Toxoplasmosis-related knowledge and practices among pregnant women in the United States Jeffrey L. Jones 1 , Folashade Ogunmodede 2 , Joni Scheftel 2 , Elizabeth Kirkland 1 , Adriana Lopez 1 , Jay Schulkin 3 and Ruth Lynfield 2 1 Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 2 Acute Disease Investigation and Control Section, Minnesota Department of Health, Minneapolis, MN 3 Department of Research, American College of Obstetricians and Gynecologists, Washington, DC Background: Infection with Toxoplasma gondii during pregnancy can lead to severe illness in the fetus. Many T. gondii infections are preventable by simple hygienic measures. Methods: We surveyed pregnant women in the US to determine their knowledge about toxoplasmosis and their practices to prevent infection. Volunteer obstetricians selected to be demographically representative of the American College of Obstetricians and Gynecologists recruited the participants. Results: Of 403 women responding to the survey, 48% indicated that they had heard or seen information about toxoplasmosis; however, only 7% were aware of being tested for the disease. Forty percent of responding women knew that toxoplasmosis is caused by an infection, but 21% thought that a poison causes it. The highest level of knowledge was about cats and T. gondii; 61% responded that the organism is shed in the feces of infected cats and 60% responded that people could acquire toxoplasmosis by changing cat litter. There was a low level of knowledge about other risk factors; only 30% of the women were aware that T. gondii may be found in raw or undercooked meat. Nevertheless, a high percentage of women indicated that they do not eat undercooked meat during pregnancy and that they practice good hygienic measures such as washing their hands after handling raw meat, gardening or changing cat litter. Conclusion: Except for the risk of transmission from cats, knowledge among pregnant women about toxoplasmosis is low. However, toxoplasmosis-preventive practices are generally good, suggesting that providers should continue to offer education about practices that help prevent foodborne diseases in general as well as information about preventing toxoplasmosis specifically. Key words: PREVENTION; SURVEY; RISK FACTORS; TOXOPLASMOSIS Infection with Toxoplasma gondii during pregnancy can lead to severe illness in the fetus and infant including central nervous system and ocular dis- ease, and even death 1 . Based on local and regional studies, the Centers for Disease Control and Prevention (CDC) estimates that there are 400–4000 cases of congenital toxoplasmosis per year 2 and that toxoplasmosis is the third leading cause of foodborne deaths in the US 3 . Population-based studies in the US have shown that most (85%) pregnant women are susceptible to infection with T. gondii 4 . Many congenital T. gondii infections acquired during gestation are preventable by simple precautions during Infect Dis Obstet Gynecol 2003;11:139–145 Correspondence to: Jeffrey L. Jones, MD, MPH, Division of Parasitic Diseases, Centers for Disease Control and Prevention, NCID, Mailstop F-22, 4770 Buford Highway NE, Atlanta, GA 30341-3724, USA. Email: [email protected]2003 The Parthenon Publishing Group 139 9 Z:\Customer\PARTHEN\IDOG\A4625 - IDOG Vol 11 No 3 - September 2003.vp 06 November 2003 15:35:02 Color profile: Disabled Composite Default screen
Transcript
Toxoplasmosis-related knowledge and practices amongpregnant women in the United States
Jeffrey L. Jones1, Folashade Ogunmodede2, Joni Scheftel2, Elizabeth Kirkland1,Adriana Lopez1, Jay Schulkin3 and Ruth Lynfield2
1Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control andPrevention, Atlanta, GA
2Acute Disease Investigation and Control Section, Minnesota Department of Health, Minneapolis, MN3Department of Research, American College of Obstetricians and Gynecologists, Washington, DC
Background: Infection with Toxoplasma gondii during pregnancy can lead to severe illness in the fetus. ManyT. gondii infections are preventable by simple hygienic measures.Methods: We surveyed pregnant women in the US to determine their knowledge about toxoplasmosis andtheir practices to prevent infection. Volunteer obstetricians selected to be demographically representative of theAmerican College of Obstetricians and Gynecologists recruited the participants.Results: Of 403 women responding to the survey, 48% indicated that they had heard or seen information abouttoxoplasmosis; however, only 7% were aware of being tested for the disease. Forty percent of responding womenknew that toxoplasmosis is caused by an infection, but 21% thought that a poison causes it. The highest level ofknowledge was about cats and T. gondii; 61% responded that the organism is shed in the feces of infected cats and60% responded that people could acquire toxoplasmosis by changing cat litter. There was a low level of knowledgeabout other risk factors; only 30% of the women were aware that T. gondii may be found in raw or undercookedmeat. Nevertheless, a high percentage of women indicated that they do not eat undercooked meat duringpregnancy and that they practice good hygienic measures such as washing their hands after handling raw meat,gardening or changing cat litter.Conclusion: Except for the risk of transmission from cats, knowledge among pregnant women abouttoxoplasmosis is low. However, toxoplasmosis-preventive practices are generally good, suggesting that providersshould continue to offer education about practices that help prevent foodborne diseases in general as well asinformation about preventing toxoplasmosis specifically.
