Abortion legislation, maternal healthcare, fertility, female literacy, sanitation, violence against women and maternal deaths: a natural experiment in 32 Mexican states

Elard Koch; Monique Chireau; Fernando Pliego; Joseph Stanford; Sebastian Haddad; Byron Calhoun; Paula Aracena; Miguel Bravo; Sebastián Gatica; John Thorp

doi:10.1136/bmjopen-2014-006013

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Abortion legislation, maternal healthcare, fertility, female literacy, sanitation, violence against women and maternal deaths: a natural experiment in 32 Mexican states

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Study still dead after resurrection attempt fails
Joyce H Arthur
Published on: 15 March 2016
Methodologically sound, with perhaps an uncomfortable result: authors' reply
Elard Koch
Published on: 15 March 2016
BMJ Open Study on Abortion Mortality in Mexico Is Deeply Flawed
Joyce H Arthur
Published on: 23 November 2015
'False Witnesses' Publish Deeply Flawed Study on Abortion Mortality in Mexico
Joyce Arthur
Published on: 23 November 2015

Published on: 15 March 2016
Study still dead after resurrection attempt fails
- Joyce H Arthur, Executive Director
The August 11 response of Dr. Elard Koch and several co-authors fails to rectify the two major flaws in their study that I exposed in my April 9 rebuttal, and in fact, further confirms those flaws. Their very lengthy response also ignored many of my arguments and repeated many of their disputed points. This reply explains why those two major errors remain fatal to their study's conclusions. I then address the question of anti...
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The August 11 response of Dr. Elard Koch and several co-authors fails to rectify the two major flaws in their study that I exposed in my April 9 rebuttal, and in fact, further confirms those flaws. Their very lengthy response also ignored many of my arguments and repeated many of their disputed points. This reply explains why those two major errors remain fatal to their study's conclusions. I then address the question of anti-abortion bias, which I believe played a key role in the flawed design of the study. To be fair, I also address my own biases. Finally, I deal with several ancillary issues arising from Koch et al.'s response (for those interested to read on).
FATAL FLAWS ARE STILL FATAL
My rebuttal had explained that abortion law was not related to abortion practice in Mexico, and that this invalidates the study's methodology and conclusion. That's because you can't hypothesize a possible effect on abortion mortality based on the existence or absence of various legal exemptions across Mexican states, when those exemptions don't even work. In practice, few Mexican women can access abortions under the legal exemptions. In response, Koch et al. confirmed this flaw by saying: "...between states, legal permissiveness may be the same, but accessibility may differ by multiple unmeasured factors. We do not say nor have we stated that we are using this term as a proxy for greater or less accessibility to pregnancy termination..." But their failure to account for the difference between law and practice IS THE FLAW. Their methodology implicitly assumed that abortion restrictions reflect abortion practice, but since they now concede that's not the case, their conclusion that maternal mortality is unrelated to the presence or absence of certain abortion restrictions is meaningless.
I had shown that it was arbitrary and erroneous to select, in particular, the legal exemption for abortion in cases of genetic or congenital malformation as the criterion for assigning Mexican states to the categories of "more permissive" or "less permissive" abortion legislation, depending on whether the state had that exemption. The rarity of abortion for fetal abnormality makes this variable useless as a proxy, because the miniscule numbers of maternal deaths that may result would be impossible to detect statistically in order to compare states with and without the exemption. The authors' only response is to argue that such abortions may be slightly less rare than I claim, based on the low prevalence of Down???s syndrome at birth in several other countries. But that has nothing to do with Mexico or the fact that abortions for any kind of serious fetal abnormality are in the range of 1% of all abortions in countries where abortion is widely legal. So their error remains, especially since abortions due to fetal abnormality are likely even rarer in Mexico than in western countries because of its restrictive laws, inaccessibility of legal abortion under the exemptions, profound stigma, and physician refusals.
The authors say that exploratory analyses are "valid and valuable tools to avoid an arbitrary categorization." But somehow, that's exactly what they ended up with. The authors confirm their flaw by explaining that they selected the legal exemption for fetal abnormality as the main variable because it was the only one that yielded an association with maternal mortality, as well as the only one where the 32 Mexican states had a roughly equal distribution in terms of whether they had the exemption or not. In other words, the variable was arbitrarily selected on the basis of convenience and because it happened to yield an association that I've already shown is meaningless. (Correlation does not equal causation.) A random association is easy to find if you conduct a fishing expedition for one amongst a host of variables, but one should not then base an entire study on it and draw conclusions from it.
AUTHOR BIAS
Nine out of ten authors of the BMJ Open study had an undisclosed bias because they are signatories to the "Dublin Declaration." (http://www.dublindeclaration.com/signatories/) This document denies the need for legal abortion even to save a woman's life. Notably, the peer review process for their BMJ Open study failed to catch the substantive errors in the study because neither peer reviewer had expertise in the subject matter, and one (R. Lieva) appears to hold the same position as the authors. (http://www.thelancet.com/journals/lancet/article/PIIS0140- 6736%2810%2961251-2/abstract) The study contains repeated citations (over 30) of the authors' own past research on abortion and lists over a dozen references from Koch and various co-authors. The effect is to create a false picture of scientific confusion and conflicting data in the abortion field. This same pattern is repeated in their reply to me, even though several of their studies have been criticised. (Here's a compendium of rebuttals to their work: http://choice-joyce.blogspot.ca/2012/08)) Koch et al. have gone to great lengths (in this and other studies) to try and show that factors such as access to emergency obstetric care have the greatest apparent impact on maternal mortality, not abortion laws. But their focus on maternal deaths, while important, obscures all the other suffering and harms that criminal abortion laws cause to women, including high complication rates from unsafe abortion (about 159,000 women are hospitalized annually in Mexico: http://www.guttmacher.org/pubs/Unintended -Pregnancy-Mexico.html). The implication is that we should accept this human cost as long as good health care systems can save women's lives in the end. Presumably the authors would disagree, and hopefully their implication was unintentional.
Given the overwhelming global and historical evidence of the danger posed to women by criminal abortion laws, (http://www.who.int/reproductivehealth/publications/unsafe_abortion/9789241501118/en/ and http://www.ncbi.nlm.nih.gov/pubmed/1949105 and numerous other sources) any study that concludes that restrictive abortion laws do not contribute to maternal mortality should be treated with suspicion.
But let me turn now to the question of my own biases, since Koch et al. would presumably claim that I'm the one who's biased, as well as unscientific. This is apparent from the authors' near ad hominem treatment of my criticisms, dismissing them as "based largely on personal opinions or speculative assumptions," and "not scientifically based." I'm a writer and pro-choice activist, not a scientist. I do not apologize for my impassioned defense of women's rights and lives. I've been monitoring the anti-choice movement for 25 years and Koch's work for 3 years.
For the record, I did not have "discomfort" with the study's findings, because I recognized the study methodology and conclusions were deeply flawed. However, I did feel offended by the study. I object to its very premise and even that it was published in a reputable scientific journal where it does not belong. Please allow me to explain.
I have a bias in favour of the belief that women deserve equality, human rights, and dignity. I also have a bias against criminalizing life- saving healthcare that only women need. Should such biases, if expressed, lessen my credibility or weaken my arguments? If so, it must be because it's still up for debate whether women deserve human rights and freedoms, including the fundamental right to control their fertility.
ADDENDUM: ANCILLARY ISSUES
Unsafe Abortion as a Contributing Factor to Maternal Mortality: The authors protest my "unsubstantiated and dissociated" suggestion that they are using other contributing factors to maternal mortality as a smokescreen to cover up the effect of unsafe or illegal abortion. Their objection is largely answered by my points above on author bias. Further, I believe the authors are being disingenuous when they say they want to emphasize the other factors that contribute to women suffering and dying in childbirth from preventable causes. Rather, they appear to be primarily concerned with abortion. Their study's title begins with "Abortion legislation" as the key factor. The study objective is: "To test whether there is an association between abortion legislation and maternal mortality outcomes after controlling for other factors thought to influence maternal health." Their press release for the study (http://www.melisainstitute.org/pr-18022015-english.html) opens with: "Laws protecting the unborn and therefore, less permissive in regard to abortion, bear a negative ...connotation, because induced abortion in clandestinity might increase maternal deaths. However, a new study conducted in 32 Mexican states ...challenges this notion..." And most of their other research focuses on abortion.
