Survey of congenital cytomegalovirus (cCMV) knowledge among medical students.

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Journal of Clinical Virology xxx (2014) xxx–xxx

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Survey of congenital cytomegalovirus (cCMV) knowledge among medical students H.R. Baer ∗ , H.E. McBride 1 , A.C. Caviness 2 , G.J. Demmler-Harrison 1 Department of Pediatrics, Baylor College of Medicine, Houston, TX, United States

a r t i c l e

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Article history: Received 9 February 2014 Received in revised form 13 March 2014 Accepted 31 March 2014 Keywords: Cytomegalovirus Knowledge Congenital infection Medical education

a b s t r a c t Background: Congenital cytomegalovirus (cCMV) is a leading cause of congenital infection worldwide and the most common congenital infection in the United States, affecting 30,000–40,000 US newborns each year and causing permanent disabilities in 8000–10,000. In contrast to how commonly it occurs, physicians and medical students have little knowledge of cCMV. Objectives: To test the hypothesis medical students have little awareness about cCMV infection, and to collect data on medical students’ knowledge about cCMV. The long-term goal of this project is to establish medical student awareness of cCMV infection and educate students about available treatments and strategies for prevention in at-risk populations. Study design: Medical students at one institution were surveyed by questionnaire to assess their knowledge of cCMV. Responses were described, quantified, and compared between groups. Results: 751 surveys were sent and 422 completed responses were received. Respondents were well distributed over all 4 medical school (MS) class years. Only 34% MS1 had heard of cCMV compared to 100% MS2-4 (P < 0.0001). All MS2-4 who reported being “very familiar” with CMV learned about it in medical school, 80% in one lecture. MS1 respondents were significantly less knowledgeable about cCMV than MS2-MS4 respondents. Conclusion: A baseline lack of knowledge about cCMV was documented in first year medical students. A sharp increase in knowledge of cCMV occurred between MS1 and MS2 years, likely due to preclinical medical student curriculum. However, significant knowledge gaps regarding transmission and treatment were observed in all MS years, representing opportunities for medical education. © 2014 Elsevier B.V. All rights reserved.

1. Background Congenital cytomegalovirus (cCMV) is a leading cause of congenital infection worldwide and is the most common congenital infection in the United States (US). In industrialized countries, with relatively lower overall maternal CMV seroprevalence (50–70%), an average of 0.4–1.2% of newborns are congenitally infected with

Abbreviations: cCMV, congenital cytomegalovirus; MS, medical student; MS1, first-year medical student; MS2-4, second through fourth year medical students. ∗ Corresponding author at: 8181 Fannin St. #1222, Houston, TX 77054, United States. Tel.: +1 318 557 0491. E-mail addresses: [email protected], [email protected] (H.R. Baer), [email protected] (H.E. McBride), [email protected] (A.C. Caviness), [email protected] (G.J. Demmler-Harrison). 1 Address: Feigin Center Suite 1150, 1102 Bates Street, Houston, TX 77030, United States. Tel.: +1 832 824 4330; fax: +1 832 825 4347. 2 Address: 26621 Fannin St., MC 1-1481, Houston, TX 77030-2399, United States. Tel.: +1 832 824 6461; fax: +1 832 824 5425.

CMV, and in developing nations, with usually higher CMV seroprevalence (over 80%), higher rates between 1 and 5% of cCMV infection have been documented [1]. In the US, approximately 40,000 newborns annually are diagnosed with cCMV, resulting in an estimated 400 deaths and leaving another 8000–10,000 with permanent disabilities including hearing loss, vision loss, intellectual disability, and seizures [2]. The highest risk of transmission and serious disease to the fetus occurs during a primary CMV infection of the mother; however, the fetus can also be affected by maternal CMV reactivation or reinfection with a different strain, causing sequelae in the newborn and child. An important route of CMV infection in pregnant women is contact with young children’s saliva or urine (e.g. diapers, toys, silverware, kissing) [3]. Prenatal hygiene counseling has been shown to decrease maternal CMV infection and therefore the risk of transmitting CMV to the fetus [4]. A CMV vaccine would also likely provide protection against CMV infections, but a vaccine is not yet licensed, leaving behavior measures as the only method available to reduce maternal CMV infection during pregnancy. Treatment with

http://dx.doi.org/10.1016/j.jcv.2014.03.023 1386-6532/© 2014 Elsevier B.V. All rights reserved.