Infection with Toxoplasma gondii during pregnancycan lead to severe illness in the fetus and infantincluding central nervous system and ocular dis-ease, and even death1. Based on local and regionalstudies, the Centers for Disease Control andPrevention (CDC) estimates that there are400–4000 cases of congenital toxoplasmosis
per year2 and that toxoplasmosis is the thirdleading cause of foodborne deaths in the US3.Population-based studies in the US have shownthat most (85%) pregnant women are susceptibleto infection with T. gondii4. Many congenitalT. gondii infections acquired during gestationare preventable by simple precautions during
Infect Dis Obstet Gynecol 2003;11:139–145
Correspondence to: Jeffrey L. Jones, MD, MPH, Division of Parasitic Diseases, Centers for Disease Control and Prevention,NCID, Mailstop F-22, 4770 Buford Highway NE, Atlanta, GA 30341-3724, USA. Email: [email protected]
2003 The Parthenon Publishing Group 139
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pregnancy. These precautions include fully cook-ing meat, not ingesting uncooked or undercookedmeat and not ingesting soil or water contaminatedwith cat feces (for example, soil from sand boxesand cat litter boxes, or soil on raw fruits andvegetables2).
In order to determine their knowledge abouttoxoplasmosis and the practices that preventinfection, the Department of Research of theAmerican College of Obstetricians and Gyne-cologists (ACOG), in collaboration with the CDCand the Minnesota Department of Health (MDH),surveyed pregnant women in the US. We presenthere the results of the survey and a discussion ofcongenital toxoplasmosis prevention.
METHODS
In the fall of 2002, the Department of Researchof ACOG asked physician members of itsCollaborative Ambulatory Research Network(CARN) to participate in the survey. The mem-bers of the network are practicing obstetrician-gynecologists who volunteer to participate insurveys implemented by the College. CARNmembers are chosen to be demographicallyrepresentative of all ACOG members by age andgender. The study was limited to obstetrician-gynecologists practicing in the US. Participatingphysicians were asked to recruit up to fivevolunteer pregnant women from their practiceto complete the survey.
The MDH developed the survey with inputfrom staff at the CDC and ACOG. Infectiousdisease physicians, public health physicians, healtheducators and laboratorians assisted in thedevelopment of the questionnaire. Demographicinformation was requested, followed by questionscovering general knowledge about toxoplasmosis,risk factors, symptoms and timing of infection,prevention knowledge and preventive behavior.The questionnaire took approximately 20 minutesto complete. Pilot testing was done at CDC(among non-medical staff) and by ACOGobstetricians. No personal identifiers wererecorded in the survey. The survey was reviewedand exempted by the MDH, ACOG and CDCinstitutional human subjects review boards.