Of course, many factors contribute to maternal mortality, and many effective ways exist to address it. But as I said in my rebuttal, this range of other factors could swamp the effect of unsafe abortion on maternal mortality rates and make it harder to detect statistically, particularly if a country's mortality rate from unsafe abortion is relatively low compared to other countries. The study methodology the authors employed was almost guaranteed to find no meaningful association anyway, which allowed them to present their foregone conclusion that abortion laws don't affect maternal mortality. Clandestine abortion is still a major cause of maternal mortality in many parts of the world, particularly in Africa and Asia. (http://www.prb.org/pdf11/abortion-facts-and-figures-2011.pdf) It is unusual for developing countries with strict bans on abortion to have relatively low maternal mortality rates. In such countries (like Chile and a handful of others in Latin America), other factors indeed play an important role including widespread use of misoprostol - however, maternal mortality would almost certainly be even lower if abortion was legal, safe, and accessible. Regardless, complications from unsafe abortion remain high throughout Latin America and the Caribbean, with over one million women hospitalized annually - 159,000 in Mexico alone during 2009 (http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3557184/ and http://www.guttmacher.org/pubs/Unintended-Pregnancy-Mexico.html). This demonstrates that restrictive abortion laws continue to pose a great danger to women in Mexico, even if fewer are dying than in the past.
Issues with Vital Statistics for Abortion Deaths: The authors' arguments that Mexico does not have a problem with underreporting or misclassification of abortions and associated mortality are unpersuasive. They put a lot of faith in vital statistics from the Mexican government - their only source - but it's unlikely that government statistics are as robust and accurate as they claim. The authors can only cite their own research as support. I found mentions in several studies (listed below) about the problems of misclassification and underreporting associated with the use of vital statistics when it comes to abortion, even in countries like Mexico that have otherwise high-quality records for maternal mortality.
In settings like Latin America where abortion is mostly illegal and highly stigmatized, women and their families would be more likely to not report or misreport an abortion, and health care personnel would be more likely to misclassify causes of death out of ignorance, fear, or compassion. For example, even with the existence of specific ICD codes for "Abortive Outcomes" (ICD-10 O00 to O08), why should we exclude the possible misclassification of unsafe abortion deaths under the codes for sepsis or hemorrhage in early pregnancy (ICD-10 O20 and O23)?
Vital statistics should not be relied upon alone to determine maternal mortality from unsafe abortion. Reputable studies employ a variety of sources and methods, including studies, hospital data, various types of surveys, and more. For no valid reason, Koch et al. neglect and dismiss these additional methodologies, while their own narrower methodology for estimating abortion incidence has been questioned. (http://www.guttmacher.org/media/resources/response-to-methodology- critique.pdf)
Recent studies on maternal death from unsafe abortion do not support Koch et al's claim that the rate for Mexico is as low as 3% of all maternal mortality. Before looking at these other figures, it's important to understand that studies and official statistics on maternal mortality rates and causes do not always distinguish adequately between deaths from induced abortion and spontaneous abortion (miscarriage), or even other "abortive outcomes" such as ectopic or molar pregnancies and other "unspecified" complications. However, we know that maternal deaths from miscarriage, legal abortion, and molar pregnancy are all very rare, at least in settings with reasonable access to health care. While ectopic pregnancies carry a higher risk of death, they are far less common than abortion or miscarriage. Therefore, the majority of officially-recorded abortion deaths in countries with restrictive laws are plausibly due to unsafe induced abortion, including many coded under other "Abortive Outcomes."
The following studies provide rates of maternal mortality due to abortion in Latin America and/or Mexico. The data for Mexico appear to be sourced from vital statistics only, except for #3, which also cites the WHO Mortality Database (in the study's Appendix).
1. The Schiavon et al. estimate for Mexico was 7% for 2008. (http://www.ncbi.nlm.nih.gov/pubmed/22920626)
2. A May 2014 global analysis by the World Health Organization (WHO) (http://www.thelancet.com/pdfs/journals/langlo/PIIS2214-109X%2814%2970227- X.pdf) provided an estimate of 9.9% for Latin America and the Caribbean. For Mexico, the study shows a rate of almost 8% as denoted on a bar graph in the Appendix (page 36). (http://www.thelancet.com/cms/attachment/2014592567/2036073535/mmc1.pdf)
3. A September 2014 study by IHME, the Institute for Health Metrics and Evaluation, shows in bar graphs an average rate of about 17.5% for Latin America and the Caribbean in 2013 (Figure 6, http://www.thelancet.com/action/showFullTextImages?pii=S0140- 6736%2814%2960696-6), and a rate of about 11% for Mexico (Appendix, page 127: http://www.thelancet.com/cms/attachment/2019762887/2039744952/mmc1.pdf).
Why are these data from Mexico (7%, 8%, and 11%) higher than Koch et al's estimate of 3%? It appears it's because Koch et al. excluded deaths coded under ICD-10 O00, O01, O02, and O08 (respectively: ectopic pregnancy, molar pregnancy, other abnormal products of conception [including missed abortion], and complications following abortion and ectopic and molar pregnancy). Excluding these codes could omit many unsafe abortion deaths that were misreported or misclassified.
GLOBAL RATES: The oft-cited 2008 WHO figure of 13% for global maternal mortality due to unsafe abortion (http://apps.who.int/iris/bitstream/10665/44529/1/9789241501118_eng.pdf) should be retired due to the new WHO analysis (#2 above). That study provides a figure of 7.9% globally for 2003 to 2009, with the reduction due to the use of recent data and improved methods. I would suggest that the reduced figure may also reflect the increased use of safer medical abortion by women in some regions. Using a somewhat different methodology, the IHME study (#3 above) yields an estimate of about 15% global maternal mortality from abortion in 2013 (see Table 2, page 995: http://www.thelancet.com/pdfs/journals/lancet/PIIS0140-6736%2814%2960696- 6.pdf). The variance with the WHO figure of 7.9% is unexplained.
INCIDENCE OF UNSAFE ABORTION: This report: http://www.guttmacher.org/pubs/Unintended-Pregnancy-Mexico.pdf was the source for my figures on the significant number of unsafe abortions and complications in Mexico (over a million abortions a year, and 159,000 hospitalizations). These numbers are higher than the estimates from Koch et al. because the latter are based only on vital statistics data, which is insufficient.
Medical Abortion: The authors state: "It is self-contradictory to say that unsafe abortions have increased substantially over the last decades while observing substantial reductions in deaths from this cause." Unsafe abortions have increased globally in recent years but not substantially (from 19.7 million in 2003 to 21.6 million in 2008). But in Latin America, unsafe abortions DECREASED by a third between 1990 and 2008, and maternal mortality went down 70%. (http://apps.who.int/iris/bitstream/10665/75173/1/WHO_RHR_12.01_eng.pdf) This dramatic reduction in maternal deaths coincides with the widespread availability of medical abortion (using misoprostol) in Latin America over the last two decades. In contrast, maternal mortality from unsafe abortion remains high in regions where misoprostol is not as easily attainable, such as Africa. This suggests that misoprostol plays a significant role in reducing women's deaths.
Several studies and reports also attribute the reduction in maternal deaths in Latin America to the increased use of medical abortion (such as: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3557184/). This method has largely replaced more dangerous traditional methods, although it can still lead to a high rate of mostly non-lethal complications when used without medical supervision.
Koch et al. are unsatisfied however, and want to see an epidemiologic study with evidence that misoprostol decreases unsafe abortion mortality "independently of other major factors such as access to emergency obstetric care." This seems to be an unreasonable expectation given the swamping effect those factors would have on the detection of unsafe abortion mortality, especially if the study plugs in artificially low death rates from abortion.
Conflict of Interest:
None declared
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Conflict of Interest:
None declared.
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Published on: 15 March 2016
Methodologically sound, with perhaps an uncomfortable result: authors' reply
- Elard Koch, Director of Research
- Other Contributors:
  Joseph Stanford, Monique Chireau, Sebastian Haddad, on behalf of the REAL Group
Joyce Arthur, from the Abortion Rights Coalition of Canada, has claimed in a letter that our study, "Abortion legislation, maternal healthcare, fertility, female literacy, sanitation, violence against women, and maternal deaths: a natural experiment in 32 Mexican states," has "fatal flaws." We appreciate the opportunity to respond to the questions and critique raised in the letter and to clarify specific issues. After...
