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. 2022 Dec 14:10.1002/bdr2.2136. Online ahead of print. doi: 10.1002/bdr2.2136

Physician hesitancy to recommend COVID‐19 vaccination in pregnancy as a cause of maternal deaths ‐ Robert Brent was prescient

Amos Grunebaum 1,✉, Frank A Chervenak 1
PMCID: PMC9878218  PMID: 36515139

1. INTRODUCTION

COVID‐19 is caused by the 2019 novel coronavirus (2019‐nCoV). The first cases of COVID‐19 were identified in December 2019, and the first U.S. case was identified on January 20, 2020. Since then, COVID‐19 has spread throughout the world and was declared a pandemic by the WHO on March 11, 2020 (Cucinotta & Vanelli, 2020).

As of July 2022, there have been 224,587 pregnant patients infected with COVID‐19, and 34,527 were hospitalized in the United States. The first death of an unvaccinated pregnant woman from COVID‐19 was reported in March 2020 and as of July 2022, there have been 305 deaths of pregnant women in the United States. The majority (155) of these deaths occurred in the 7 months between August 2021 and February 2022, (Centers for Disease Control, 2022a, 2022b, 2022c, 2022d, 2019) more than 9 months after vaccines were first introduced.

As early as February 2021, within 2 months after COVID‐19 vaccines were introduced, there were no “red flags” according to Fauci (United States Today, 2021), and no increased serious adverse events for women who were or became pregnant in the clinical trials of COVID‐19 vaccines pregnant women that would have warranted suspension of these trials. There was no documented theoretical risk of maternal, fetal, or neonatal harm, and there were no documented increased adverse outcomes in vaccinated pregnant women. Chervenak et al. concluded that COVID‐19 vaccination should be strongly recommended by providers to prevent severe maternal morbidity and death. (Chervenak et al., 2021).

2. HOW DOES COVID‐19 AFFECT PREGNANCY?

Pregnant patients are more likely to be very sick and die from COVID‐19 compared to people who are not pregnant, require increased hospitalization, admission to an intensive care unit (ICU), or use of a ventilator or special equipment to breathe. (Badell et al., 2022) Pregnant patients also have an increased risk of hospital admission, need for oxygen therapy, need for endotracheal intubation, an elevated case‐fatality rate among pregnant women compared with nonpregnant women of similar age, (Metz et al., 2021); Wei et al. (2021); Villar et al. (2021) and they have an increased risk of stillbirth. (DeSisto, 2021) It should be no surprise when considering that the immune system is affected in pregnancy, that COVID‐19 infected pregnant patients are sicker than nonpregnant patients, and that unvaccinated pregnant patients are at increased risks for maternal morbidity, deaths, and pregnancy complications. (Badell et al. 2022) Admission of COVID‐19 infected pregnant patients to the ICU and maternal mortality were exclusively in unvaccinated patients. (Atak et al. 2022; Aslam et al. 2022).

3. HESITATION TO RECOMMEND COVID‐19 VACCINATION

In a sentinel publication in 2003 Robert Brent (2003) called for establishing successful vaccine programs for pregnant women as the quintessence of preventive medicine. Maternal vaccination against COVID‐19 is the best way not only to protect against maternal morbidity and mortality, but also protects the soon‐to‐be‐born child and infant. (Badell et al. 2022; Razzaghi et al. 2021; Rasmussen & Jamieson 2022). As with other vaccines recommended in pregnancy, there are no known pregnancy‐specific adverse effects of COVID‐19 vaccines.

In February 2021 Chervenak et al., (2021) laid out a professionally responsible COVID‐19 vaccination counseling guide for patients who are pregnant, planning to become pregnant, and breastfeeding or planning to breastfeed. The authors advocated that clinicians should strongly recommend COVID‐19 vaccinations and how this assessment should be presented to patients during the informed consent process with the goal of empowering them to make informed decisions to improve their safety and the safety of their soon‐to‐be born child.

