27 women).

Table 2 describes the factors that contributed to the deathsaccording to the type of delay. Only those the investigating commit-tee considered to have contributed directly to the deaths weretaken into account.

The supplies, materials, or resources that were not available at thefacilities where the patients were treated, and whose lack of availabil-ity contributed to the deaths, included antihypertensive (19.1%) andhemoderivative (4.4%) agents, an intensive care unit or other placeto perform close monitoring (2.9%), computed tomographic imaging(2.9%), and magnesium sulfate (1.5%).

4. Discussion

In Antioquia, deficiencies in quality of care are strong determiningfactors for the death of women who present with HDP. In the presentstudy, two-thirds of the patients who died from HDP presented tohealthcare facilities in a timely manner, but the correct measureswere not applied soon enough to prevent the progression of the con-dition. Some patients who arrived with an advanced stage of HDP didnot receive the care required to stabilize their condition. One studyquantified the reduction in mortality due to hypertensive complica-tions of pregnancy after evidence-based practices were implemented,and reported that the in-hospital mortality of women with severepre-eclampsia or eclampsia could be reduced by more than 84%,even when there was a delay in seeking medical attention [13].

Table 1Characteristics of the study population.a

Characteristicb Value

Age, y (n=68) 29.1±8.8Women with prenatal visits (n=63) 49 (77.8)Median number of prenatal visits 4 (1–5)Median parity 2 (1–4)Multiple gestation 2 (2.9)Relevant medical history

Chronic hypertension (n=63) 17 (27.0)Pre-eclampsia (n=55) 9 (13.2)Diabetes (n=61) 1 (1.6)Autoimmune disease (n=60) 0(0.0)

Area of residence (n=56)Rural residence 29 (42.6)Urban residence 39 (57.4)

Marital status (n=63)Married 17 (27.0)Common union 35 (55.6)Single 10 (15.9)Separated 1 (1.6)

Education level (n=51)None 4 (7.4)Primary, incomplete 7 (13.0)Primary, complete 15 (27.8)Secondary, incomplete 9 (16.7)Secondary, complete 12 (22.2)University or technological 4 (5.9)

Place of death (n=68)Home 4 (5.9)InstitutionPrimary 7 (10.3)Secondary 14 (20.6)Tertiary 39 (57.4)

During transfer 3 (4.4)In a public place 1 (1.5)

Time of death relative to delivery (n=68)Before 17 (25.0)b24 hours postpartum 23 (33.8)2–7 days postpartum 18 (26.5)8–42 days postpartum 10 (14.7)

a Values are given as mean±SD, number (percentage), or median (interquartilerange).

b The indicated number of patients is the number for whom the information wasavailable.

Table 2Factors contributing to maternal deaths associated with HDP, using the 3-delays model.

Contributing factor No. (%)a

Delay 1Negative attitude of the woman toward healthcare services 14/59 (23.7)Initial consultation with a traditional healer 7/62 (11.3)Delay in consulting a physician for economic reasons 6/56 (10.7)

Delay 2Delay in reaching a healthcare facility for an initial consultation 17/59 (28.8)

Delay 3Misdiagnosis

Mistake in classifying HDP 34/64 (49.1)Delay in suspecting HDP 25/61 (41.0)Delay in performing laboratory tests 12/63 (17.6)The laboratory results were not returned 6/52 (11.5)Substandard physical examination 6/62 (9.7)Substandard medical interview 5/57 (8.8)Poor interpretation of laboratory results 4/49 (8.2)

Inadequate clinical monitoringInadequate monitoring of warning signs in the postpartum 5/46 (10.9)Inadequate monitoring of magnesium sulfate administration,with non-detection of magnesium sulfate poisoning

3/46 (6.5)

Incomplete laboratory tests 4/48 (5.9)Postpartum bleeding not quantified 2/48 (4.2)Non-quantification of diuresis 2/61 (3.3)

Treatment failureNon-administration of emergency antihypertensive agents 42/65 (64.6)Administration of inadequate antihypertensive agents 30/51 (58.8)No prophylaxis with magnesium sulfate to prevent eclampsia 17/48 (35.4)Non-administration of magnesium sulfate in patients with eclampsia 14/43 (32.6)Administration of medications not recommended for thetreatment of eclampsia

10/46 (21.7)

Inadequate management of intravenous fluids 12/62 (19.4)Non-admission to an intensive care unit when indicated 11/61 (18.0)Non-administration of blood products when indicated 5/44 (11.4)No prophylaxis withmagnesium sulfate to prevent eclampsia in thepostpartum

3/45 (6.7)

Inadequate decisionRetaining management of a patient when the facility wasinadequate for her clinical state

35/64 (54.7)

Untimely referral 32/63 (50.8)Inadequate decisions after receiving the laboratory results 15/50 (22.1)Discharge before 48 hours 1/22 (4.5)

OtherResources not matching the facility's level of complexity 19/63 (30.2)Substandard teamwork 14/57 (24.6)Inadequate referral conditions 11/47 (23.3)Administrative difficulties that hampered care 7/64 (10.9)

a Denominators indicate the number of patients for whom the information wasavailable or relevant.

