Influenza vaccination during pregnancy: opinions and practices of obstetricians in an urban community.

Background: Influenza vaccination is recommended for all women who will be pregnant during the influenza season; however, little is known about the attitudes of physicians regarding vaccination of pregnant women.

Methods: We conducted a survey of all the fellows of the American College of Obstetricians and Gynecologists (ACOG) who live and practice in Nashville, Tennessee, focusing on physician knowledge, practices, and opinions regarding influenza vaccination of pregnant women.

Results: Thirty-seven of 58 (64%) eligible physicians participated. Obstetrician opinion on the earliest influenza vaccine administration for healthy pregnant women was 62% during the second trimester, 32% during the first trimester, and 6% felt that the vaccine should not be given during pregnancy. All physicians responded that pregnant women with an underlying high risk condition should be vaccinated.

Conclusion: Practicing obstetricians differ in their preferences regarding the timing of influenza vaccine administration in pregnant women. Obstetrician and patient opinion and practice should be studied and considered in developing vaccine guidelines and vaccine implementation strategies.

Key Words: influenza vaccine, obstetricians, pregnancy

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Certain groups of the general population are at increased risk for influenza complications. (1,2) Those high-risk populations include the elderly, young children, and pregnant women. (1,3) The most severe complications from influenza in pregnant women are from primary influenza pneumonia or secondary bacterial pneumonia. (4) We have shown that when superimposed on a high-risk condition (asthma, diabetes mellitus, etc.), influenza infection during pregnancy, especially with advancing pregnancy, contributes to morbidity that is three to four times greater than in comparable postpartum or nonpregnant women with similar high-risk conditions. (3,5)

Historical data reflecting an account of mortality during two major influenza pandemics in the 20th century substantiate the considerable risk influenza poses to pregnant women. (3) In the first pandemic of 1918 to 1919, the gross mortality was 27%, and among those with influenza complicated by pneumonia, 54% died. (6) During the second influenza pandemic in 1957 to 58, 10% of 216 deaths in New York City occurred in pregnant women and nearly one half of all women of childbearing age who died were pregnant. (7) More recent studies have shown an increase in maternal morbidity associated with influenza with advancing pregnancy. (3,8)

While approximately 10% of adults and up to 30% of children are infected with influenza every year, pregnant women and women of childbearing age also have higher exposure risk, in addition to having higher morbidity associated with influenza virus. (2) In 1997, ACOG and the Centers for Disease Control and Prevention (CDC) officially recommended influenza vaccination during the second trimester for healthy pregnant women, and in the first trimester for pregnant women with high-risk conditions. (9) In 2004, the CDC expanded its recommendation to include all women who will be pregnant during the influenza season, without a preference for time of vaccination. (10) Despite these recommendations, only 13% of pregnant women actually received an influenza vaccination in 2003. (11)

The low influenza vaccination rate and relatively high morbidity among pregnant women indicate that there are barriers that are impeding compliance with vaccination guidelines. Pregnant women and/or physicians may view indications and risks of vaccination differently during pregnancy compared with vaccination of nonpregnant persons. These barriers first need to be identified, and if found to be modifiable, could be addressed by physician education, patient education, and/or public health policy changes to improve vaccination rates among this vulnerable population. To obtain a greater understanding of the knowledge, actual practices and opinions of healthcare providers regarding this issue, we surveyed practicing obstetricians in an urban region of middle Tennessee.

Materials and Methods

In May 2004, an anonymous 37-item questionnaire, developed and modified from the survey developed by Schrag et al, (12) which focused on knowledge, practices, and opinions on influenza vaccination, was mailed to 100 ACOG fellows who live in Nashville and Davidson County, Tennessee. The 100 practitioners we surveyed represent all ACOG members who live and are practicing obstetrics and gynecology in the Nashville and Davidson county area of Tennessee. The ACOG is a professional organization to which most obstetricians and gynecologists belong. Family physicians, nurse practitioners, and nurse midwives who also practice obstetrics and gynecology were not included in this survey. To better understand to what extent the proportion of providers identified through ACOG represented for the total providers to pregnant women in this urban area, we used the 2003 to 2004 yellow pages data for Nashville, Tennessee. Survey questions were developed with the assistance of obstetricians and vaccine specialists employed by the CDC. The questionnaire included basic demographic information about the healthcare provider, their practice and patient mix. It sought information about influenza vaccine practices and asked about personal opinions regarding what trimesters influenza vaccination should be administered to both healthy and high-risk pregnant women. The timing of our survey followed the CDC updated recommendation of influenza vaccination to include all women who will be pregnant during the influenza season, without a preference for time of vaccination. (10) Approximately four weeks following the first survey mailing, a second mailing was sent to increase the response rate. Physician responses were included in the study if they reported that they were actively practicing obstetrics (n = 58).