A recommendation by a physician or another health care professional is crucial to improve vaccine acceptance. (Badell et al. 2022; Chervenak et al, 2021; Chervenak et al. 2022). Even though considering that COVID‐19 infected patients have higher morbidity and mortality rates and that there were no documented ill effects of COVID‐19 vaccination in pregnancy, or increased pregnancy complications, professional organizations including the CDC hesitated to recommend COVID‐19 vaccinations for most of 2021. The lower vaccine acceptance rate of pregnant women especially among persons of Black and Hispanic race and among younger women (aged 18–24 years), (CDC, 2022e; Davies et al. 2022) led to a significant increase in maternal mortality at the end of 2021. (Davies et al. 2022).

The American College of Obstetricians and Gynecologists (ACOG) and the Society for Maternal‐Fetal Medicine (SMFM) as well as the Centers for Disease Control (CDC) hesitated to recommend COVID‐19 vaccination recommendations to pregnant women until the end of July, 2021. (ACOG, 2022b; ACOG, 2022c; CDC, 2022g; CDC, 2022h; CDC, 2022f) In fact, pregnant patients were the only group who had been specifically excluded from these recommendations. At that time, it had become evident that there was a significantly elevated maternal mortality in unvaccinated pregnant patients.

As early as February 2021, most states in the United States (36 of 51; 71%) encompassing 71% of the population in the United States did not include pregnant individuals among their priority populations. (Grünebaum et al., 2021) Only 6 of 13 states mentioned pregnancy as a priority indication for COVID‐19 vaccination and none of the 36 states not including pregnancy in priority groups linked back to the Centers for Disease Control and Prevention definition of pregnancy as an increased risk of severe illness. (Grünebaum et al., 2021).

In a news release on January 27, 2021, (ACOG, 2022a) ACOG and SMFM stated that “Data have demonstrated that symptomatic pregnant individuals with COVID‐19 are at increased risk of more severe illness and death compared with nonpregnant peers. Many pregnant individuals have medical conditions known to put them at further increased risk of severe illness and complications. Therefore, given clear evidence of the dangers of COVID‐19 in pregnancy, an absence of data demonstrating adverse effects associated with the vaccine in pregnancy, and in the interest of patient autonomy, ACOG and SMFM recommend that pregnant individuals be free to make their own informed decisions regarding COVID‐19 vaccination.” (ACOG, 2022a) The terminology “recommend …. to make their own decision.” clearly shows the hesitation of these professional organizations to recommend vaccination. It is also a misapplication of understanding the meaning of patient autonomy.

Subsequently, the CDC and ACOG changed their language concerning COVID‐19 vaccination in pregnancy over time (Tables 1 and 2) The authors believe that the initial hesitation to explicitly recommend COVID‐19 vaccination for pregnant patients was due to physician hesitancy with three root causes: Misapplication of therapeutic nihilism, misapplication of shared decision making, and misapplication of respect for autonomy. (Chervenak et al. 2022) Therapeutic nihilism had and continues to have an important place in professional obstetric practice embodied in the ethical principle of nonmaleficience (primum non nocere). However, this is not an absolute professional obligation when the medical evidence of benefit is clear and there is no documented harm such as was the case in January 2021.

TABLE 1.

American college of obstetricians and gynecologists (ACOG) statements on COVID‐19 and pregnancy

ACOG before July 30, 2021 (ACOG, 2022c) ACOG from July 30, 2021 (ACOG, 2022d)

ACOG recommends that pregnant individuals have access to COVID‐19 vaccines.

COVID‐19 vaccines should be offered to lactating individuals similar to nonlactating individuals. Pregnant patients who decline vaccination should be supported in their decision.

ACOG recommends that pregnant individuals be vaccinated against COVID‐19.

ACOG recommends that lactating individuals be vaccinated against COVID‐19.
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TABLE 2.

Centers for disease control statements on COVID‐19 and pregnancy

CDC January 1, 2021 (CDC, 2022g) CDC June 29, 2021 (CDC, 2022h) CDC August 1, 2021 (CDC, 2022h)

People who are pregnant and part of a group recommended to receive COVID‐19 vaccine, such as healthcare personnel, may choose to be vaccinated.