Please cite this article in press as: Baer HR, et al. Survey of congenital cytomegalovirus (cCMV) knowledge among medical students. J Clin Virol (2014), http://dx.doi.org/10.1016/j.jcv.2014.03.023

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Fig. 1. Questionnaire administered to medical students.


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antiviral medications, ganciclovir and valganciclovir, have been shown in published randomized clinical trials to improve hearing and neurodevelopmental outcomes in newborns with congenital CMV disease [14]. Unfortunately, despite this knowledge among CMV experts, the general population has little awareness of cCMV [4–9] and this lack of awareness extends to the medical profession as well [10–13]. 2. Objectives The purpose of this study was to assess US medical students’ knowledge of cCMV transmission, prevention and treatment, at one institution, and to identify knowledge gaps that represent opportunities for medical education. 3. Study design Medical students at one institution were surveyed by electronic questionnaire, which was developed by the authors and conducted

using the online Survey Monkey® program. The 10-minute questionnaire (Fig. 1) contained questions about cCMV manifestations, transmission, prevention, treatment options, and the medical students’ source of cCMV knowledge (if applicable), as well as basic demographic information. An email invitation to participate in the survey was sent to all medical students (MS) in all classes (year one through four) enrolled at one institution in the US (Baylor College of Medicine, Houston, Texas). The prospective participants were not told that cCMV was the primary topic of the study, but that they were being surveyed about general medical knowledge. The online questionnaire remained open for three months and was timed so that, based on the school’s curriculum, first year students (MS1s) had not yet encountered cCMV in didactic lecture but second year students (MS2s) had encountered exposure to cCMV in at least one didactic lecture. As an incentive, MS respondents who completed the survey were offered a $10 gift card. Responses were analyzed descriptively and also compared between MS year classes.




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Table 1 Demographics of medical students (N-422), by year of medical school, who adequately responded to congenital CMV awareness and knowledge survey. MS1 (n = 143) Gender Male Female Age group 18–24 years 25–34 years 35–44 years Ethnicity (mark all that apply) Asian Black/African-American Hispanic/Latino Native American/Alaskan native Native Hawaiian/Pacific Islander White Other Marital status Single Married Life partner Parents Contact with children Never Less than 1 day/week 1–2 days 3–4 days 5–7 days

MS2 (n = 117)

MS3 (n = 84)

MS4 (n = 78)

Total (n = 422)

71 72

56 61

48 36

37 41

212 210

128 14 1

87 30 0

40 44 0

7 71 0

262 159 1

49 8 11 2 0 77 5

39 4 18 0 0 72 1

33 2 4 0 0 50 1

18 5 15 1 0 44 3

139 19 48 3 0 243 10

127 12 4

100 15 2

67 12 5

65 12 1

359 51 12

4

3

5

1

13

40 80 16 3 4

30 71 10 2 4

16 48 9 2 9

7 48 13 4 6

93 247 48 11 23

4. Results Survey invitations were emailed to 751 students, with 503 initial responses. There were 50 responders who did not finish the survey and an additional 31 were duplicate responses, leaving 422 (56%) complete, original responses included in the analysis (Fig. 2). For the 31 individuals who completed the survey twice, only the first recorded response was included. Demographic characteristics are reported in Table 1; gender and ethnicity distribution adequately reflects the school’s demographics as reported in its enrollment statistics. The percentage of each class that responded was estimated as follows: approximately 75% of all MS1, 62% of all MS2, 48% of all MS3, and 41% of all MS4 completed the survey. Only 48 (34%)