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Joyce Arthur, from the Abortion Rights Coalition of Canada, has claimed in a letter that our study, "Abortion legislation, maternal healthcare, fertility, female literacy, sanitation, violence against women, and maternal deaths: a natural experiment in 32 Mexican states," has "fatal flaws." We appreciate the opportunity to respond to the questions and critique raised in the letter and to clarify specific issues. After carefully reviewing the criticisms by Arthur we believe that her concerns are based largely on personal opinions or speculative assumptions and that she misrepresents important methodological issues. The letter does not in fact document "deep flaws"; rather, it seems to perhaps reflect discomfort with the study's findings. It quotes several Op -Ed pieces published in non-peer reviewed sources, including personal or ad-hoc blogs, which focus on political discussions or personal views on the legal status of abortion. In fact, many of her concerns are about issues not directly germane to the data and the analysis. Below, we give a point-by-point response to Arthur's criticisms.
OVERALL FINDINGS
Arthur asserts that our study "purports to show that Mexican states with more restrictive abortion laws have lower maternal mortality rates than states with more permissive laws." This critique oversimplifies and misconstrues our study conclusion focusing only on simple and purely descriptive differences in maternal mortality according to abortion legislation. In fact, as stated in the conclusions of the abstract and the discussion section of the article (first paragraph), our findings support the null hypothesis, namely that differences in abortion legislation do not correlate ultimately with maternal mortality when the influence of other major factors is accounted for. Further, robust and exhaustive multivariate analyses showed that most of the differences (up to 88%) in maternal mortality were largely explained by other factors such as women's literacy, maternal healthcare, emergency obstetric care, individual-level risk factors, clean water, sanitation, fertility rate and intimate-partner violence against women. These findings suggest that reducing disparities in these factors may facilitate an epidemiological transition towards low maternal mortality rates in developing countries, especially in poorer nations. However, Arthur suggests that our study is using such factors as a "smokescreen" to cover up the effect of unsafe or illegal abortion on maternal mortality. We deeply disagree with this unsubstantiated and dissociated assertion from our paper's discussion and results. We wish to emphasize the importance of addressing these factors that strongly impact women's health in developing nations, who continue suffering and dying in childbirth from preventable causes.
PREVIOUS STUDIES ON MATERNAL MORTALITY IN MEXICO
Arthur refers to a previous study of abortion-related mortality in Mexico conducted by Schiavon et al. from Ipas-Mexico [1] to imply that maternal mortality and abortion-related mortality was grossly underestimated in our study. In an exploratory research on maternal mortality in Mexico,[2] we in fact reanalysed the dataset used by Schiavon et al.[1] In that study, significant overestimation of maternal and abortion-related mortality in the entire Mexican country (up to 35%) was found, mainly due to the consideration of flawed denominators of live births. For example, these authors used indirect estimates of live births as denominator to calculate maternal mortality ratios. Compared with observed live births officially registered in Mexico, these indirect estimates for the period 1990-2010 totalled 46,505,160 while the actual figure of official live births totalled 56,759,478 (the difference is more than10 million live births). It is immediately obvious that using substantially smaller figures of live births as denominator resulted in a significant overestimation of maternal mortality ratios in the study by Schiavon et al.[1] The current study in BMJ Open used vital statistic of corrected live births by residence and occurrence as denominator of mortality ratios in every state (see Tables S2 and S3, Data Supplement 1). Consequently, we are reporting accurate maternal mortality ratios for each state based on the actual official records and not based on indirect estimates of live births; this is a serious deficiency in the study quoted in the letter by Arthur.
RELIABILITY OF MORTALITY DATA
Although the letter criticizes the quality of official statistics in Mexico, we would like to point out that Mexico is a country which has been commended by the WHO as being reliable in terms of completeness of civil registration, integrity of vital records, use of international standards for coding of disease, and maternal death audit [3, 4]. While maternal deaths occur most often in settings with poor or non-existent national vital registration systems, this is not the case for countries such as Mexico [2, 5, 6] Chile [7] and at least other six countries with reliable and virtually complete vital records in the American continent.[4] Accurate Mexican mortality records allowed us to distinguish maternal deaths by place of occurrence and place of residence. For instance, the Federal District showed the highest difference in maternal mortality outcomes for those residing outside versus inside the Federal District (61.9 vs 48.7 for MMR per 100,000 live births, respectively) suggesting that inter-state mobility into the Federal District is associated with an increased risk of maternal death for pregnant women arriving from other states. Although errors such as misreported deaths are still possible, in the case of Mexico, minimal errors are expected since 2002 because of the strengthening of the epidemiological surveillance system in that year, incorporating maternal death audits to identify miscoding and minimising under-reporting.[5] In addition the data allowed us to segregate deaths by different abortive outcomes. For instance, in a 2009 audit of maternal deaths in Mexico during the influenza A H1N1 epidemic, researchers were able to distinguish subcategories of causes of maternal deaths, including complications of spontaneous abortion, induced abortion and unspecified abortion.[6] In other words, the results exposed in the BMJ Open article are based on the best mortality data available for every Mexican state at the present, making unlikely that the differences among states are explained by errors in the death registry.
IDENTIFYING AND SEGREGATING ABORTION-RELATED DEATHS
Arthur asserts that there may be widespread misclassification of maternal deaths suspected to be the result of an illegally induced abortion in Mexico. As reviewed elsewhere,[2, 7] however, this has become much less likely in view of ICD-10 codes for death due to other abortion (O05), unspecified abortion (O06), and failed attempted abortion (O07), especially in countries with adequate civil registration of vital data and active epidemiological surveillance of maternal deaths. Usage of these ICD codes, especially O06, allows safeguarding of both professional and patient confidentiality when physicians suspect a self-provoked abortion or when the primary cause is poorly defined in clinical history.[7] Otherwise, the code O04 is used to classify complications for legal medical abortions.[2]
At present in most of Latin American countries (including Mexico) where maternal mortality audit is routinely performed, physicians are exposed to legal and administrative sanctions if they are found guilty of intentionally distorting or misclassifying actual causes of death.[2, 7] This suggests a higher quality of registry data in these countries.[2, 5] For instance, in a recent 10-year times series study of complete hospital discharges for different abortive outcomes in Chile from 2002 to 2011 using the nine ICD-10 codes,[8] over 70% of these discharges are related to ectopic pregnancy (O00), molar pregnancy and other abnormal products of conception (O01, O02 and O08), and spontaneous abortion (O03). It is a prevalent error to consider codes O00, O01, O02, O03 and O08 to be an estimate of illegal, clandestine, or unsafe abortions, an assumption that would mistakenly inflate the numbers.[1, 8, 9] As highlighted by a recent review of the use of ICD-10 codes for the documentation of abortion- related outcomes,[2] none of these codes is likely to be related frequently to illegal procedures. For example, code O02 is used (among others) to classify an anembryonic pregnancy [10] terminated with curettage, which has become an early diagnosis increasingly frequent in territories exhibiting high rates of echography and surgical obstetrical services.[8] The same may be expected for molar pregnancies and miscarriages in settings with high rates of such services. Therefore, it remains highly speculative to assume that most of hospital discharges from abortive outcomes classified using the codes O00, O01, O02, O03 and O08 reflect complications of unsafe or illegal abortions, and consequently we segregate the specific codes O04, O05, O06 and O07 for the construction of induced abortion mortality ratio (iAMR) in the Mexican study. Arthur did apparently not note this important methodological refinement.
Another matter for concern is the possibility of misreporting or misclassification of deaths from induced abortion as deaths for other causes such as haemorrhage or sepsis. Nevertheless, in Mexico, this seems unlikely because of the maternal mortality audit [5, 6] discussed above and the parallel decreasing trend in maternal mortality overall and due to these causes. For instance, deaths from haemorrhage have decreased by 17% between 2002 (10.6 deaths per 100,000 live births) and 2011 (8.8 per 100,000 live births) and deaths from sepsis have decreased over 25% in the same period (from 3.38 to 2.52 per 100,000 live births). Therefore, the iAMR is a proxy that provides a reasonable method to address the problem of under-reporting of maternal deaths from complications of illegal procedures in countries with reasonably reliable records, such as Mexico.