Data are reported as median (interquartile range: IQR) for continuous variables. For categorical variables, proportions were used. Not every physician answered all questions polled on our survey, which was taken into account in the analysis.

The study protocol was reviewed by the Vanderbilt University Institutional Review Board and approved, and physicians were informed that returning the questionnaire implied their consent to participate in the study.

Results

Questionnaires were mailed to all Nashville/Davidson County ACOG fellows (n = 100); 14 physicians (14%) could not be found or had relocated, and 28 (28%) were not currently practicing obstetrics. Using the 2003 to 2004 yellow page data, 97 physicians were identified as practicing obstetrics or gynecology in the Nashville/Davidson County area. Among these, 78 advertised practicing obstetrics, confirming that our survey population represented the majority of physician providers in this urban area. Of 58 eligible physicians surveyed who confirmed that they were actively practicing obstetrics, 37 surveys were completed and returned, for a 64% response rate.

Demographics of Survey Respondent

The median age of physicians was 48 (42-54) years. Sixty-five percent were male; 86% were Caucasian, 11% were African-American, and 3% were Asian (Table 1). Eighty-six percent (31 of 37) of physicians were personally immunized with the influenza vaccine in 2003 to 2004.

Practice Characteristics

The median time an obstetrician had been in practice was 17 (12-21) years. The median proportion of the physicians' practice devoted to obstetrics was 50% (40-60). These obstetricians considered themselves the primary care provider for 40% (20-50) of their patients. The median number of deliveries each physician performed in 2003 was 120 (100-150). The physicians spent, on average, 58 (42.5-60) hours per week practicing clinical medicine (Table 1). Forty-two percent (15 of 36) of obstetricians saw between 0 to 15 women in a half day of clinic, while 58% saw 16 to 30 women. The median number of physicians in each practice group was 5 physician providers and 1 nurse practitioner and/or physician assistant. Seventy percent of the survey respondents practiced obstetrics in a private setting (Table 1).

Patient Characteristics

Approximately 73% (60-75) of the patients cared for were Caucasian, 20% (18-28) were African-American, and 9.5% (5-15) were other racial and ethnic groups (Hispanic, Asian, and Native American). An estimated 5% (0-35) of the women were eligible for Medicaid at the time of delivery, and an estimated 10% (5-40) of these obstetric patients had an additional chronic medical condition (Table 1).

Influenza Vaccination Practices

Among the physicians surveyed, 68% of obstetricians had specific influenza guidelines in place in their practices, and 89% reported that they routinely recommend influenza vaccination to their pregnant patients. Seventy-three percent of obstetricians administered the influenza vaccine at their offices (Table 2). Among the 27 (73%) physicians who actually administered influenza vaccine in their practice, all offered the vaccine to obstetric and postpartum patients, 59% offered it to gynecology patients, and 15% responded that they also referred patients elsewhere. Forty-one percent of physicians reported the approximate number of doses their practice administered to pregnant patients during the 2003 to 2004 season. Fifty-eight percent of obstetricians reported experiencing a vaccine shortage in 2003 to 2004. Pregnant patients were notified of the need for influenza vaccination by recommendation during the office visit (100%), by notice posted in the office (7%), and also by notice posted on a website (4%). Physicians administered the influenza vaccine at scheduled visits (100%), nurse-only visits (33%), by standing orders for drop-ins (19%), and at "flu shot" times in specified clinics (4%). Seventy percent (30-80) of the pregnant patients were estimated to receive the influenza vaccine in the 2002 to 03 influenza season; while 73% (45-80) were estimated to have received the influenza vaccine in the 2003 to 04 season (Table 2).

