Maternal mortality: An autopsy auditKD Jashnani1, AB Rupani1, RJ Wani2
1 Department of Pathology, T N Medical College and B Y L Nair Ch Hospital, Mumbai Central, Mumbai-400 008, India
2 Department of Gynaecology and Obstetrics, T N Medical College and B Y L Nair Ch Hospital, Mumbai Central, Mumbai-400 008, India
Background: The process of audit standardizes protocols in departments and has long-term benefits. Maternal autopsies though routinely performed, deserve a special attention. Aims: This study was carried out to calculate the maternal mortality ratio (MMR) in a tertiary care hospital and to correlate final cause of death with the clinical diagnosis. An audit of maternal autopsies was carried out to evaluate current practices, identify fallacies and suggest corrective measures to rectify them. Materials and Methods: Eighty-nine autopsies of maternal deaths in the period 2003 to 2007 were studied in detail along with the clinical details. Results: There were 158 maternal deaths and 13940 live births in this five-year period. Maternal mortality rate was found to be very high (1133/ 100000 live births) in our institution with a high number of complicated referral cases (68/89 cases, 76%). Of the 89 autopsies, acute fulminant viral hepatitis was the commonest cause of indirect maternal deaths (37 cases, 41.5%). This was followed by direct causes like pregnancy-induced hypertension (12 cases, 13.4%) and puerperal sepsis (10 cases, 11.2%). Certain fallacies were noted during the audit process. Conclusion: During the audit it was realized that in maternal mortality autopsies, special emphasis should be given to clinicopathologic correlation, microbiological studies, identification of thromboembolic phenomenon and adequate sectioning of relevant organs. We found difficulty in identification of placental bed in the uterus in postpartum autopsies. A systematic approach can help us for better understanding of the pathophysiology of diseases occurring in pregnancy.
Keywords: Audit, maternal autopsy, maternal mortality rate
Of all the rights of women, the greatest is to be a mother' - Lin Yutang.
The last decade has seen many safe motherhood programs being introduced in India for whom maternal death is a "social injustice" or a "health disadvantage". As per the International Statistical Classification of Diseases and Health-related problems (ICD-10) maternal death is defined as a death occurring during pregnancy or within 42 days of childbirth or of an abortion from any cause related to or aggravated by pregnancy or its management but not from accidental or incidental causes.  Deaths occurring between 43 days to one year are termed as late deaths. Maternal deaths are further classified as direct, indirect and fortuitous deaths. , Maternal mortality ratio (MMR) is commonly used as a parameter to assess safe motherhood programs. According to the National Health Policy (2002), MMR in India is around 407 per 100000 live births with Maharashtra being a better performing state with an MMR of 135. , This national average is, however, much higher than that in countries like the United States of America (17), United Kingdom (7), Russia (45), Australia (13) and Poland (10.48). ,,, Countries like Nigeria report an MMR as high as 1,000-2,000.  It is every nation's priority to reduce the MMR further.  Substandard patient care is defined as failure in direct clinical care and other identifiable adverse factors. It also includes an inadequately performed or incompletely recorded autopsy.  Hence, in cases of maternal deaths, autopsies deserve special attention as compared to other autopsies. , With this in mind we thought of conducting an audit of our maternal autopsies to determine the MMR at our hospital, classify causes of death on post-mortem examination and to correlate the final cause of death with the clinical diagnosis. The audit also intended to identify various shortcomings in our current practices and to suggest corrective measures.
The study was conducted at B Y L Nair Ch Hospital, a tertiary care hospital situated in Central Mumbai which serves as a major referral hospital in the city and provides antenatal care as well as inpatient medical care in obstetrics and gynecology. This hospital also manages pregnant patients with infectious diseases, such as viral hepatitis, which are transferred from the nearby Kasturba Hospital for Infectious Diseases. Routinely in our institution, autopsies are performed by resident pathologists under training. In certain postoperative deaths, autopsies are conducted by the senior faculty members along with an obstetrician. As a protocol, Maternal Mortality meetings are held every two months since the last three years, which are attended by the concerned clinicians and pathologists. Preventable deaths are identified and measures to be taken are discussed. A copy of this meeting is also sent to the Ministry of Health and Family welfare.
This was a retrospective study spanning over a period of five years from January 2003 to December 2007. The MMR was calculated as the total number of maternal deaths per 100000 live births. Maternal deaths in which autopsies were conducted were identified from the autopsy records and classified into direct, indirect, fortuitous and late deaths as per ICD-10. Final cause of death after histopathological examination was compared with the clinical diagnosis. For audit purposes, we defined an ideal maternal mortality autopsy as one which included: 1. complete clinical details, 2. complete autopsy, 3. samples for microbiologic studies preserved wherever necessary and 4. sections studied from brain(3), pituitary gland(1), heart(1), lungs(2 to 3), liver(1-2), spleen(1), kidney(1-2), gastrointestinal tract with pancreas(4-5), adrenal(1), uterus(1) and placenta(2-3), wherever available. These are similar to the guidelines on autopsy practices in case of maternal death as suggested by the Royal College of Pathologists (UK).  All the relevant clinical details and other information regarding the number of sections taken and microbiologic studies were obtained from the autopsy notes filled by the prosector during the autopsy. These autopsy records are stored for 15 years in our institute. Gross specimens available were scrutinized. All slides were reviewed by two pathologists (first two authors) for uniformity of reporting. Cases with inter-observer disagreement were re-reviewed and finally a consensus diagnosis was given.