 Pregnant and recently pregnant people are more likely to get severely ill with COVID‐19 compared with nonpregnant people. If you are pregnant, you can receive a COVID‐19 vaccine. Getting a COVID‐19 vaccine during pregnancy can protect you from severe illness from COVID‐19.

COVID‐19 vaccination is recommended for all people 12 years and older, including people who are pregnant, breastfeeding, trying to get pregnant now, or might become pregnant in the future.
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Shared decision making (nondirective counseling) has an important role in professional obstetric practice when the choice between medical options is uncertain. (CDC, 2022) This was not the case in January 2021 regarding COVID‐19 vaccination in pregnant patients. Respect for autonomy is a core ethical obligation in professional obstetric practice. However, when the medical evidence is decisive and when vaccinations have population‐level impact, it is a misapplication of this core ethical obligation to respect a patient's autonomy to not recommend an immunization such as vaccination against COVID‐19. This was clearly the case in January 2021 regarding COVID‐19 vaccination for pregnant patients. (Grünebaum et al., 2021) It must be emphasized that pregnant patients report that the health care providers recommendation for vaccination is the most decisive factor in their cdc informed decision, thereby documenting that the physician's recommendation for vaccination is an important autonomy‐enhancing strategy. (Badell et al., 2022, Chervenak et al., 2022).

Chervenak et al. stated that “…the longer physician hesitancy continues and the longer the low vaccine acceptance rate of pregnant women lasts, preventable serious diseases, deaths of pregnant women, intensive care unit admissions, stillbirths, and other maternal and fetal complications of unvaccinated women will continue to occur.” (Chervenak et al. 2022) Unfortunately, their fears became a reality when, likely as a result of physician hesitancy and delaying vaccine recommendations for pregnant women by major organizations until later in 2021, unvaccinated women died at the end of 2021 and beginning of 2022 as a consequence of a lower vaccine acceptance rate by pregnant women. (Atak et al. 2022, Aslam et al. 2022).

In an extensive review of COVID‐19 vaccination in pregnancy, there were no concerning safety signals, specifically no increase in fetal malformations, (Badell et al. 2022) and studies indicated that the administration of the mRNA vaccines resulted in a robust maternal humoral response. Although the antibody response to vaccination among pregnant patients has not been rigorously compared with the response among nonpregnant patients, there has been no reason to expect differences. Furthermore, maternal immunoglobulin G antibodies efficiently cross the placenta, resulting in relatively high titers in the fetus. (Badell et al. 2022) There are no known or theoretical risks of COVID‐19 vaccination of breastfeeding women and there are no restrictions to the vaccination. Women should be reassured that COVID‐19 vaccines do not affect fertility, that COVID‐19 vaccines cannot cause COVID‐19 as none of them contain the live virus, that the COVID‐19 vaccines do not interact with or alter genetic material, and that the vaccines do not contain any controversial substances. (ASRM 2022).

In August 2022 Walensky, the director of the Centers for Disease Control and Prevention, delivered a sweeping rebuke of her agency's handling of the coronavirus pandemic. (New York Times 2022) She said it had failed to respond quickly enough and needed to be overhauled. “To be frank, we are responsible for some pretty dramatic, pretty public mistakes, from testing to data to communications”. Its public guidance has often been confusing, even to public health experts.