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Physician Opinion Regarding Influenza Vaccine Administration

Among obstetricians who administered influenza vaccine in their practices, physicians responded that they recommended the vaccine to 95% of their pregnant patients. All survey respondents were asked to state, in their opinion, in what trimester healthy pregnant patients should receive the influenza vaccine. Sixty-two percent reported the earliest administration should be the second trimester; 32% reported the earliest administration should be the first trimester; none responded that vaccination should be withheld until the third trimester, while 6% responded that vaccine should not be administered at any time during pregnancy (Fig). Of those who felt that the influenza vaccine should not be administered to healthy pregnant women until the second trimester, they cited guidelines, vaccine liability, vaccine safety, patient concerns, association with an unrelated spontaneous abortion, and impact of vaccine on embryogenesis during the first trimester as reasons influencing their opinion. A similar question was asked about pregnant women with an underlying high-risk condition. All physicians believed that high-risk pregnant patients should be vaccinated. Fifty-four percent reported the earliest administration should be the second trimester, while 46% reported the earliest administration should be the first trimester. Again, none responded that vaccination should be withheld until the third trimester (Fig.). The reasons physicians cited to withhold influenza vaccine until the second trimester were similar to reasons cited for healthy pregnant women.

Physicians were asked to identify the potential barriers to administering influenza vaccine to pregnant patients. Patient refusal (48%), inadequate reimbursement (42%), ambiguous guidelines (24%), lack of patient-oriented vaccine information (24%), liability concerns (21%), vaccine efficacy concerns (21%), lack of time during patient visits (18%), vaccine safety (18%), vaccine availability (3%), and lack of staff (3%) were identified as barriers preventing physicians from administering influenza vaccine to their pregnant patients. The most problematic issue identified regarding influenza vaccine administration in clinical practice during the 2003 to 04 season was vaccine availability.

Discussion

This study represents the knowledge, practice and opinions of practicing obstetricians with regard to influenza vaccine administration of pregnant women in the Nashville/Davidson County area, an urban region in middle Tennessee. This survey revealed that many practitioners believe the influenza vaccine poses little risk to the mother and/or fetus, but this continues to remain an area of concern for some obstetricians. Among the obstetricians surveyed, all agreed that the influenza vaccine should be provided to all pregnant women with additional high-risk conditions. For otherwise healthy pregnant women, 6% of obstetricians believed no influenza vaccine should be administered, and a majority thought that it should be withheld until the second trimester (Fig). Our survey revealed that most obstetricians believed in the beneficial effect of the influenza vaccine and recommended vaccination to most of their pregnant patient population. However, although both the ACOG and CDC have updated influenza vaccine recommendations to include all pregnant women at any gestational age, the opinion (not practice) of more than half of the physicians in this survey was that vaccine should be withheld until the second trimester for healthy pregnant women. This pattern is consistent with the ACOG survey in 2004, which revealed that nearly half of the physicians surveyed reported that they would not recommend influenza vaccination for a healthy woman during the first trimester of pregnancy, while approximately 40% of physicians did not recommend influenza vaccination for pregnant women with high-risk conditions in the first trimester. (13) Despite current recommendations, 6% of practicing obstetricians believed that the influenza vaccine should not be given at all to healthy pregnant women throughout pregnancy (Fig). This might reflect lack of knowledge of the recommendations, for which educational interventions might help, but it might also reflect personal preferences based on concerns about the safety of vaccinating women during pregnancy or liability, as illustrated by the reasons respondents cited for not vaccinating in the first trimester.