SEGREGATING MEXICAN STATES BY ABORTION LEGISLATION
Arthur uses the term "data dredging" for the exploratory analyses used to segregate the states in two groups according abortion laws of each state. Our pragmatic approach, completely described in the article, was to assess a spectrum of differences of law across the 32 states summarized in Table 1 of the BMJ Open article, and from these to define an operational binary term for subsequent statistical analysis, meaning 1 = less permissive and 0 = more permissive. Arthur misconstrues the reason for the choice of this term, which makes her criticism of this issue largely misguided. Firstly, this variable is a proxy of legal permissiveness, not an indicator for abortion accessibility. In other words, between states, legal permissiveness may be the same, but accessibility may differ by multiple unmeasured factors. We do not say nor have we stated that we are using this term as a proxy for greater or less accessibility to pregnancy termination in our study. Secondly, as a parsimonious approach, exploratory analyses are valid and valuable tools to avoid an arbitrary categorisation, assessing the initial correlation between a set of categorical variables (in this case, the presence or absence of different types of criminal exemptions for pregnancy terminations in each state) and the primary outcome of interest (i.e., maternal mortality ratio in our study). Thirdly, the single legal characteristic with the greatest discrimination in terms of mortality rates between the states was whether or not there was an exemption for genetic or congenital malformation combined with any other exemption. Finally, this was the criminal exemption that resulted in the most balanced distribution of states in each comparison group: 14 of Mexican states formally allow criminal exemptions in cases of genetic or congenital malformations and 18 states do not allow such exceptions. Other alternative combination of laws were not significantly associated with maternal mortality, supporting the final conclusion of the paper, namely that differences in abortion legislation do not correlate ultimately with maternal mortality in Mexico.
EXEMPTION FOR GENETIC AND CONGENITAL FOETAL CONDITIONS
Similarly, Arthur asserts that the criminal exemption for pregnancy termination in cases of non-lethal conditions such as genetic or congenital foetal anomalies is not a good proxy to study the relationship between abortion legislation and different health outcomes, including maternal mortality. However, there is good evidence from other countries that this particular exemption has a substantial impact on how abortion is utilized, which makes it a likely indicator of both the legal and cultural climate related to abortion. For instance, prenatal screening and more permissive laws of abortion appear to have a strong impact on Down syndrome (trisomy 21), decreasing the prevalence of this condition at birth to less than 1 per 1,000 in Europe [11-14]. Conversely, the prevalence of Down syndrome at birth is higher in settings with less permissive laws: Chile (2.47 per 1,000), Argentina (2.01 per 1,000) and Ireland (2.1 per 1,000 in Dublin) and over 1.7 per 1,000 live births in most other Latin American countries.[8, 13, 14] Thus, it is reasonable to think that the presence or absence of this exemption actually changes some of the utilization of abortion and may reflect the predominance of different cultural factors and attitudes toward abortion in general.
LAWS AS AN INDICATOR OF CULTURAL FACTORS, ATTITUDES AND BEHAVIOURS
Along this line, as we have noted, there is consensus that diversity of abortion legislation in different regions, countries, and territories may partially reflect the predominance of different cultural factors, behaviours, and attitudes in the population towards abortion itself.[15- 23] In our view, Arthur neglects this point. For example, Kilck et al. assessed gonorrhoea incidence rates as a proxy of high-risk sexual behaviour in a panel of 41 countries for which consistent gonorrhoea data were available for a 20-year study period. Compared with less permissive laws allowing abortion only for lethal conditions, the switch to more permissive abortion laws for non-lethal maternal conditions was associated with large increases in reported gonorrhoea incidence.[24] According to the authors, modern economic theory predicts that abortion laws affect sexual behaviour since they change the marginal cost of having high-risk sex (i.e., sexual activity during which barrier contraception is not used, which by definition is associated with higher risk for both STD acquisition and unintended pregnancy). In another study conducted in Spain between 1997 and 2007, Due?as et al. reported that an increasing trend in the use of effective contraceptive methods (49.1% to 79.9%), was paradoxically also associated with an increasing trend in the utilization of pregnancy termination (5.52 to 11.49 per 1,000 women), especially in young women, who reported engaging in high-risk sex more frequently and more precociously.[25] Interestingly, in the Russia Longitudinal Monitoring Survey the availability of abortion was one of the reasons cited for non-use of contraception for the female population.[26] The change in the marginal cost of unprotected or risky sex vis a vis different abortion laws proposed by Klick et al. well may be a plausible mechanism that influences the global efficacy of family planning programs to decrease unintended pregnancies and abortion rates. Altogether, these studies support the need to investigate the relationship between different abortion laws and cultural patterns, attitudes and behaviours that ultimately influence sexual and reproductive health outcomes in different populations. The diversity of abortion laws in Mexico represents a valuable natural laboratory at the population level. Thus, although we did not find an independent association of differences in legal exemptions with maternal mortality, it would be worthwhile for future studies to assess possible associations with other reproductive health outcomes.
OTHER FACTORS IMPACTING MATERNAL MORTALITY
Arthur's letter states that "it's already well established -- practically self-evident-- that maternal mortality can be significantly reduced by educating women, upgrading health systems, and improving access to contraception, skilled birth attendants, clean water, sanitation, and so on". We note that science is not "self-evident" as stated in the letter; our study is consistent with previous research and also adds important original scientific evidence on this subject. Although some previous studies have documented the impact of factors such as women's education level, fertility rate, clean water, sanitation and delivery by skilled attendants, relatively few studies have tested the impact of these variables in a simultaneous fashion, as our study has. In addition, we provide an exhaustive literature review for each factor in the BMJ Open article. We would like to emphasize that simple epidemiologic correlations do not necessarily mean causation. Therefore, we have used multivariate regression models to test the independent contribution of each factor. Furthermore, our study addressed the problem of multicollinearity in providing estimates of unbiased effect sizes for each variable in different panels of multiple regression models (a panel of 24 multivariate regression models, 12 unrefined models and 12 refined models). In the case of Mexico, we detected important disparities among states on different independent predictors, and these disparities appear to explain differences in maternal and abortion-related mortality. Again, we object to Arthur's dismissive statements towards the importance of these positive findings of the study, because addressing these factors could have a major impact to improve the survival and health of women and families worldwide.
On the other hand, the impact of some variables has been scarcely evaluated in the epidemiologic literature. For instance, this is the first study assessing directly the relationship between prevalence of intimate- partner violence against women and maternal mortality rates at the population level in 32 Mexican territories. The Mexican study is also the first study to assess the possible impact of constitutional amendments protecting the unborn on maternal mortality rates. It is noteworthy that the results of the Mexican natural experiment are remarkably consistent with other natural experiment recently conducted in Chile.[7] Arthur's letter fails to provide direct evidence supporting the statement that differences in abortion legislation have a significant association with maternal death rates independent of other factors known to influence maternal mortality at the population level. At present, research on this subject in Mexico and Chile, provisionally supports the null hypothesis, namely that differences in abortion legislation do not correlate ultimately with maternal mortality in these countries when the influence of other major factors is taken into account.