The survey data were analyzed using techniquesfor random samples. Ninety-five percent confi-dence limits (CL) were calculated for proportions;the maximum 95% CL are given in a footnote toTable 2 (i.e. the maximum 95% CL calculated forany question). Because we collected zip codes andfelt that respondents may be more similar if theywere from the same zip code area, we also analyzedthe data as if it were collected by a one-stage clusterdesign with zip code being the primary samplingunit. Of the 327 unique zip codes recorded inthe survey, 287 (87.8%) had one respondent, 31(9.5%) had two respondents, 6 (1.8%) had threerespondents and 3 (0.9%) had four respondents.When the data were analyzed as a one-stage clusterdesign, the design effect was less than 1.2 indicatingthat clustering of responses by zip code did nothave a large effect on the variance. Nonetheless,we used 1.2 as a design effect when calculating themaximum 95% CL shown in the footnote toTable 2 (Clopper–Pearson method, StatXact 5software5). The stratified analysis was conductedwith EpiInfo6 software. Trends for categoricalvariables were analyzed with the chi-square fortrend and differences between categorical variableswere analyzed with the chi-square test.
RESULTS
Two hundred twenty-five CARN physicianmembers participated in the survey and recruited403 pregnant women. The median age of thepregnant women surveyed was 29 (range 12–49),the median duration of pregnancy was 30 weeks(range 1–40) and the median parity was 1 (range0–6); other characteristics of the study populationare shown in Table 1. Information was notcollected on the number of pregnant women whodeclined to participate. Respondents were welldispersed throughout the US by region, butwere more likely to be white, educated and live inrural locations than the general US population(Table 1).
Knowledge about toxoplasmosis and how toprevent it varied by topic, but in general therewas a great deal of uncertainty about the disease(Table 2). Only 7% of respondents indicated thatthey had been tested for toxoplasmosis; however,43% of respondents were uncertain if they had
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been tested. Only 40% of respondents were certainthat toxoplasmosis is caused by an infection and21% thought that a poison causes it. The highestlevel of knowledge was about cats and toxo-plasmosis, 61% indicated that toxoplasmosis(T. gondii) is shed in the feces of infected cats and60% indicated that people can be exposed totoxoplasmosis by changing cat litter. Respondentsalso seemed to be reasonably aware that pregnantwomen can develop serious complications afteracquiring toxoplasmosis (58%) and that unbornand newborn children can develop serious compli-cations from toxoplasmosis (56%).
There was a low level of knowledge about riskfactors for toxoplasmosis other than cat feces, asnoted by the following examples: only 30% ofrespondents indicated that the organism that
causes toxoplasmosis may be found in raw orundercooked meat, 26% indicated that peoplecan get toxoplasmosis by eating undercookedpork and 29% indicated that people can acquiretoxoplasmosis by gardening without gloves. Ingeneral, respondents were unsure of the answersto questions about the timing of infection andthe symptoms of toxoplasmosis in both themother and the infant (Table 2, symptoms andtiming of infection section). In addition, except foravoiding changing the cat litter box duringpregnancy, there was uncertainty about waysto avoid or prevent toxoplasmosis (Table 2,prevention knowledge section).
When we examined key questions about toxo-plasmosis, knowledge often increased with higherlevels of education and less frequently with age(Table 3). However, there was not as muchvariation in the level of knowledge by trimester ofpregnancy or parity (first pregnancy versus two ormore). The numbers were quite small in manyracial/ethnic categories, therefore we split theracial/ethnic groups into two categories: (i) white-nonHispanic and (ii) non-white or Hispanic.When examining the key questions in Table 3 byrace/ethnicity, a higher percentage of white-nonHispanic persons than non-white or Hispanicpersons had heard of toxoplasmosis (51% versus36%, p = 0.008), knew that toxoplasmosis can beprevented by cooking meat well (52% versus 37%,p = 0.015), knew that people can get toxo-plasmosis by gardening without gloves (34% versus17%, p = 0.002), knew that toxoplasmosis can beavoided by only feeding cats dry or commercial catfood and not letting them kill and eat rodents(34% versus 17%, p = 0.002) and knew thattoxoplasmosis can be prevented by thoroughlywashing and/or peeling all fruits and vegetablesbefore eating them (44% versus 29%, p = 0.014).There were no significant differences by region ofthe country.