Vaccine effects on the fetus continue to be a concern for both potential parents and healthcare providers. The Collaborative Perinatal Project sponsored by the National Institute of Neurologic and Communicative Disorders and Stroke followed 50,000 women through pregnancy and delivery. Influenza vaccines were administered to a portion of the cohort. The patients were closely observed and the children of those patients were followed for seven years for any ill effects. No adverse side effects were associated with the vaccine. (14) No serious adverse events occurred within 42 days of vaccination and no difference in the outcomes of pregnancy and in the health of the infants from birth to six months of age were reported when comparing healthy vaccinated women to un-vaccinated women in the Houston, Texas area from 1998 to 2003. (15) There is also evidence that pregnant women who receive the influenza vaccine have comparable immune responses to nonpregnant, age-matched controls. (14) In addition, there is effective transfer of vaccine-specific antibodies to the fetus. (14,16) However, it is clear that despite the availability of national practice guidelines for many diseases and their prevention, women remain concerned about the potential for vaccinations and medications to cause birth defects. (17)

The potential for a false correlation should be an important area of concern for public health specialists. In one study, (18) approximately 22% of pregnant women with detectable human chorionic gonadotropin (hCG) in their urine miscarried, usually before clinical recognition of the pregnancy. The loss rate for clinically recognized pregnancies has been accepted to be 10 to 12%, with most of those occurring before eight weeks. (19) Three percent of pregnancies abort after 8 to 9 weeks, and there is a 1% loss rate after 16 weeks. (19,20) Using ultrasonography, studies confirmed that fetal demise often occurs weeks before the mother experiences symptoms. (19) The inability to determine exactly the timing of a spontaneous abortion could increase the chances of a grieving mother identifying anything temporally linked to the event as causative. It is logical that delaying vaccine administration until the second trimester, when miscarriages fall dramatically, would lessen the likelihood of a false correlation.

False correlations of adverse events with vaccines can have powerful effects. The alleged link between measles, mumps, and rubella (MMR) vaccine and autism led to declines in vaccination in the UK from a peak of 92% in the mid-1990s to a national level of 82% in 2003 and less than 75% in London. (21) In this country, concerns about vaccines and autism led to a Congressional hearing in 2000, where heartbroken parents shared their suspicions and stories. The proportion of parents who chose not to immunize their children despite this being a condition of school entry has increased significantly in some areas. (21) Controversy on this issue has continued despite an Institute of Medicine review that found the evidence favors rejection of a causal relationship between MMR vaccine and autism, based on at least ten studies. (22)

Physicians in our survey reported an estimated rate of vaccination of greater than 70% among pregnant women, which is much higher than the nationally estimated rate of 13%. (11) The likely reason for this discrepancy is that the vaccination rates represent a select group of physicians who responded to the survey, and the vaccination rates were estimated by physicians, and not validated. There are additional common barriers that prevent higher rates of vaccination despite the benefits that the influenza vaccine offers pregnant women. Such barriers include inadequate reimbursement, lack of patient-oriented vaccine information, liability concerns, and even patient refusal. One study reported that 14% of obstetricians surveyed believed that pregnant women did not need the influenza vaccine at all. (12) Physician-patient counseling also plays an important role in influenza vaccine administration. A discussion of how the neonate could benefit from the intervention is a stronger predictor of the patient accepting the vaccine than a physician recommendation by itself. (5) Wide discrepancies may exist between what is said by the practitioner about the influenza vaccination and what is perceived by the patient. In one study, 75% of physicians reported discussing influenza vaccination with their patients, but only 25% of the patients recalled that discussion. (5)

Several potential limitations of this study should be considered. The population of obstetricians surveyed is small, so variations in opinion may have a large effect on statistical parameters. The inherent flaw in voluntary surveys is that the most favorably practicing respondents may be the largest percentage of those to respond. Therefore, it may be difficult to obtain an accurate reflection of actual practices. We only surveyed the practice and opinions from physicians in the ACOG group, not including family physicians, nurse practitioners, and nurse midwives practicing obstetrics. Therefore, our results may not be representative of all those providers practicing obstetrics around the survey region.

Conclusion

Pregnant women infected with the influenza virus are at high risk for serious complications. Influenza vaccination provides an effective and safe way to protect pregnant women from influenza virus infection. However, practicing obstetricians have differing opinions from ACOG and ACIP guidelines regarding the timing of influenza vaccination of pregnant women, which may impact vaccination rates among pregnant women. A greater understanding of actual practices and opinions of both healthcare providers and patients is needed to impact vaccine policy and aid in improving vaccination rates. The barriers that are impeding progress, if found to be modifiable, could be addressed by physician education, patient education, and/or public health policy.