MS1 respondents had heard of congenital CMV compared to 100% MS2-4 (P < 0.0001, Fig. 3). Significant differences were observed between MS1 and MS2 students and there were no statistically significant differences or trends among MS2, MS3, and MS4 students. Accordingly, MS2-4 responses were grouped together for the purposes of this analysis. MS1 respondents were significantly less knowledgeable about cCMV transmission than MS2-MS4 respondents: 18% MS1 vs. 94% MS2-4 students knew cCMV caused disease in the fetus and newborn; 6% MS1 vs. 15% MS2-MS4 knew CMV can be contracted by contact with wet diapers; 11% MS1 vs. 58% MS2-4 were aware CMV can be transmitted by kissing; 13% MS1 vs. 44% MS2-4 knew CMV was transmitted by sharing food or drink; 20% MS1 vs. 81% MS2 –4 knew CMV was transmitted by blood transfusion (Table 2). A similar pattern was observed for knowledge of cCMV manifestations. 20% MS1 vs. 83% MS2-4 believed cCMV can cause asymptomatic infection, 12% MS1 vs. 84% MS2-4 knew cCMV can cause developmental disabilities, 7% MS1 vs. 78% MS2-4 knew cCMV can cause hearing loss, 9% MS1 vs.77% MS2-4 knew cCMV can cause vision loss, and 13% MS1 vs. 81% MS2-4 knew it can be fatal. Of all respondents, 32% incorrectly believed cCMV was associated

Self-Reported Familiarity With Congenital CMV

Percent of respondents

100 80 MS1

60

MS2

40

MS3 20

MS4

0 Never heard of it Fig. 2. Flow chart of congenital CMV knowledge survey administered to first, second, third and fourth year medical students.

Not very familiar

Somewhat Very familiar familiar

Fig. 3. Bar graph depicting self-reported knowledge and awareness of congenital CMV according to medical school year.


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H.R. Baer et al. / Journal of Clinical Virology xxx (2014) xxx–xxx Table 2 Comparison between medical student classes of knowledge and awareness of modes of CMV transmission. MS1 (n = 143) n (%)

MS2-4 (n = 279) n (%)

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Table 3 Comparison between medical student classes of knowledge and awareness about signs and symptoms and outcomes associated with congenital CMV infection. MS1 (n = 143) n (%)

MS2-4 (n = 279) n (%)

Contact with cat litter

Yes No Don’t know

5 (3) 15 (10) 123 (86)

11 (4) 240 (86) 28 (10)

Silent or asymptomatic infection

Yes No Don’t know

20 (14) 1 (1) 122 (85)

232 (83) 15 (5) 32 (11)

Contact with rodents

Yes No Don’t know

5 (3) 14 (10) 124 (87)

7 (3) 226 (81) 46 (16)

Heart defect

Yes No Don’t know

11 (8) 3 (2) 129 (90)

126 (45) 74 (27) 79 (28)

Contact with birds

Yes No Don’t know

3 (2) 15 (10) 125 (87)

9 (3) 229 (82) 41 (15)

Developmental disabilities

Yes No Don’t know

17 (12) 1 (1) 125 (87)

233 (84) 12 (4) 34 (12)

Contact with wet diapers

Yes No Don’t know

9 (6) 10 (7) 124 (87)

43 (15) 169 (61) 67 (24)

Hearing loss

Yes No Don’t know

10 (7) 2 (1) 131 (92)

218 (78) 26 (9) 35 (13)

Coughing or sneezing

Yes No Don’t know

19 (13) 10 (7) 114 (80)

145 (52) 83 (30) 51 (18)

Vision loss

Yes No Don’t know

13 (9) 2 (1) 128 (90)

216 (77) 23 (8) 40 (14)

Sharing eating utensils

Yes No Don’t know

15 (10) 11 (8) 117 (82)

123 (44) 106 (38) 50 (18)

Cleft lip or palate

Yes No Don’t know

4 (3) 7 (5) 132 (92)

42 (15) 139 (50) 98 (35)

Eating undercooked meat

Yes No Don’t know

2 (1) 15 (11) 126 (88)

5 (2) 245 (88) 29 (10)

Seizures

Yes No Don’t know

11 (8) 4 (3) 128 (90)

183 (66) 29 (10) 67 (24)

Kissing someone

Yes No Don’t know Yes No Don’t know

16 (11) 12 (8) 115 (80) 18 (13) 11 (8) 114 (80)