RISK OF COMPLICATIONS FOR LATE-TERM ABORTIONS
Arthur acknowledges that almost all abortion for foetal abnormality occurs later in pregnancy "because the anomaly cannot usually be detected until then". We agree on this point. However, she also claims that the selected exemption for foetal anomaly cannot possibly by itself show any trends or differences in abortion mortality rates "because abortions due to foetal abnormality are always a tiny minority of abortions in any country." This ignores the fact that the risk of complications from second -trimester or late-term abortions is much higher than from terminations conducted during the first trimester. In the classic study by Bartlett et al. "Risk factors for legal induced abortion-related mortality in the United States", the relative risk of abortion-related mortality was 14.7 at 13-15 weeks of gestation, 29.5 at 16-20 weeks, and 76.6 at or after 21 weeks (95% CI 32.5, 180.8). [27] Hence, the small number of late terminations will contribute significantly to related maternal mortality. This has been suggested empirically in a study using hospital discharge data in the U.S. to assess the rates of major abortion complications from 2001 to 2008 and their relationship to more and less permissive abortion legislation in 23 states with reasonably reliable records. After controlling for socio-economic characteristics and the pregnancy complication rate, less permissive laws were associated to lower complication rates (odds ratio of 0.79 for mandatory delays and 0.74 for Medicaid funding restrictions). According to the authors, this result may reflect the fact that states without restrictions perform a higher percentage of late term abortions, including terminations for genetic or congenital foetal diseases.[28]
ILLEGAL USE OF MISOPROSTOL AND ABORTION COMPLICATION RATES
We agree with Arthur that the illegal use of drugs with abortive effects, especially misoprostol, probably has become the most prevalent method to conduct unsafe abortions in Mexico and other countries.[7, 8, 29 -32] However, approximately half of the women that use this drug could experience bleeding and pelvic pain greater than that of a regular menstrual cycle and may consequently seek medical assistance. In addition, the rate of complications and failures can reach 30% or more with the use of self-administered misoprostol when taken in inadequate dosages or after more than nine weeks of gestation.[33, 34] Thus, one might predict that any significant increase in the illegal use of misoprostol at the population level at least would translate into an increase in less severe cases of abortion-related complications in hospital discharges, particularly in code O06 (unspecified abortion). However, to the best of our knowledge, no epidemiologic study has provided evidence that the illicit distribution or illegal use of misoprostol decreases maternal mortality rates from clandestine, illegal, or unsafe abortion, independently of other major factors such as access to emergency obstetric care.
THE IMPORTANCE OF EMERGENCY OBSTETRIC CARE
An independent inverse association between all-abortion hospitalization ratios and maternal mortality ratios was found in our study. The unadjusted coefficient represented a reduction of 1.71 maternal deaths per 100,000 live births for each unit of all-abortion hospitalisation ratio (see Table 6 of the BMJ open article). After full adjustment, for each incremental unit in this variable, a decrease of 0.8 maternal deaths per 100,000 live births was estimated among states (see Table 7). The result was remarkably consistent through different panels of regression models (see Table 8). Mexican states classified as having less permissive abortion legislation exhibited higher all-abortion hospitalisation ratios than more permissive states (see Table 9). This indicator of all-abortion hospitalization ratio serves as proxy for access to opportune or immediate emergency obstetric care in women experiencing complications from any kind of abortion. In other words, we found evidence that improved access to emergency obstetric care is likely a key factor decreasing maternal deaths in women resorting to illegal, clandestine, or unsafe abortions in settings with less permissive abortion laws regardless of the procedures utilised to conduct abortions. Arthur neglects this important finding of our study.
ESTIMATES OF ILLEGAL ABORTIONS IN MEXICO
Arthur makes a number of assertions about the practice of illegal abortion in Mexico and other countries that do not directly relate to the findings of our paper in BMJ Open. We do assume that legislation will have some influence on the practice of abortion (an assumption that we suspect Arthur shares, or there would be no concern about abortion laws). We do not dispute the existence of illegal, clandestine, or unsafe abortion. For the record, we do not advocate imprisoning women who have received illegal abortions, and as this idea is nowhere stated or implied in our paper. We are not making any recommendation in our paper regarding the legal status of abortion at the population level. However, we are interested in the prevention of abortion and its deleterious consequences for women's health. Furthermore, we acknowledge the importance of estimating empirically plausible figures of abortion.
Elsewhere, we have reviewed the methodological problems that produce inconsistent figures of illegal abortions in M?xico and other Latin American countries.[2, 8, 35, 36] For instance, a study conducted in 1990 that was based on opinion surveys with expansion factors reported controversial figures for Chile, suggesting that approximately 160,000 illegal abortions were performed every year in this country.[37] However, a review of the methodology found it lacking reproducibility and subject to selection bias, recall bias, and possibly ideological bias of the interviewed individuals, especially in the calculation of an expansion factor that multiplies the number of discharges by abortion complications surveyed in health institutions.[35] There is no study validating the utilization of expansion factors based on the mere opinion of subjects arbitrarily selected.[36] In contrast, three major global reports have detected important reductions in maternal and abortion-related mortality in Latin American countries.[38-40] It is self-contradictory to say that unsafe abortions have increased substantially over the last decades while observing substantial reductions in deaths from this cause.
Other examples from countries that have modified their abortion legislation also suggest large estimation errors. For example, in the Federal District of Mexico, Juarez et al estimated that more than 194,875 abortions were performed every year before liberalizing changes in legislation.[41] After more than 5 years following the new law allowing first trimester terminations on demand, the number of pregnancy terminations in the public health sector has not reached 20,000 per year.[2] In Mexico, most of the population utilise the public health system,[42] however, even assuming some degree of underreporting for legal abortions in the private sector of the Federal District, the numbers presented by Juarez et al appear to be overestimates. Similarly, in Uruguay, 33,000 illegal abortions per year were estimated pre- legislation,[43] but after the first full year of complete statistics post -legislation allowing first-trimester abortion on demand, the total number of terminations was 6,676.[44] The second year post-legislation, the number of pregnancy terminations increased about 20% (8,500 procedures, an increment from 9 to 12 per 1,000 women at 15-45 years old, according the Ministry of Public Health).
CAUSES OF MATERNAL DEATH IN MEXICO
Arthur claims that an estimated 13% of maternal mortality globally is due to unsafe abortion without providing the source of such estimate. The 2014 global analysis carried out by Say et al. reported an estimated 7.9% of deaths from abortion.[40] The WHO report during 2008 reported an estimated 13%.[45] Previously in 2006, Khan et al. reported 12% for Latin America in a systematic review published by The Lancet.[46] Regardless of these global reports, a detailed analysis in Mexico [2] shows the following proportions for different maternal mortality causes during 2009, in decreasing order: 33.9% for Indirect Obstetric Causes (O98-O99); 21.5% for Hypertension and Eclampsia (O10-O16); 19.9% for Haemorrhage (O20, O43- O46, O67, O72, O73); 13.7% for Other Direct Obstetric Causes (O01-O02, O21, O24-O26, O28-O36, O40-O42, O47-O48, O60-O66, O68-O71, O74-O75, O80); 5.7% for Sepsis (O22, O23, O85-O88); 2.5% for Ectopic Pregnancy (O00); 2.1% for Medical Abortion, Other Abortion, Unspecified Abortion, and Failed Attempted Abortion (O04-O07); and 0.9% for Spontaneous Abortion (O03).[2] According this analysis, nearly 98% of maternal death causes in Mexico are unrelated to pregnancy termination, regardless of whether if it is legal or illegal.[2] Therefore, the global estimate of 13% quoted by Arthur does not apply in the case of Mexico.
ADDITIONAL INCONSISTENCIES
In our study, we present all-abortion hospitalisation ratios segregated for each state (Table 5 of the BMJ Open article). Arthur's letter quotes about 159,000 hospital discharges for abortion complications in public institutions in Mexico for 2009, an estimate of 1,026,000 unsafe abortions, and a complication rate of 36% for these abortions. The letter further states that approximately 25% of women with complications by unsafe abortions do not seek treatment. Arthur fails to provide any verifiable sources for these figures. In addition, a simple analysis reveals that these numbers apparently do not add up. According Mexican official data for 2012, from the total of 189,694 hospital discharges for any kind of abortion, 68,715 were related to ectopic pregnancy, mole, other abnormal products of conception and miscarriage (ICD codes O00-O03 and O08) and 112,979 associated to induced abortion, including medical abortion, other abortion, unspecified abortion, and failed attempted abortion (codes O04-O07). Subtracting the number of cases for legal terminations of pregnancies (codes O04 and O07) the hospital discharges associated with complications of other induced abortions comprise 112,564 cases and we estimate that at least 50% or more of these cases are probably the result of complications from illegal or unsafe abortions.[8] If we assume the rate of complications claimed by Arthur: 36% for 1,026,000 unsafe abortions, the result is 369,360 cases; after subtracting 25% of women that do not seek treatment, the expected number of hospital discharges related to unsafe abortions will be 277,020 cases. However, the official figure of 112,564 cases of hospital discharges probably related to unsafe abortion in public health institutions roughly represents 40% of the estimates from Arthur's letter. The overestimate suggested in the Arthur's letter is unlikely because most of the Mexican population attends public health facilities [42] and does not appear to be consistent with available data.