Although in many topic areas there was a lack ofknowledge about toxoplasmosis, its symptoms andhow it is prevented, the women surveyedindicated that they practice behaviors that wouldprevent toxoplasmosis. Of the women responding,93% indicated that they routinely wash their handsafter gardening, 80% routinely washed their handsafter changing cat litter, 96% routinely washed
Toxoplasmosis and pregnant women Jones et al.
INFECTIOUS DISEASES IN OBSTETRICS AND GYNECOLOGY • 141
DemographicsStudy population
(%)US population*
(%)
Education**< High school graduateHigh school graduateSome collegeCollege graduateGraduate school
Residence location***RuralSuburbanUrban
RaceAmerican Indian/
Alaskan nativeAsian or Pacific IslanderBlackWhiteOther
EthnicityHispanic
US regionNortheastSouthMidwestWest
117283717
335315
< 1
59
797
9
17392817
11312229
7
205030
< 1
41275
8
13
19362322
*2000 Census, n = 281 421 906; **for US population, educationfor women 20–49 years of age, n = 61 219 000; ***for USpopulation, categories are: central city, metropolitan statisticalarea (MSA) outside of central city, and non-MSA
Table 1 Characteristics of pregnant women surveyedin the US, 2002, n = 403
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their hands after handling raw meat and 92%indicated that they had not eaten rare meat duringpregnancy.
Of the 403 women who participated in thesurvey, 192 (48%) indicated that they had heard orseen information about toxoplasmosis. On the
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142 • INFECTIOUS DISEASES IN OBSTETRICS AND GYNECOLOGY
Questions nYes(%)
No(%)
Not sure(%)
General information and knowledgeHave you ever read, heard or seen any information about toxoplasmosis
(see text for where information acquired)?Have you ever been tested for toxoplasmosis?Is toxoplasmosis caused by an infection?Is toxoplasmosis caused by a poison?Is toxoplasmosis (Toxoplasma gondii) shed in the feces of infected cats?Is toxoplasmosis (T. gondii) sometimes found in raw or undercooked meat?
Risk factorsCan people get toxoplasmosis by changing cat litter?Can people get toxoplasmosis by eating undercooked pork?Can people get toxoplasmosis by handling raw venison (deer meat)?Can people get toxoplasmosis by gardening without gloves?
Symptoms and timing of infectionCan pregnant women develop serious complications after infection with toxoplasmosis (T. gondii)?Can unborn and/or newborn children develop serious complications after infection with
toxoplasmosis (T. gondii)?Can toxoplasmosis in a pregnant woman cause fever and feeling like you have the ‘flu’?Can toxoplasmosis in a pregnant woman cause swollen glands (lymph nodes)?Can toxoplasmosis in a pregnant woman cause no symptoms?Toxoplasmosis (T. gondii) can only be passed from a pregnant woman to her fetus if she is
newly infected during that pregnancy.Toxoplasmosis (T. gondii) is rarely passed from a pregnant woman to her fetus if she was
infected before becoming pregnant.A baby with toxoplasmosis may have no signs of illness at birth, but develop illness later.A baby with toxoplasmosis may have vision problemsA baby with toxoplasmosis may be treated with medicine
Prevention knowledgeWays to avoid toxoplasmosis include: feeding your cat dry or commercial cat food and
not letting it kill and eat rodents.Ways to avoid toxoplasmosis include: avoiding stray cats.Ways to avoid toxoplasmosis include: letting someone else change the cat’s litter box.Ways to avoid toxoplasmosis include: making sure the cat’s litter box is changed daily.Toxoplasmosis can be prevented by cooking meat well until no pink is seen and the juices
run clear.Toxoplasmosis can be prevented by thoroughly washing and/or peeling all fruits and
vegetables before eating them.Toxoplasmosis may be prevented by cleaning all cutting boards and utensils thoroughly
after each use.
Preventive behaviorSince becoming pregnant, do you routinely wash your hands after gardening?Since becoming pregnant, do you routinely wash your hands after changing cat litter?Since becoming pregnant, do you routinely wash your hands after handling raw meat?Since becoming pregnant, do you eat rare meat?