162 (58) 80 (29) 37 (13) 141 (51) 93 (33) 45 (16)

Microcephaly

Yes No Don’t know

12 (8) 3 (2) 128 (90)

206 (74) 25 (9) 48 (17)

Brain calcifications

Yes No Don’t know

6 (4) 4 (3) 133 (93)

137 (49) 78 (28) 64 (23)

Blood transfusions

Yes No Don’t know

29 (20) 1 (1) 113 (79)

227 (81) 23 (8) 29 (10)

Enlarged liver and spleen

Yes No Don’t know

16 (11) 0 127 (89)

186 (67) 28 (10) 65 (23)

Organ or marrow transplant

Yes No Don’t know

24 (17) 3 (2) 116 (81)

239 (86) 14 (5) 26 (9)

Thrombocytopenia

Yes No Don’t know

10 (7) 4 (3) 129 (90)

128 (46) 51 (18) 100 (36)

Sexual intimacy

Yes No Don’t know

28 (20) 4 (3) 111 (78)

155 (56) 79 (28) 45 (16)

Death

Yes No Don’t know

18 (13) 0 125 (87)

226 (81) 15 (5) 38 (14)

Sharing food or drink

with heart defects (8% MS1 vs. 45% MS2-4) and 11% (3% MS1 vs. 15% MS2-4) incorrectly answered cCMV was associated with cleft lip or palate. MS1 students were more likely to answer “don’t know” than their MS2-4 colleagues (Table 3). In addition, 87% MS1 vs. 32% MS24 did not know whether drug treatment exists for cCMV, and 26% MS2-4 believed there was no treatment. However, when prompted, 48% MS2-4 were able to correctly identify ganciclovir as a potential treatment, while 30% incorrectly believed acyclovir was effective and 16% answered cidofovir was effective (Table 4). 90% MS1 and 30% MS2-4 did not know whether a licensed vaccine exists to prevent cCMV. 7% MS1 vs. 62% MS2-4 correctly responded that no vaccine currently exists (Table 5). All MS2-4 who reported being “very familiar” with cCMV learned about it in medical school, 80% in lecture. 12% of all MS2-4 also encountered patients with congenital CMV in their clinical rotations (Table 6). Additionally, 43 (15%) MS2-4 reported learning about cCMV at some point during medical school but not from lecture, patients, or research. Of these, 39 were unable or unwilling to specify where they encountered it and 4 covered it during independent study.

Table 4 Comparison between medical student classes of knowledge of treatment options for cCMV.

Acyclovir Amphotericin Ampicillin Cidofovir Foscarnet Ganciclovir Ritonavir Valacyclovir Valganciclovir Vitamin A Don’t know None, there is no treatment for this disease

MS2-4 (n = 279) n (%)

9 (6) 1 (1) 1 (1) 6 (4) 1 (1) 8 (6) 7 (5) 8 (6) 9 (6) 2 (1) 130 (91) 3 (2)

78 (30) 1 (0.4) 0 45 (16) 77 (28) 133 (48) 16 (6) 66 (24) 71 (25) 2 (1) 63 (23) 2 (1)

Table 5 Responses to the question, “Is there a licensed vaccine to prevent congenital CMV?”.

5. Discussion A limitation of this study is that we used a convenience sample of students at a single medical school, which may not necessarily reflect the situation in other institutions. Furthermore, since our

MS1 (n = 143) n (%)

Yes No Don’t know

MS1 (n = 143) n (%)

MS2-4 (n = 279) n (%)

4 (3) 10 (7) 129 (90)

20 (7) 174 (62) 85 (30)


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20 Table 6 Students’ sources of knowledge about congenital CMV.