OTHER UNWARRANTED COMMENTS
Arthur makes unwarranted comments that are not scientifically based. For example, in reference to our studies, it is claimed that by "rendering those women invisible, such studies become dangerous weapons that threaten to slow down the global decrease in maternal mortality and continue allowing women to suffer and die unnecessarily" and that "the BMJ Open study is the latest contribution to this ideological battle disguised as science". It is further asserted that our "studies appear professional and are published in reputable journals." Although we value some criticisms in the letter, which have facilitated the contrast and free exchange of scientific ideas, we feel that such comments as the above are not germane inasmuch as they do not focus on science or the results of our research. Instead, these comments reflect the discomfort and personal beliefs of the writer. Science is not a question of authority, prejudices or subjective opinions, but a question of objective data, falsifiable hypotheses, rigorous methodology, testability and reproducibility.[47]
THE USE OF THE WORDS "PROGRESSIVE CHANGES" AND "UNBORN"
Arthur states that we characterize the Mexican states' constitutional amendments protecting the "unborn" from conception as "progressive changes." Arthur considers these expressions as "anti-abortion language". This is a distortion, which takes these terms out of context. The term "progressive changes" refers to legal changes that have steadily added Mexican states over time (Figure S1, Supplementary Material). The word "unborn" is a common legal term utilised in constitutional amendments.
UNSUBTANTIATED CRITICISM TO BMJ OPEN
Arthur states that BMJ Open accepted our study without subjecting it to sufficient scrutiny. As detailed in this point-by-point rebuttal letter, we consider this criticism unsubstantiated and inappropriate. Although our times-series study on determinants of maternal mortality in 32 Mexican states had some inherent limitations - as any observational study - all of our data come from reliable sources that can be checked independently. Following current rules of scientific transparency, BMJ Open conducted an open peer-review and the entire pre-publication history has been published. The database is publicly available, published as supplementary data at BMJ Open and also available via the Dryad data repository. Consequently, statistical analyses can be fully reproduced or re-analysed by any research group interested in corroborating or refuting our findings. Finally, BMJ Open offered a valuable opportunity to Arthur to express her ideas and criticisms of our study in an e-letter. Undoubtedly, this is another proof of scientific transparency from BMJ Open.
CONCLUSIONS
While some of the issues raised in Arthur's letter represent areas of legitimate scientific discussion, we believe she has relied on several highly questionable assumptions, overstated some concerns and neglected other important methodological strengths. The epidemiologic methods used in our study are robust, valid, reproducible, and based on reliable data from a country that has met high standards in improving and auditing their ascertainment of maternal mortality and its components, including abortion -related mortality. Additionally, many of the comments in the Arthur's letter appear to reflect a lack of understanding or difficulty accepting the conclusions of our study. We find it remarkable that maternal mortality was unrelated to differences in abortion legislation, but was largely explained by other factors such as women's literacy, maternal healthcare, emergency obstetric care, individual-level risk factors, clean water, sanitation, fertility rate and intimate-partner violence against women. Again, we wish to emphasize the importance of addressing promptly these factors that strongly impact women's health in developing nations.
REFERENCES
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6. Fajardo-Dolci G, Meljem-Moctezuma J, Vicente-Gonzalez E, et al. [Analysis of maternal deaths in Mexico occurred during 2009]. Rev Med Inst Mex Seguro Soc 2013;51:486-95.
7. Koch E, Thorp J, Bravo M, et al. Women's education level, maternal health facilities, abortion legislation and maternal deaths: a natural experiment in Chile from 1957 to 2007. PLoS One. 2012;7(5):e36613.
8. Koch E. The epidemiology of abortion and its prevention in Chile. Issues Law Med. 2015;30(1):71-85
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10. Pandya PP, Snijders RJ, Psara N, Hilbert L, Nicolaides KH. The prevalence of non-viable pregnancy at 10-13 weeks of gestation. Ultrasound Obstet Gynecol1996;7(3):170-3.
11. Boyd PA, Devigan C, Khoshnood B, Loane M, Garne E, Dolk H, et al. Survey of prenatal screening policies in Europe for structural malformations and chromosome anomalies, and their impact on detection and termination rates for neural tube defects and Down's syndrome. BJOG 2008;115(6):689-96
12. Cocchi G, Gualdi S, Bower C, Halliday J, Jonsson B, Myrelid A, et al. International trends of Down syndrome 1993-2004: Births in relation to maternal age and terminations of pregnancies. Birth Defects Res A Clin Mol Teratol 2010;88(6):474-9.
13. Nazer HJ, Cifuentes OL. [Congenital malformations in Latin America in the period 1995-2008]. Rev Med Chil 2011;139(1):72-8.
14. European Surveillance of Congenital Anomalies [EUROCAT] Available at http://www.eurocat-network.eu/accessprevalencedata/prevalencetables
15. Kulczycki A. Abortion in Latin America: changes in practice, growing conflict, and recent policy developments. Stud Fam Plann 2011;42:199-220.
16. Gissler M, Fronteira I, Jahn A, et al. Terminations of pregnancy in the European Union. BJOG 2012;119:324-32.
17. Denisov BP, Sakevich VI, Jasilioniene A. Divergent Trends in Abortion and Birth Control Practices in Belarus, Russia and Ukraine. PLoS ONE 2012;7:e49986.
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19. Aniteye P, Mayhew SH. Shaping legal abortion provision in Ghana: using policy theory to understand provider-related obstacles to policy implementation. Health Res Policy Syst 2013;11:23.
20. Okamoto E. Japan turns pro-life: recent change in reproductive health policy and challenges by new technologies. Int J Health Policy Manag 2014;2(2):61-3
21. Donoso E, Carvajal JA. [Eugenic abortion could explain the lower infant mortality in Cuba compared to that in Chile]. Rev Med Chil 2012;140(8):999-1005.
22. Culwell KR, Hurwitz M. Addressing barriers to safe abortion. Int J Gynaecol Obstet 201;121 Suppl 1:S16-9
23. Donoso E, Carvajal JA. [Eugenic abortion could explain the lower infant mortality in Cuba compared to that in Chile]. Rev Med Chil 2012;140(8):999-1005.
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25. Due?as JL, Lete I, Bermejo R, Arbat A, P?rez-Campos E, Mart?nez- Salme?n J, et al. Trends in the use of contraceptive methods and voluntary interruption of pregnancy in the Spanish population during 1997-2007. Contraception 2011;83(1):82-7.
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28. Rolnick JA, Vorhies JS. Legal restrictions and complications of abortion: Insights from data on complication rates in the United States. J Public Health Policy 2012;33:348-62.
29. Zamberlin N, Romero M, Ramos S. Latin American women's experiences with medical abortion in settings where abortion is legally restricted. Reprod Health 2012;9(1):34.
30. Donoso E, Carvajal JA. [The change in the epidemiological profile of maternal mortality in Chile will hinder the fulfillment of the Millennium 5th goal]. Rev Med Chil 2012;140(10):1253-62
31. Manouana M, Kadhel P, Koffi A, Janky E. [Illegal abortion with misoprostol in Guadeloupe]. J Gynecol Obstet Biol Reprod (Paris). 2013;42(2):137-42.
32. Flory F, Manouana M, Janky E, Kadhel P. [Sociodemographic and medical features of abortion among underage people in Guadeloupe (French West Indies)]. Gynecol Obstet Fertil. 2014;42(4):240-5.
33. Ngai SW, Tang OS, Chan YM, Ho PC. Vaginal misoprostol alone for medical abortion up to 9 weeks of gestation: efficacy and acceptability. Hum Reprod 2000;15(5):1159-62.
34. Ngoc NT, Shochet T, Raghavan S, Blum J, Nga NT, Minh NT, et al. Mifepristone and misoprostol compared with misoprostol alone for second- trimester abortion: a randomized controlled trial. Obstet Gynecol 2011;118(3):601-8.
35. Koch E, Bravo M, Gatica S, Stecher JF, Aracena P, Valenzuela S, Ahlers I. [Overestimation of the ocurrence of induced abortions in Colombia and other Latinoamerican countries]. Ginecol Obstet Mex. 2012 May;80(5):360-72.