There were 158 maternal deaths and 13940 live births in this period of review. The average MMR for five years was 1133/100000 live births. Eighty-nine (56.32%) of these 158 maternal deaths underwent autopsy. They accounted for 4.65% of the total 1912 medical autopsies performed in this period. Of the autopsy cases, 63 (70%) belonged to the age group of 21-30 years and 73 females (82%), who died during childbirth, were in the third trimester. In 40 (44%) cases it was their first pregnancy. Seventy-three cases (82%) had a hospital stay of less than five days. There were 63 postpartum deaths (70%). The causes of deaths in the 89 autopsies are shown in [Table 1]. When the final cause of death after histopathological examination was compared with the clinical diagnosis, no discrepancy was noted in 81 cases (91%). The eight (9%) discrepant cases where the autopsy helped in coming to the actual diagnosis are shown in [Table 2].
On auditing the maternal autopsies, that is when we compared the current practices with the standard criteria laid down, it was noticed that in most of the referral cases complete clinical details including the antenatal details were not available. A complete autopsy was performed in 87 cases, except two cases where partial autopsy was conducted in cases of spontaneous rupture of uterus and rheumatic heart disease. Amongst the microbiologic workup as a part of postmortem investigations, blood for culture and swabs was collected by the prosector in only 4/16 clinically suspected cases of puerperal sepsis. Though viral hepatitis was the commonest cause of death [Table 1], viral markers were not available in most of the cases. From the 37 cases of hepatitis in our study, serology for hepatitis E virus (HEV) antibodies was performed in 15 cases antemortem, out of which 10 were positive.
When we went through the sectioning pattern of organs in these autopsies, it was found that uterine sections were taken in 78 of 86 cases (90%). However the uterine bed was not included in eight out of 12 cases (66%) of pregnancy-induced hypertension (PIH). In three cases of postpartum hemorrhage (PPH), obstetric hysterectomy was performed to control the bleeding. There were 59 intrauterine fetal deaths (IUFD) also out of which 33 were stillbirths just preceding the maternal death. Amongst the remaining 26 cases, placental sections were taken only in 17 (65%) cases. Ten cases showed normal placenta. Of the remaining seven cases, three were of cerebral malaria showing numerous parasitized red blood cells in the intervillous spaces. Other significant findings were large intraplacental hemorrhage in a case of PIH, acute placentitis in two cases of puerperal sepsis and foci of caseous necrosis in case of disseminated tuberculosis [Figure 1]. The pituitary gland was sectioned in mere 37 (42%) cases. Normal histology was noted in 34 cases; two cases showed infarction, out of which one was a case of intracranial hemorrhage in a hypertensive female and the other was a case of puerperal sepsis in a human immunodeficiency viral infection (HIV)-positive mother. A case of PPH showed numerous microhemorrhages in the anterior pituitary gland. Sections from the gastrointestinal tract, pancreas and adrenal were not really contributory except for one case each; hemorrhagic enteropathy in a case of puerperal sepsis, acute pancreatitis and pheochromocytoma respectively. Spleen sections were helpful in three cases of cerebral malaria.
As the World Health Organization theme (2005) is 'Make every mother and child count', it is important to take appropriate steps in this direction. The Maternal Health Programme which is a component of the RCH II, 2005 (Reproductive and Child Health Programme) aims at reducing MMR to less than 100 by the year 2010 in India. Being a tertiary care center, MMR is higher in our hospital than the national average in view of large number of complicated referral cases received. Low socioeconomic status, absence of emergency obstetric care in peripheral smaller centers, delays in referral of complicated cases and poor utilization of available obstetric facilities are contributory factors. , Hence healthcare providers at peripheral centers should be trained on a regular basis to recognize early signs of obstetric and medical complications and refer cases promptly.