Magazine or newspaper TV or radio Internet Friends or relatives Family physician Internal medicine doctor OB/GYN High school College Medical school Lecture Patient(s) Research Other Not sure I am not familiar with congenital cytomegalovirus (CMV) Other (please specify)

MS1 (n = 143) n (%)

MS2-4 (n = 279) n (%)

1 (0.7) 1 (0.7) 2 (1.4) 1 (0.7) 0 2 (1.4) 1 (0.7) 0 4 (2.8) 8 (5.6) 6 (4.2) 0 0 2 (1.4) 8 (5.6) 123 (86.0)

2 (1) 0 18 (6) 6 (2) 2 (1) 6 (2) 15 (5) 1 (0.4) 7 (3) 270 (97) 227 (87) 33 (12) 8 (3) 17 (6) 5 (2) 10 (4)

4 (2.8)

4 (1)

institution is known for work on cCMV, it is possible that our results might actually overestimate cCMV knowledge among US medical students. However, since the co-authors with expertise in CMV do not have formal influence over the medical school curriculum for students, the influence of their expertise is likely to be small or nil. Nevertheless, this survey identified several gaps in cCMV knowledge among college-educated individuals entering medical school, and for medical students continuing their medical school education. Of beginning MS1 students (who at the time of the survey had not yet encountered cCMV in medical school coursework), only 34% had heard of cCMV. For comparison, this is slightly better than the rate of awareness among the general population of collegeeducated women. The 2005 Healthstyles survey found 22% of US college graduates were aware of cCMV [5], which dropped to 15% in the 2010 survey [6]. Another multi-state survey reported 31% of respondents who had at least a bachelor’s degree had heard of cCMV [7]. Our study suggests that even among entering US medical students—a highly motivated, educated population, all with at least an undergraduate degree—the awareness of cCMV is low at baseline. This finding is quite out of proportion to the extent of the problem, as cCMV is the most common congenital infection and affects tens of thousands of newborns each year. The sharp increase in awareness and knowledge between MS1 and MS2 years is likely accounted for by the school’s preclinical infectious disease course occurring at the end of MS1 year. However, this remained the sole source of cCMV knowledge for the vast majority of students, even MS4s. Other studies have documented a worldwide lack of knowledge among medical professionals disproportionate to the incidence of the disease. A 2007 survey of practicing US obstetricians showed that only 57% were aware sharing utensils is a route for cCMV transmission and 55% knew it can be acquired through contact with saliva [12]. A survey of practicing physicians in the Netherlands found only 52% knew CMV can be transmitted by kissing and 23% were aware it can be acquired from contact with wet diapers [10]. More recently, a similar survey of physicians and midwives in France revealed that although 81% of respondents were aware cCMV can be acquired from kissing, 68% were aware of transmission via contact with wet diapers and only 5% of physicians surveyed were able to correctly identify all hygiene recommendations to prevent infection [11]. Another study from Germany found that only 20% of midwives surveyed felt well-informed about cCMV, and only one-third were able to state measures that reduce infection risk [13]. Our survey both confirms