References

1. Bridges CB, Fukuda K, Uyeki TM, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2002;51:1-31.

2. Neuzil KM, Griffin MR, Schaffner W. Influenza vaccine: issues and opportunities. Infect Dis Clin North Am 2001;15:123-141.

3. Neuzil KM, Reed GW, Mitchel EF, et al. Impact of influenza on acute cardiopulmonary hospitalizations in pregnant women. Am J Epidemiol 1998;148:1094-1102.

4. Sur DK, Wallis DH, O'Connell TX. Vaccinations in pregnancy. Am Fam Physician 2003;68:299-304.

5. Silverman NS, Greif A. Influenza vaccination during pregnancy: patients' and physicians' attitudes. J Reprod Med 2001;46:989-994.

6. Englund JA. Maternal immunization with inactivated influenza vaccine: rationale and experience. Vaccine 2003;21:3460-3464.

7. Greenberg M, Jacobziner H, Pakter J, et al. Maternal mortality in the epidemic of Asian influenza, New York City, 1957. Am J Obstet Gynecol 1958;76:897-902.

8. Hartert TV, Neuzil KM, Shintani AK, et al. Maternal morbidity and perinatal outcomes among pregnant women with respiratory hospitalizations during influenza season. Am J Obstet Gynecol 2003;189:1705-1712.

9. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 1997;46:1-25.

10. Harper SA, Fukuda K, Uyeki TM, et al. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2004;53:1-40. Available at: http://www.cdc.gov/mmwr/preview/mmwrhtml/rr53e430a1.htm. Accessed July 11, 2006.

11. CDC. National Health Interview Survey: 2003. Table: Self-reported influenza vaccination coverage trends 1989-2003 among adults by age group, risk group, race/ethnicity, health-care worker status, and pregnancy status, United States. National Health Interview Survey. Available at: http://www.cdc.gov/flu/professionals/vaccination/pdf/vaccinetrend.pdf. Accessed July 11, 2006.

12. Schrag SJ, Arnold KE, Mohle-Boetani JC, et al Prenatal screening for infectious diseases and opportunities for prevention. Obstet Gynecol 2003;102:753-760.

13. Influenza vaccination in pregnancy: practices among obstetrician-gynecologists: United States, 2003-04 influenza season MMWR Morb Mortal Wkly Rep 2005;54:1050-1052.

14. Munoz FM, Englund JA. Vaccines in pregnancy. Infect Dis Clin North Am 2001;15:253-271.

15. Munoz FM, Greisinger AJ, Wehmanen OA, et al. Safety of influenza vaccination during pregnancy. Am J Obstet Gynecol 2005; 192:1098-1106.

16. Englund JA, Mbawuike IN, Hammill H, et al. Maternal immunization with influenza or tetanus toxoid vaccine for passive antibody protection in young infants. J Infect Dis 1993;168:647-656.

17. Chambers K. Asthma education and outcomes for women of childbearing age. Case Manager 2003;14:58-61.

18. Wilcox AJ, Weinberg CR, O'Connor JF, et al. Incidence of early loss of pregnancy. N Engl J Med 1988;319:189-194.

19. Simpson JL. Fetal wastage. In: Gabbe SG, Niebyl JR, Simpson JL, eds. Obstetrics: Normal and Problem Pregnancies. New York, Churchill Livingstone, 2002.

20. Simpson JL, Mills JL, Holmes LB, et al. Low fetal loss rates after ultrasound-proved viability in early pregnancy. JAMA 1987;258:2555-2557.

21. Fitzpatrick M. MMR: risk, choice, chance. Br Med Bull 2004;69:143-153.

22. Institute of Medicine. Immunization Safety Review: Vaccines and Autism. Washington, DC, The National Academies Press, 2004.