36. Koch E, Aracena P, Bravo M, et al. [Methodological flaws on abortion estimates for Latin America: authors' reply to Singh and Bankole]. Ginecol Obstet Mex 2012;80:740-7.
37. Singh S, Wulf D. Niveles estimados de aborto inducido en seis pa?ses latinoamericanos. Perspectivas Internacionales en Planificaci?n Familiar 1994;N?especial: 3-13. Guttmacher Institute.
38. Hogan MC, Foreman KJ, Naghavi M, et al. Maternal mortality for 181 countries, 1980-2008: a systematic analysis of progress towards Millennium Development Goal 5. Lancet 2010;375:1609-23.
39. Kassebaum, NJ, Bertozzi-Villa, A, Coggeshall, MS et al. Global, regional, and national levels and causes of maternal mortality during 1990 -2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014; 384: 980-1004
40. Say L, Chou D, Gemmill A, Tun?alp ?, et al. Global causes of maternal death: a WHO systematic analysis. Lancet Glob Health. 2014;2(6):e323-33.
41. Juarez F, Singh S, Garcia SG, Olavarrieta CD. Estimates of induced abortion in Mexico: what's changed between 1990 and 2006? Int Fam Plan Perspect. 2008;34(4):158-168.
42. Knaul FM, Gonz?lez-Pier E, G?mez-Dant?s O, et al. The quest for universal health coverage: achieving social protection for all in Mexico. Lancet 2012;380:1259-79
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Conflict of Interest:
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Published on: 23 November 2015
BMJ Open Study on Abortion Mortality in Mexico Is Deeply Flawed
- Joyce H Arthur, Executive Director
A recent study in the BMJ Open that looked at the effect of abortion laws on maternal mortality in Mexico is egregiously flawed and biased. It poses an unacceptable risk to public health because it could be used to advocate the criminalization of necessary healthcare for women. This letter exposes the study's biases and flaws in detail.
The study purports to show that Mexican states with more restrictive abort...
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A recent study in the BMJ Open that looked at the effect of abortion laws on maternal mortality in Mexico is egregiously flawed and biased. It poses an unacceptable risk to public health because it could be used to advocate the criminalization of necessary healthcare for women. This letter exposes the study's biases and flaws in detail.
The study purports to show that Mexican states with more restrictive abortion laws have lower maternal mortality rates than states with more permissive laws. Although the authors refrain from hypothesizing a causal link between criminalized abortion and better maternal health outcomes, that counter-intuitive implication comes through nonetheless. It's even clearer in the authors' press release about the study.
BMJ Open is an open access journal that offers easier and quicker publication of studies, but its website also states: "Our aim is to provide a home for all properly conducted medical research to be fully reported, after a rigorous and transparent peer review process."
So what happened? Why did BMJ Open accept this study without subjecting it to greater scrutiny? Some anti-abortion language even slipped through--on page three of the study, the authors characterize the Mexican states' constitutional amendments protecting the "unborn" from conception as "progressive changes."
Leading author Elard Koch (and various other co-authors) have published previous studies related to abortion (in Chile, Colombia, and Mexico), but the methodology of those studies has been shown to be seriously flawed and biased, rendering their conclusions invalid. My blog has a compendium of rebuttals (http://choice-joyce.blogspot.ca/2012/08/a- disgraceful-example-of-bad-science.html) of Koch et al.'s previous work from both professional and lay sources.
For example, in 2012, Ipas-Mexico published an analysis (http://www.ipas.org/~/media/Files/Ipas%20Publications/SchiavonIJGO2012.ashx) of maternal and abortion-related mortality in Mexico from 1998 to 2008, showing that one in 13 maternal deaths were from abortion. Koch and some co-authors then published a rebuttal to this, and Ipas responded with a statement that referred to the Guttmacher Institute's previous rebuttals to Koch et al.'s work. Guttmacher had explained and defended (http://www.guttmacher.org/media/resources/response-to-methodology- critique.pdf) widely accepted scientific methodologies for estimating numbers of illegal abortions and resulting maternal mortality rates--which Koch et al. had grossly underestimated.
FATAL FLAW #1: DATA DREDGING TO FIND AN ASSOCIATION
The BMJ Open study concludes that "maternal and abortion-related mortality ratios were lower in states with less permissive abortion legislation compared with states with more permissive legislation." However, this is based on arbitrarily dividing Mexican states into two categories using a variable with little significance for maternal mortality: those that ban abortion for reasons of "serious genetic or congenital conditions" in the fetus, and those that don't. It's worth quoting the authors in full to expose the nature of their error:
"In exploratory analyses, segregating states by the number of exemptions provided in criminal codes did not result in detectable differences in sensitivity analyses, with the exception of abortion allowed by genetic or congenital fetal malformations. The remaining seven exemptions were distributed differentially in almost every state or very few states, thus offering no discrimination potential. Therefore, to differentiate between states with more or less permissive abortion legislation in subsequent statistical analyses, states allowing pregnancy termination due to serious genetic or congenital conditions were considered more permissive (14 states) while the remaining states were considered less permissive (18 states)."
In other words, the authors subjected each legal exemption to a "sensitivity analysis"--which checks all the data to look for patterns among variables--until they found a variable that happened to show a detectable difference in maternal mortality. They then presented this as the primary finding. This error is called "data dredging" because chance associations between just about any two things are easy to find if you crunch enough numbers. To make their random association sound more meaningful, the authors manipulated the definition of "states with less permissive legislation" into something it didn't actually mean at all.
Twelve Mexican states actually have a more liberal exemption allowing abortion in cases of serious risk to the woman's health, yet nine of those states ended up in the study's category of "less permissive." This demonstrates the arbitrariness of the chosen exemption factor of fetal anomaly, and indicates that the study could well have come to the opposite conclusion if the health exemption had been chosen as the dividing criterion instead. (All Mexican states allow abortion in cases of rape. Otherwise, abortion is mostly or completely illegal in all states except Yucatan, where it is allowed for economic or social reasons, and the Federal District of Mexico City, which allows abortion on request up to 12 weeks.)
The selected exemption for fetal anomaly cannot possibly by itself show any trends or differences in abortion mortality rates between states. That's because abortions due to fetal abnormality are always a tiny minority of abortions in any country. In Britain for example, only 1 percent of abortions are carried out for reasons of fetal anomaly, and the numbers are similarly tiny for other countries. Further, almost all abortions for fetal abnormality occur later in pregnancy because the anomaly cannot usually be detected until then.
In settings like Mexico, the numbers of abortions for fetal anomaly will likely be far smaller than 1 percent regardless of legality, because of stigma and other obstacles. Indeed, here's a study (http://www.ncbi.nlm.nih.gov/pubmed/9482653) showing that most Mexican geneticists advise against abortion when the fetus has a genetic or chromosomal disorder. And there's no reason to assume that the average Mexican woman would even know that abortion might be legally available for reasons of fetal abnormality, let alone that she would have the means, resources, or courage to pursue that option. In other words, abortions for reasons of fetal abnormality must be very rare throughout Mexico, and cannot possibly serve as a proxy for tracking trends in maternal mortality due to abortion.
This fatal flaw renders the study meaningless and the conclusion invalid, because it relies solely on a rarely occurring variable that would not have any noticeable statistical effect on maternal mortality.
FATAL FLAW #2: MISTAKING LEGAL ABORTION FOR ACCESSIBLE ABORTION
Similarly, the study assumes that because about half of Mexican states tightened their already strict laws against abortion after 2007--by passing a constitutional amendment protecting "the unborn" from conception --this would have a measurable effect on death from unsafe abortion. There is absolutely no basis for this assumption. Criminal laws restricting most abortions were already in effect everywhere outside Mexico City, so women would not be driven to unsafe abortion in any greater discernible numbers.
This helps expose the second major flaw in the study: the authors' assumption that abortion law accurately predicts abortion practice. In reality, few Mexican women actually obtain abortions under the legal exemptions due to fear and stigma, lack of resources or knowledge, and refusals by anti-abortion doctors.