Unvaccinated women who contracted COVID‐19 during pregnancy were at a higher risk of stillbirths. They also were more likely to be admitted to the intensive care unit, give birth prematurely or die. Yet their greatest protection—the COVID‐19 vaccine—sat largely untouched, buried under doubt, polluted by disinformation.” (ProPublica, 2022) Other professional organizations have yet to acknowledge that the hesitancy to recommend COVID‐19 vaccination for pregnant patients for a long time likely contributed to the low acceptance of COVID‐19 vaccination in pregnant women, and consequently the unacceptable increase in maternal deaths. Instead of acknowledging the delay to recommend the vaccine to pregnant patients, they emphasize the failure to recommend vaccines to pregnant patients on the absence of having included pregnant patients in the initial vaccine trials: “It played out in real time in the COVID pandemic because we see the effects of not including pregnant people in these trials.” (ProPublica, 2022) We emphasize that the final guideline of professional groups to change from “offer” to “recommend” was made without a randomized clinical trial (RCT). The conclusion that COVID‐19 vaccines should be recommended to pregnant women, did not require completion of the clinical trials, US Food and Drug Association approval, or sanction by professional association. It is important to keep in mind that although RCTs are considered as the “gold standard,” they should not be considered the only standard. Most therapeutic and clinical recommendations in pregnancy are made without the benefit of RCTs.

4. THE RISK OF DOING NOTHING

Dr. Brent (Brent 2006) was prescient 17 years ago when he wrote an insightful article called: “Risks and benefits of immunizing pregnant women: the risk of doing nothing.” Dr. Brent laid out six beneficial points for immunizing pregnant women or women of reproductive age:

  1. To protect the mother, to protect the newborn and infant and to prevent diseases and complications of pregnancy.

  2. Preparation of vaccines against infectious agents that are known to result in reproductive pathology and congenital malformation if the infection of the mother occurs during pregnancy.

  3. To utilize vaccines used routinely to protect the nonpregnant population, for administration during pregnancy.

  4. Utilization of vaccines to protect women from diseases to which they are susceptible because of pregnancy.

  5. Utilization of vaccines for use before or during pregnancy, primarily to protect the newborn and infant via maternal transplacental antibodies,

  6. The prevention of intrauterine infection that has been alleged to initiate premature labor.

With the advent of COVID‐19 Dr. Brent's points are even more important. Doing nothing was a clinical error. Hesitating to recommend the COVID‐19 vaccine in pregnancy, despite clear evidence of harm to COVID‐19 infected pregnant patients who were no vaccinated, and even though there was no evidence of potential harm from vaccination likely led to fewer pregnant women accepting vaccination and subsequently the preventable increase in maternal mortality. Physicians and other health care providers should continue to strongly recommend COVID‐19 and other safe indicated vaccinations to pregnant patients, those trying to get pregnant, and those who breastfeed, and those who initially decline vaccination.

5. CONCLUSION

Pregnancy increases the risk of severe maternal and fetal/neonatal disease associated with COVID‐19 infection. Compared to unvaccinated pregnant, vaccinated pregnant patients are significantly less likely to develop severe disease, adverse pregnancy and neonatal outcomes are more common among women infected with COVID‐19, and a pregnant patient's vaccination also protects the newborn infant because maternal antibodies protect the fetus and newborn. COVID‐19 vaccinations and boosters in pregnancy are safe for the pregnant patient and her fetus. There is no evidence vaccination impairs fertility.

Data on vaccine coverage show that pregnant women have been less likely to receive a COVID‐19 vaccine despite their increased risk for severe disease and the risks of adverse pregnancy and neonatal outcomes if infected. This lower vaccine acceptance rate is consistent with physician hesitancy and a significant delay in vaccine recommendations in pregnancy to recommend COVID‐19 vaccination for pregnant patients. The three root causes of physician hesitancy: Misapplication of therapeutic nihilism, misapplication of shared decision making, and misapplication of respect for autonomy (Chervenak et al. 2022) should not be ignored.

It is important that we heed Robert Brent's insightful recommendations. (Brent 2006) Doing nothing in respect to vaccination is not an option, with COVID‐19 and with future pandemics. Physician hesitation is not an option. When there is sufficient evidence of vaccine safety and effectiveness without documented risks, vaccine recommendations before, during, and after pregnancy should be explicitly made to prevent maternal, fetal, and neonatal morbidity and mortality.

Grunebaum, A. , & Chervenak, F. A. (2022). Physician hesitancy to recommend COVID‐19 vaccination in pregnancy as a cause of maternal deaths ‐ Robert Brent was prescient. Birth Defects Research, 1–6. 10.1002/bdr2.2136

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