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In the present study, some women were not instructed to seek thecare of a physician when warning signs or symptoms presented, andsome of those who consulted a physician did not receive appropriatetreatment—a situation also noted by others [14]. Moreover, becausethere were problems assessing the severity of HDP, the potentialcomplications were probably underestimated. Consequently, avail-able treatment may not have been administered at an opportunetime or at all, or the necessary human and technological resourceswere not available at the facilities reached by the patients. For womenwho consulted a physician at an early stage of the disease, the most in-fluential factors of mortality were omissions and errors in the pharma-cologic management. Studies that have evaluated the implementationof evidence-based practices for the treatment of pre-eclampsia insistthat actions at the primary care level should be directed toward theearly identification, stabilization, and timely referral of women withcomplications or who are at risk for complications [13].

A significant number of women did not receive magnesium sulfatefor the prevention or initial management of eclampsia. A work groupcited by the Program for Appropriate Technology in Health describedthe administration of magnesium sulfate as the most important ac-tion to prevent death from eclampsia [15]. The situation observed inthe present study is common elsewhere as well. A study performedin hospitals in Argentina and Uruguay between 2003 and 2005reported the use of magnesium sulfate in only 33% of women withpre-eclampsia to prevent eclampsia, and in only 58.3% of womenwith eclampsia to treat the condition [16].

Two-thirds of thematernal deaths fromHDPwere considered second-ary to eclampsia and its complications. The frequency of pre-eclampsiahas remained stable in both high-income and low-income countries.However, there have been much larger decreases in the incidence ofeclampsia in the former than in the latter, with the incidence 10-foldlower in high-income countries [1]. Likewise, mortality from pre-eclampsia is 10-fold higher in low-income than in high-income countries[1]. In Antioquia, during the period studied, the maternal mortality ratiofor HDP was lower than it was for Latin American and the Caribbeancombined for 2005, which was 33.4 per 100 000 live births, but wellabove the 1.4 per 100 000 for high-income countries [13].

It is believed that inadequate practices directly contribute to morethan one-third of allmaternal deaths [17]. In a study conducted in Tanza-nia, only 63% of patients with eclampsia received treatment for severehypertension, the patients were poorly monitored during labor, andthey were inadequately prescribed magnesium sulfate and other intra-venous fluids [14]. A multicenter study in Argentine about maternalmortality found that women experienced misdiagnosis, inappropriatetreatment, and delays in referral, and that there was an overall shortageof supplies and skilled personnel [18]. These situations are less severe butnot unknown in high-income countries. The underestimation of clinicalsymptoms by physicians, and the non-administration or insufficient

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administration of required antihypertensive agents and magnesiumsulfate have been reported in the Netherlands [19]. In the Report ofthe Confidential Enquiries into Maternal Deaths in the UK coveringthe 2006 through 2008 period, 20 of the 22 women who died fromHDP had received substandard care [20]. Consistent with the presentstudy, the absence of an adequate antihypertensive treatment wasidentified in that report as the most frequent treatment failure.

Although basic interventions to reduce maternal mortality arewell known, simple to perform, and even profitable, vast segmentsof the world population do not benefit from them, as verified by thefindings of the present study [7]. It is not difficult to determinewhat practices should be observed to reduce maternal mortality dueto pre-eclampsia but the difficulty lies in knowing how to implementthese practices. In 2001, Villar et al. [21] suggested that factorsinfluencing the non-implementation of established measures inlow-income countries included the attitude of the healthcare provid-er, the use of outdated information, the passive transmission ofknowledge, and a loss of interest in updating received knowledge.Grol and Grimshaw [22] noted that sufficient evidence indicatesthat a change in behavior is possible but that such a change would re-quire comprehensive approaches adapted to different scenarios andtarget groups.

The present study has several strengths. First, it transcends the de-scription of features and non-modifiable risk factors [23,24]. More-over, it provides an analysis of the medical care factors that directlycontribute to maternal mortality from HDP, and can be modified atall levels of care. It was recommended that information obtained inthe study of maternal mortality be suited to a purpose [17]. In thepresent case, the obtained information precisely identifies the clinicalaspects that must be prioritized. The second strength of the presentstudy is that it decreases variability in the judgments made by the in-vestigating committee, as the findings concerning clinical historywere compared with recognized evidence-based clinical practiceguidelines. Its third strength is that it includes all the maternal deathsfrom HDP that occurred in an entire department of Colombia over7 years. The extended period enables more reliable conclusions anda greater possibility of extrapolation. It is likely that the knowledgeobtained will also be useful in other regions of Colombia, and proba-bly also in other low-income countries. One limitation is that thestudy does not rely on a baseline number of HDP cases in Antioquiato calculate the incidence and lethality of the condition. Additionally,some subjectivity in the judgments made may persist becausepre-eclampsia is a dynamic disease, and many variations in the careprocess hinder analysis.

In conclusion, because pre-eclampsia cannot be prevented or pre-dicted, it is necessary to rely on trained personnel for the early detec-tion and adequate management of the disease, to have emergencyresources available for conducting initial treatment at all levels ofcare, and to terminate the pregnancy at the right time under safeconditions. One of the steps required for ensuring that the personnelare qualified is to design and implement training and retraining pro-grams based on innovative and practical methodologies.

Acknowledgments

The study was financed by the Secretaría Seccional de Salud yProtección Social de Antioquia.

Conflict of interest

The authors have no conflicts of interest.

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