403
402395389390388
396393391390
397393
398395395396
385
387385387
387
387391388387
388
389
388298396397
48**
7**40**21**61**30**
60**26**22**29**
58**56**
36**25**17**28**
15**
20**20**27**
29**
47**65**45**48**
39**
49**
93**80**96**
6**
43
501331**1
15
3211720
43
95
165
13
523
11
53183
5
1
312
292
8
4347493956
37526159
3942
62706868
73
757871
60
47344750
56
50
4832
*The number of respondents may vary for some questions due to non-response. Percentages read horizontally may not add to 100% dueto rounding. Ninety-five percent confidence limits for percentages are ± 6.7% or less (see Methods). **Correct answer for knowledgequestions
Table 2 Toxoplasmosis-related knowledge and preventive practices of pregnant women in the US, 2002, n = 403*
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survey form, respondents were asked to check allinformation sources where they had heard abouttoxoplasmosis (multiple answers were accepted, soresponses total greater than 100%). Of these 192women, 137 (71%) indicated that they had heardabout toxoplasmosis from magazines or bookson pregnancy and childbirth, 103 (53%) from amedical professional, 86 (45%) from friends orfamily, 27 (13%) from childbirth classes or healthclasses and less than 1% from a government agencyor television.
DISCUSSION
This national survey of pregnant women abouttoxoplasmosis documents a relatively low levelof knowledge about the disease, symptoms andhow to prevent infection. The highest level ofknowledge was about the association between catsand toxoplasmosis. There was a relatively lowlevel of knowledge about the role of undercooked
meat and other risk factors for T. gondii infection.The United States Department of Agricultureestimates that one-half of the T. gondii infectionsin the US are due to ingestion of undercookedmeat7. A recent community-based case–controlstudy supports this estimate8.
It is interesting that knowledge about toxo-plasmosis did not vary greatly by trimester ofpregnancy. It may be that efforts to educatepregnant women about toxoplasmosis occurmost often in the first trimester, so knowledge doesnot increase in subsequent trimesters. For keyknowledge questions, the results also varied byrace–ethnicity, suggesting an even more importantrole of preventive education for some racial andethnic groups.
The findings of this study indicate that healthprofessionals play an important role in informingwomen about toxoplasmosis. Of those womenwho had heard about toxoplasmosis, over half hadheard about it from a medical professional.A previous national survey found that US
Toxoplasmosis and pregnant women Jones et al.
INFECTIOUS DISEASES IN OBSTETRICS AND GYNECOLOGY • 143
Question
Age (years)% correct
Education% correct
Trimester% correct
Pregnancy% correct
≤ 25 26–34 ≥ 35≤ Highschool
Somecollege
Collegegraduate
Graduateschool 1st 2nd 3rd 1st ≥ 2
Have you ever read, heard or seen any informationabout toxoplasmosis?
Is toxoplasmosis caused by an infection?Can people get toxoplasmosis by eating
undercooked pork?Is toxoplasmosis (T. gondii) sometimes found in raw
or undercook meat?Toxoplasmosis can be prevented by cooking meat
well until no pink is seen and the juices run clear.Can people get toxoplasmosis by gardening without
gloves?Usually toxoplasmosis can only be passed from a
pregnant women to her fetus if she is newlyinfected during that pregnancy
Ways to avoid toxoplasmosis include feeding yourcat dry or commercial cat food and not letting itkill and eat rodents
Toxoplasmosis can be prevented by thoroughlywashing and/or peeling all fruits and vegetablesbefore eating them
39
3427
26
36
14
20
26
32
53
4026
31
50
35
27
33
43
50
4924
29
58
33
37
26
40
26*
2425
21
29
10
19
17
21
46
3627
30
41
26
26
25
35
54
4427
31
54
35
27
33
46
66
5123
30
67
44
41
42
53
40
3817
27
47
26
28
27
47
46
3729
33
49
24
24
32
38
51
4227
28
48
32
29
29
39
48
3933
36
52
31
26
35
46
49
3922
25
45
29
29
25
36
*Significant trends or differences in bold for age, education, trimester or number of pregnancies (read horizontally, chi-square or chi-squarefor trend, p < 0.05)
Table 3 Selected questions about toxoplasmosis stratified by age, education, trimester and number of pregnancies
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obstetrician-gynecologists are well informed abouthow to prevent toxoplasmosis9. The findings ofthis study also indicate that women’s magazinesand books are a good place to reach women withinformation about toxoplasmosis.