Amongst the various causes of maternal deaths, acute viral hepatitis emerged as the leading cause with 37(41.5%) cases followed by PIH (12 cases, 13.4%) and puerperal sepsis (10 cases, 11.2%). The high incidence of viral hepatitis in the autopsy group is probably due to the fact that this hospital manages pregnant patients of the nearby municipal public hospital for infectious diseases. The Sample Registration System in India (2002) had reported the leading causes of maternal deaths as hemorrhage (29.6%), severe anemia (19.0%), sepsis (16.1%), obstructed labor and ruptured uterus (9.5%), abortions (8.9%) and pre-eclampsia (8.3%).  An analysis from different continents showed that hemorrhage, sepsis, anemia are more common in Asian and African countries; whereas in developed countries, pulmonary thromboembolism, pregnancy-induced hypertensive disorders, complications of anesthesia, abortions and caesarean section and ectopic pregnancy are more prevalent. ,, This could be due to the fact that they have better medical facilities to manage hemorrhage and infections as compared to India. Other important regional differences included HIV causing about 6% of deaths in Africa. , We had one HIV-positive case who had died of sepsis following incomplete spontaneous abortion. Surprisingly, no maternal deaths related to anesthesia were reported in this study. The comparison of the causes of maternal deaths in various studies is shown in [Table 3]. ,,,,,,, It is very clear that there is a high incidence of indirect deaths due to acute viral hepatitis in our study as compared to other studies. Kavatkar et al., reported majority of direct deaths due to toxemia and indirect deaths due to anemia in their autopsy study.  In other studies from India causes like toxemia, hemorrhage and anemia predominated. ,, But most of these were clinical reports and we came across very few autopsy-related studies. ,,,, Our concordance rate between autopsy and clinical diagnosis was 91% which is similar to another study from Lagos where it was 89.57%. 
Clinical audit is accepted as part of quality assurance in health services but is yet to be widely applied in most developing countries. As an effort in this direction, maternal mortality meetings held at our institute identified eight direct deaths (four cases each of PPH and puerperal sepsis) as preventable deaths. In spite of obstetric hysterectomy being performed in three out of these four cases of PPH, the patients succumbed to hemorrhage. Hepatitis E virus infection has a bad prognosis in pregnancy, often leading to fulminant hepatic failure and death in up to 60% of cases.  Hence serology for viral markers should be carried out in every pregnant female presenting with jaundice.
In the United Kingdom, confidential enquiry into maternal deaths is held regularly and is the world's longest running, continuous national system of audit. The motto is to identify substandard patient care and rectify it. It includes a detailed review of the maternal autopsy and emphasizes on the role of a pathologist. , Due to this system their death due to maternal causes has fallen from 4% in 1954 to 0.7% in 1990.  Hence audit of autopsies in maternal deaths is very important. Only if we know the prevalent diseases in pregnancy, steps can be taken to prevent them and further deaths.  Taking this into consideration, we decided to do an audit of our maternal autopsies.
Evaluating clinical details, prior to commencement of the autopsy is necessary for accurate framing of final cause of death. Failure to do so can cause a problem which has been noted by other authors also.  Regular antenatal care is also important in reducing the morbidity and mortality during delivery and this information should also be available in the clinical notes during the autopsy. As pregnancy is a hypercoaguable state, emphasis should be given to the thromboembolic phenomenon and specially looked for, which was not done in many of our autopsies. Considering that we had 53 (59%) cases of infectious diseases in our study, microbiologic workup as a part of postmortem investigations is recommended if it has not been performed antemortem. A similar observation was made in an autopsy study from Mozambique where the rate of infectious diseases was very high and attributed to high incidence of HIV-related infections. 
Sectioning of certain organs like the uterus, placenta and pituitary gland should form an integral part of the maternal autopsy. Sections from the uterus are important to study physiological and pathological changes during pregnancy and have to be specifically taken from the placental bed, especially for conditions like PIH and puerperal sepsis. Trophoblastic invasion of the myometrium as well as vessel wall, thinning of myometrial vessels with evidence of fibrinoid necrosis are the normal physiological changes noted in the placental bed which are not seen in cases of PIH. , Similarly in puerperal sepsis, endometritis usually begins from the placental bed. , But we found identification of the placental bed in a postpartum uterus very difficult. We either had to rely on the antenatal ultrasonography report for the placental site (which was anyway not available in the majority of cases) or serially cut the uterus in the transverse plane to identify gaping vessels in the myometrium and take multiple sections from the endomyometrium [Figure 2]. However, even that was not helpful and only one to two sections showed proper placental bed. Due to severe financial constraints in our setting, taking extra sections is not routinely feasible. It is important to study the placenta in IUFD cases as 11-50% of such deaths are due to placental factors, though it is also a well-known fact that placental changes in the majority of cases are an effect of IUFD.  The pituitary gland also commonly shows physiological and pathological changes in pregnancy. Pituitary gland necrosis/ Sheehan's syndrome is one of the most common causes of hypopituitarism in underdeveloped or developing countries in the postpartum period.  Pituitary gland infarction is also known in HIV-positive individuals, which was noted in the only HIV-positive case we had.  Uterus, placenta and pituitary gland examination in maternal autopsies is informative and can help in a better understanding of the pathophysiology of pregnancy-related diseases. However, this information was lacking in many cases and may be considered as one of the limitations of this study. Hence now we have made a checklist for maternal autopsy (provided at the end of the article) for junior resident pathologists who routinely perform the autopsies. A re-evaluation of maternal autopsies following these corrective actions has to be done to see the impact of these suggestions.
To conclude, MMR is 1133/100000 live births at our hospital, which gets a large number of complicated referral cases (76% of the autopsies). In 9% of cases the autopsy changed the final diagnosis. During maternal mortality autopsies, special emphasis needs to be given to microbiological studies, identification of thromboembolic phenomenon, detailed gross examination and proper sampling of relevant organs.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]