those findings and suggests the root cause may be lack of education about cCMV. The risk of acquiring CMV during pregnancy can be significantly decreased by specific behavioral changes (e.g. wash hands after contact with wet diapers, avoid sharing food and utensils, avoid kissing young children on the mouth) [4]. One prospective study showed a decrease in the rate of CMV seroconversion after pregnant women were given 5–10 min of hygiene counseling about cCMV [4]. Despite this knowledge, the CDC reported in 2008 that less than half (44%) of US obstetricians routinely counsel patients about cCMV [12]. Treatment of cCMV with intravenous ganciclovir or oral valganciclovir therapy has been shown to reduce the risk of hearing loss progression, reduce developmental delays, and improve head circumference growth in symptomatic newborns [14]. In our survey, 58% MS2-4 either did not know whether there is an available treatment, or responded that no treatment exists. This finding represents another important gap in cCMV knowledge. It is essential that physicians are aware of the modes of CMV transmission in order to properly counsel their patients. However, the most significant knowledge gaps identified in our study were in the areas of cCMV transmission and treatment. Most concerning was that only 15% of upperclassmen recognized cCMV can be contracted from contact with wet diapers and less than half were aware it can be spread by sharing food or drink. In addition, 45% MS2-4 incorrectly answered cCMV can cause heart defects, suggesting that the reported knowledge of cCMV manifestations may actually be overestimated in this survey. Another noteworthy finding was knowledge of cCMV increases dramatically between MS1 and MS2 years, then plateaus. Although differences between MS2, MS3, and MS4 in this study were not statistically significant, Fig. 3 seems to suggest that some knowledge gained during MS2 year may be temporarily lost in MS3 but recovered by MS4 year, possibly through direct clinical experience, studying for clinical rotations, or board exam preparation. This would seem to indicate that further educational efforts about cCMV should target the clinical years, particularly in specialties such as family practice, OB/GYN, and pediatrics which involve the care of women and children. Funding Research supported by CMV Research Fund, Department of Pediatrics, Baylor College of Medicine. Competing interests The authors have no competing interests to declare. Ethical approval Ethical approval obtained from the Institutional Review Board for Baylor College of Medicine and Affiliated Hospitals, protocol H-30346 References [1] Manicklal S, Emery VC, Lazzarotto T, Boppana SB, Gupta RK. The “silent” global burden of congenital cytomegalovirus. Clin Microbiol Rev 2013;26(January (1)):86–102. [2] Cannon M, Davis K. Washing our hands of the congenital cytomegalovirus disease epidemic. BMC Public Health 2005;June (5):70. [3] Nyholm J, Schleiss M. Prevention of maternal cytomegalovirus infection: current status and future prospects. Int J Womens Health 2010;2:23–35. [4] Vauloup-Fellous C, Picone O, Cordier A, Parent-du-Châtelet I, Senat M, Frydman R, et al. Does hygiene counseling have an impact on the rate of CMV primary infection during pregnancy? Results of a 3-year prospective study in a French hospital. J Clin Virol 2009;46(December (Suppl. 4)):S49–53.




[5] Ross D, Victor M, Sumartojo E, Cannon M. Women’s knowledge of congenital cytomegalovirus: results from the 2005 HEALTHSTYLES survey. J Womens Health 2008;17(June (5)):849–58. [6] Cannon M, Westbrook K, Levis D, Schleiss M, Thackeray R, Pass R. Awareness of and behaviors related to child-to-mother transmission of cytomegalovirus. Prev Med 2012;54(May (5)):351–7. [7] Jeon J, Victor M, Adler SP, Arwady A, Demmler G, Fowler K, et al. Knowledge and awareness of congenital cytomegalovirus among women. Infect Dis Obstet Gynecol 2006:80383. [8] Cordier AG, Guitton S, Vauloup-Fellous C, Grangeot-Keros L, Ayoubi JM, Benachi A, Picone O. Awareness of cytomegalovirus infection among pregnant women in France. J Clin Virol 2012;53(April [4]):332–7. [9] Lim SL, Tan WC, Tan LK. Awareness of and attitudes toward congenital cytomegalovirus infection among pregnant women in Singapore. Int J Gynaecol Obstet 2012;117(June [3]):268–72. [10] Korver A, de Vries J, de Jong J, Dekker F, Vossen A, Oudesluys-Murphy A. Awareness of congenital cytomegalovirus among doctors in the Netherlands. J Clin Virol 2009;46(December [Suppl. 4]):S11–5.

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[11] von Gartzen A, Hollins Martin C. An email survey of midwives knowledge about CytoMegaloVirus (CMV) in Hannover and a skeletal framework for a proposed teaching program. Nurse Educ Pract 2012 December. pii:S14715953(12)00207-7. [12] Centers for Disease Control and Prevention. Knowledge and practices of obstetricians and gynecologists regarding cytomegalovirus infection during pregnancy – United States, 2007. MMWR Weekly 2008;57(January (03)): 65–8. [13] Cordier AG, Guitton S, Vauloup-Fellous C, Grangeot-Kero L, Benachi A, Picone O. Awareness and knowledge of congenital cytomegalovirus infection among health care providers in France. J Clin Virol 2012 Oct;55(2): 158–63. [14] Oliver S, Cloud G, Sánchez P, Demmler G, Dankner W, Shelton M, et al. Neurodevelopmental outcomes following ganciclovir therapy in symptomatic congenital cytomegalovirus infections involving the central nervous system. J Clin Virol 2009;46(December (Suppl. 4)):S22–6.


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