Our survey is subject to several limitations. Thephysicians and patients participating in the surveywere volunteers, therefore the results are notrepresentative of all pregnant women in the USand may be subject to some statistical biases. Thewomen in our study were more highly educatedthan women in the US population (Table 1) andbecause we found that toxoplasmosis-relatedknowledge increased with educational level, ourfindings may over-estimate knowledge about thisdisease among US women. In addition, because avery high percentage of women indicated that theypractice good preventive behaviors, one wondersif the respondents were motivated to give thecorrect answers because the survey was providedin their place of medical care. However, mostwomen (in general, not specifically pregnantwomen) also responded that they practice good
preventive behaviors in a survey of the generalpopulation about foodborne disease conducted bythe CDC in 1998–199910.
It is encouraging that a study in Canada hasshown that even brief education of pregnantwomen helps to improve some congenital toxo-plasmosis preventive behaviors11 and that a studyin Belgium found that health education wasassociated with a 63% reduction in T. gondiiseroconversion12. In addition, researchers workingin Poland found that toxoplasmosis-relatededucation of pregnant women doubled theirknowledge about the disease and prevention in4 years13.
Education about meat- and cat/soil-relatedhygiene should be provided to women of child-bearing age by educational institutions and topregnant women at their first prenatal visit2. It isimportant that the educational materials becomplete and accurate14 and that they be madeavailable in a culturally and linguistic appropriateformat15. With these measures, many cases ofcongenital toxoplasmosis could be prevented.
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3. Mead PS, Slutsker L, Dietz V, et al. Food-relatedillness and death in the United States. Emerg InfectDis 1999;5:607–24
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6. Dean AG, Dean JA, Coulombier D, et al. Epi Info,Version 6: A Word Processing, Database, andStatistics Program for Epidemiology on Micro-computers. Centers for Disease Control andPrevention, Atlanta, GA, 1994
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8. Roghmann MC, Faulkner CT, Lefkowitz A, et al.Decreased seroprevalence for Toxoplasma gondiiin Seventh Day Adventists in Maryland. Am JTrop Med Hyg 1999;60:790–2
9. Jones JL, Dietz VJ, Power M, et al. Survey ofobstetrician-gynecologists in the United Statesabout toxoplasmosis. Infect Dis Obstet Gynecol2001;9:23–31
10. Centers for Disease Control and Prevention.Foodborne Diseases Active Surveillance Network(FoodNet): Population Survey of Exposures:1998–1999. Atlanta: Centers for Disease Controland Prevention, 1999
11. Carter AO, Gelmon SB, Wells GA, Toepell AP.The effectiveness of a prenatal educationprogramme for the prevention of congenitaltoxoplasmosis. Epidemiol Infect 1989;103:539–45
12. Foulon W, Naessens A, Derde MP. Evaluation ofthe possibilities for preventing congenital toxo-plasmosis. Am J Perinatol 1994;11:57–62
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13. Pawlowski ZS, Gromadecka-Sutkiewicz M,Skommer J, et al. Impact of health education onknowledge and prevention behavior for congenitaltoxoplasmosis: the experience in Poznan, Poland.Health Educ Res 2001;16:493–502
14. Newton LH, Hall SM. A survey of healtheducation material for the primary prevention of
15. Jara M, Hsu HW, Eaton RB, Demaria A Jr.Epidemiology of congenital toxoplasmosisidentified by population-based newborn screeningin Massachusetts. Pediatr Infect Dis J 2001;20:1132–5
RECEIVED 05/05/03; ACCEPTED 07/30/03
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