It takes less time to do a thing right, than it does to explain why you
did it wrong.
--Henry Wadsworth Longfellow

Pingsheng Wu, PhD, Marie R. Griffin, MD, MPH, Airron Richardson, MD, Steven G. Gabbe, MD, Meredith A. Gambrell, BS, and Tina V. Hartert, MD, MPH

From the Department of Medicine and the Division of Allergy, Pulmonary and Critical Care Medicine; Department of Preventive Medicine; and the Department of Obstetrics and Gynecology, Vanderbilt University School of Medicine, Nashville, TN.

Reprint requests to T.V. Hartert, MD, MPH, Center for Lung Research, Center for Health Services Research, 6107 MCE, Vanderbilt University School of Medicine, Nashville, TN 37232. Email: [e-mail]

Accepted April 25, 2006.

RELATED ARTICLE: Key Points

* In this urban cohort of obstetricians, 89% of responding obstetricians reported that they routinely recommend influenza vaccination to their pregnant patients. These obstetricians estimated that 70% of pregnant women in their practices received influenza vaccine each year during two influenza seasons (2002-2004).

* Physicians reported their preference for earliest influenza vaccine administration for healthy pregnant women to be the second trimester (62%), the first trimester (32%), or no vaccination at all throughout pregnancy (6%). For high-risk pregnant women, their preference was the second trimester (54%) or the first trimester (46%).

* This study suggests that the preferences of obstetricians regarding timing of influenza vaccination of pregnant women differ from the Advisory Committee on Immunization Practices (ACIP) recommendations. While these preferences may affect vaccine implementation among pregnant women, obstetricians have practical and valid concerns that should also be considered in developing vaccine education and guidelines.

* An understanding of actual practices and opinions of healthcare providers is needed to guide policy and improve vaccination rates.

Table 1. Demographics and practice characteristics of obstetricians in
Nashville, TN, 2003-2004

Characteristics                                        Response (n=37)

Demographics of survey respondents
  Median age (36) (a)                                   48 (42-54) (b)
  Male gender (%)                                       65
  Race (36) (a)
    White (%)                                           86
    Black (%)                                           11
    Asian (%)                                            3

Practice Characteristics
  Years in obstetrical practice                         17 (12-21) (b)
  Practice time committed to obstetrics (%)             50 (40-60) (b)
  Primary care provider (% of patients in practice)     40 (20-50) (b)
  Deliveries performed in year 2003 (33) (a)           120 (100-150) (b)
  Work hours per week practicing clinical medicine      58 (42.5-60) (b)
    (36) (a)
  Number of providers in primary practice (36) (a,c)     5 (3-7) (b)
  Private practice (%)                                  70

Patient Population Characteristics
  Racial/ethnic distribution (36) (a,c)
    White (%)                                           73 (60-75) (b)
    Black (%)                                           20 (18-28) (b)
    Other (d) (%)                                        9.5 (5-15) (b)
  Patients in practice covered by Medicaid (35) (a)      5 (0-35) (b)
    (%)
  Patients in practice with chronic medical condition   10 (5-40) (b, e)
    (34) (a) (%)

(a) Values in parentheses are numbers of respondents.
(b) Median (IQR).
(c) Percents do not add to 100 because each number is the median (IQR)
of racial/ethnic estimations from all survey respondents.
(d) Other includes Hispanic, Asian, and Native American.
(e) Includes high-risk obstetric conditions.

Table 2. Practice patterns of obstetricians regarding influenza vaccine
administration during pregnancy in Nashville, TN, 2003-2004

Influenza vaccination practices                    Response % (n=37)

Office guidelines in place                          68
Routinely recommend vaccine to pregnant patients    89
Practice administers influenza vaccine              73
Physician practices regarding influenza vaccine
  administration (27) (a)
  Offer the vaccine to OB and postpartum patients  100
  Offer to GYN patients                             59
  Referred elsewhere                                15
When vaccine administered (27) (a)
  Scheduled visit                                  100
  Nurse-only visit                                  33
  Standing order for drop-in                        19
  Influenza vaccine administration times/clinics     4
Estimated percentage of pregnant women who were
  vaccinated
  Year 2002-2003 (25) (a)                           70 (30-80) (b)
  Year 2003-2004 (24) (a)                           73 (45-80) (b)

(a) Values in parentheses are numbers of respondents.
(b) Median (IQR).