One study (in Spanish: http://msmagazine.com/blog/2013/05/30/the- criminalization-of-abortion-continues-in-mexico/) by the Mexico City-based Group on Reproductive Choice (GIRE) showed that between 2007 and 2012, only 39 women in Mexico actually got a legal abortion under the country- wide rape exemption, out of a total of 120 who had applied for one. Why would so few apply? First, most states lack sufficient administrative mechanisms for seeking out a legal abortion under any of the exemptions, which means there's simply no way to even apply for an abortion. Second, abortion is highly stigmatized in Mexico, and it takes courage to apply for one--or seek medical attention after an illegal abortion. At least 679 women in Mexico were reported or sentenced for having an illegal abortion between 2009 and 2011. Mexico is one of at least seven countries in the world that imprisons women for having illegal abortions. From 2007 to 2012, 127 women were put on trial for abortion in Mexico, and in one particularly conservative state, Guanajuato, dozens of women have been prosecuted for abortion since 2000, with some of them receiving sentences of up to 30 years in prison.
Oddly, Koch et al. never mention such shocking facts, nor do they mention the deeply rooted stigma and shame surrounding abortion in Mexico, the judgmental attitudes of many healthcare workers, or indeed any of the social, economic, or logistical difficulties that may inhibit women from even attempting to exercise their legal right to abortion in Mexico. Instead, the study's methodology and conclusion depend on the unspoken assumption that legal exemptions for abortion mean that all or most of those exempted abortions are actually taking place as needed. Nothing could be further from the truth.
FAILING TO ACCOUNT FOR UNDERREPORTING AND THE IMPACT OF SAFER MEDICAL ABORTION
Koch et al. fail to acknowledge that "do-it-yourself" medical abortions have increased substantially over the last decade or more, with pills to end pregnancy now widely available in Mexico and most other Latin American countries. In fact, the words mifepristone and misoprostol never appear once in the BMJ Open study, which is a serious oversight. Clandestine use of the drug misoprostol is generally accepted as being much safer than traditional and more dangerous methods (for example, significantly reducing the rate of infection), even when women misuse it or misinterpret its effects because they don't have instructions on how to use it or what to expect.
In one of Koch's 2012 rebuttals to the Guttmacher Institute, he asserted that "no study currently exists to date that seriously supports a decline in maternal mortality associated with the use of abortifacient drugs such as misoprostol in Chile." But he ignored several studies from countries such as Brazil and Mexico that showed significant declines in the severity and number of abortion-related complications and sometimes mortality over the same periods in which misoprostol use has grown.
In the BMJ Open study, Koch and his co-authors follow the same pattern as in a previous Koch-led study on Chile (http://www.guttmacher.org/media/evidencecheck/2012/05/23/Guttmacher- Advisory.2012.05.23.pdf): They underestimate the number of abortions and associated maternal mortality by relying only on official statistical sources, while failing to consider that large numbers of illegal abortions are not accounted for in these sources, and that related complications and deaths may often be misclassified. In a criminalized and stigmatized environment, many women will not admit to having an abortion, and many health professionals will not officially report complications or deaths as caused by abortion, either through ignorance of the real cause, or out of compassion for women and their families.
Koch et al. claim there is no reason for healthcare professionals in Mexico to "misreport deaths from a suspected illegal abortion" due to the existence of separate reporting codes for various types of abortions, including for an unknown cause. This overlooks the fact that issues with miscoding (http://www.guttmacher.org/pubs/journals/3805812.html) have become more common with misoprostol-related complications. For example, it can be challenging for doctors to distinguish medical abortion from miscarriage or other obstetrical complications. Further, Koch et al.'s analysis ignores the effects of fear and abortion stigma on how abortion occurs in illegal settings and whether complications or deaths resulting from them are reported as such.
USING REDUCED MATERNAL MORTALITY TO MASK ABORTION DEATHS
It's already well established--practically self-evident--that maternal mortality can be significantly reduced by educating women, upgrading health systems, and improving access to contraception, skilled birth attendants, clean water, sanitation, and so on. Yet, this study and previous Koch-led studies seem to treat such factors like their own new discovery that obviates any need to reform abortion laws.
Unsafe abortion is just one of many factors that affect maternal mortality rates, though it's among the top five causes. An estimated 13 percent of maternal mortality globally is due to unsafe abortion. It is simply not possible to try to take into account a lot of contributing factors to maternal mortality and conclude that restrictive abortion laws have little or no effect, because the other factors can easily swamp the effect of unsafe abortion on maternal mortality rates. Is it possible that the authors of the BMJ Open study are using such factors as a smokescreen to cover up the effect of unsafe abortion on maternal mortality?
Mexico still has a relatively high maternal mortality rate compared to other countries--about 45 per 100,000 live births, compared to 28 for the United States, 13 for Canada, and four for Sweden. In Latin America, where abortion is mostly illegal, it's 22 for Chile and 69 for both Brazil and Argentina (2013 data). It's likely that the declines Mexico has been seeing in maternal mortality would be even steeper if abortion was safe, legal, and accessible, and the same goes for Chile.
Estimating the incidence of illegal, unsafe abortion as well as the resulting deaths and complications is of course a challenging task. Such abortions are unreported and usually never come to the attention of authorities, so vital statistics can only provide a fragment of the evidence-based picture. A variety of methods must be used to carefully piece together a picture that is as reliable as possible. These include, for example, surveys of women, surveys of specific healthcare facilities, and interviews with knowledgeable healthcare workers.
Such methodologies are embodied in the Abortion Incidence Complications Method (AICM), which was developed about 20 years ago. The AICM has been widely used in studies appearing in peer-reviewed journals, and is recognized by experts around the globe, including the World Health Organization. Despite this, Koch has simply tossed out the AICM on the basis that it uses "imaginary numbers." (http://www.guttmacher.org/media/resources/response-to-methodology- critique.pdf) Not only is this dismissal disingenuous and unwarranted, it amounts to a gratuitous slur against the hundreds of reputable scientists and researchers who spend large amounts of time carefully gathering, comparing, and adjusting abortion-related data under challenging circumstances.
REAL WORLD ABSENT FROM STUDY
The BMJ Open study has an important focus on maternal mortality, but unfortunately that focus tends to disguise certain facts that never see the light of day in the study:
* More than a million (1,026,000) abortions take place in Mexico each year, the large majority of them illegal.
* About 159,000 women were treated at public hospitals for abortion complications in 2009.
* An estimated 36 percent of all women who have illegal abortions develop complications that need medical treatment.
* One-quarter of those do not seek treatment, putting them at risk of lasting negative health consequences.
The question that Koch et al. need to answer is this: Even if the study did demonstrate that restrictive abortion laws are associated with lower maternal mortality, does that make it acceptable to let a million desperate Mexican women, year after year, suffer the distress and trauma associated with risking their lives, health, and freedom to obtain an illegal abortion?
Koch et al.'s studies, including the current one in BMJ Open, are promoted widely on the Internet by anti-abortion groups and individuals. Because the studies appear professional and are published in reputable journals, there is a real danger that they can be used to influence policy decisions of governments. For example, they may play a role in decisions to decrease or cut funding for reproductive health programs in developing countries--such as what occurred in Canada in 2010--or to further restrict abortion, despite current laws that still kill 47,000 women a year and injure over eight million.
By rendering those women invisible, such studies become dangerous weapons that threaten to slow down the global decrease in maternal mortality and continue allowing women to suffer and die unnecessarily. The BMJ Open study is the latest contribution to this ideological battle disguised as science, one that poses a grave public health risk to women.
AUTHOR'S NOTE: I would like to thank the Guttmacher Institute for its past work, cited in this letter, exposing the serious methodological flaws in Elard Koch's work and debunking his false claims.
(Further sources for this letter can be found at: http://rhrc.us/1ETRq9P)
Conflict of Interest:
None declared
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Conflict of Interest:
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Published on: 23 November 2015
'False Witnesses' Publish Deeply Flawed Study on Abortion Mortality in Mexico
- Joyce Arthur, Executive Director
This study has been comprehensively refuted, with fatal errors found that invalidate the conclusion:
http://rhrealitycheck.org/article/2015/03/25/false-witnesses-publish-deeply-flawed-study-abortion-mortality-mexico/
Conflict of Interest:
None declared

Conflict of Interest:
None declared.
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