Skip to main content
NCBI home page
HHS Author Manuscripts logoLink to HHS Author Manuscripts
. Author manuscript; available in PMC: 2016 Mar 1.
Published in final edited form as: Arch Gynecol Obstet. 2014 Sep 10;291(3):545–555. doi: 10.1007/s00404-014-3450-y

Survey of obstetrician-gynecologists in the United States about toxoplasmosis: 2012 Update

Stephanie M Davis 1, Britta L Anderson 2, Jay Schulkin 2, Katherine Jones 3, Jodi Vanden Eng 4, Jeffrey Jones 1
PMCID: PMC4720129  NIHMSID: NIHMS749362  PMID: 25205181

Abstract

Purpose

Toxoplasmosis, caused by the parasite Toxoplasma gondii, can have serious impacts on fetal development in the setting of acute maternal primary infection. The U.S. Centers for Disease Control and Prevention and the American College of Obstetricians and Gynecologists (ACOG) sought to determine current knowledge, practices, opinions and educational preferences regarding T. gondii infection in pregnancy among ACOG members practicing prenatal care.

Methods

A survey was sent to 1056 ACOG members chosen by stratified random sampling from membership lists, including 370 participants and 686 non-participants in the Collaborative Ambulatory Research Network (CARN). Mailings were sent up to 4 total times to nonresponders.

Results

Minimum response rates were 40.3% (CARN) and 19.7% (non-CARN); responses rates adjusted for imputed non-eligibility were 59.7% (CARN) and 22.6% (non-CARN). Among providers, 80.2% had diagnosed no acute maternal T. gondii infections in the past 5 years, 12.7% correctly identified the screening role of the Toxoplasma avidity test, 42.6% routinely performed serologic T. gondii screening for at least some asymptomatic pregnant women, and 62.1% of those who so did used appropriate approaches. Providers in the northeastern United States were 2.02 times more likely to routinely screen than those in the west (p=.025) and female providers were 1.48 times more likely than male providers (p=.047). The potential educational interventions considered useful by the most practitioners were updated ACOG guidelines on screening (81.4%) and management (71.7%) for acute T. gondii infection in pregnancy.

Conclusions

ACOG members would benefit from educational efforts targeted at risk factor counseling and screening approaches.

Introduction

Acute Toxoplasma gondii infection in pregnant women can cause serious sequelae in their infants. If transplacental transmission causes fetal infection, neurologic and ocular birth defects can result. However, with early maternal diagnosis, treatment regimens are available that may decrease risk of transplacental transmission, or reduce clinical manifestations if transmission occurs. Due to the lack of well-controlled studies, though, the efficacy of these treatments and the utility of routine screening remain controversial. In the United States there are no universally accepted guidelines, and practice varies.

The US Centers for Disease Control and Prevention (CDC) and the American College of Obstetricians and Gynecologists (ACOG) conducted surveys of obstetrical providers in 1998 [1] and 2006 [2]. These identified educational needs later addressed in an ACOG practice bulletin [3]. In 2012, we circulated a third updated survey to the ACOG membership to follow changes in practitioner knowledge, practices and opinions. Here we report results.

Materials and Methods

A questionnaire was developed with reference to the prior surveys, and pilot-tested by ACOG. It addressed experience, knowledge and practices regarding screening, diagnosis and management of acute maternal and fetal toxoplasmosis; and opinions on legislative regulation of screening and continuing education needs. Demographic characteristics, practice type and patient population were also collected. Participants were selected from among ACOG members, including both non-participants and participants in ACOG's Collaborative Ambulatory Research Network (CARN), a cadre of practicing obstetrician-gynecologists who have agreed to participate in periodic ACOG surveys.

Stratified random sampling was used to sort ACOG and CARN members into groups of 100, balanced on age, gender and geography, minus losses due to invalid addresses or discontinued practice. Then groups were randomly selected to total a similar target respondent number to previous ACOG surveys. In 2012-2013, the questionnaire was mailed (including four mailings to nonresponders) to 1056 ACOG members (370 CARN members, 686 non-CARN). Analysis was performed using SAS Enterprise Guide version 9.3 (SAS Institute, Cary, NC). Respondent surveys were included if their CARN affiliation was known, they answered more than three survey questions, and they were currently practicing obstetrics including prenatal care. US Census regions [4] were used to delineate practice regions.

Responses were analyzed separately for CARN and non-CARN respondents. Denominators vary because not all respondents answered all questions. Results are for total proportion of respondents selecting a given answer; for questions for which multiple answers were accepted, totals may therefore exceed 100%. Answer proportions were compared between groups using the Fisher's exact test for categorical variables and a two-sample t-test for continuous variables. If not significantly different, groups were pooled to calculate total proportions giving each answer, for which 95% Clopper-Pearson confidence intervals (CIs) were calculated; otherwise, proportions were calculated for each group separately.

Univariate Poisson regression models were used to investigate the association between selected outcome variables -- ever performing serologic screening on pregnant women, correctly identifying letting a pet cat go outdoors and gardening as risk factors, and using an “acceptable”a seroscreening method -- and covariates including provider gender, years elapsed since completing residency, primary practice field, and geographic region. If more than one covariate was associated with a given outcome, multivariate Poisson regression using all covariates significant at alpha =.05 on univariate analysis (forward stepwise approach) was performed for that outcome. P-values are provided, allowing assessment of significance at either p<.05, or p < .0125 after adjusting for multiple comparisons.

The study was reviewed and exempted by ACOG and CDC human subjects committees.

Results

Response rate

The participant flowchart, including response rates, is in Figure 1. The minimum response rates were: 40.3% CARN, 19.7% non-CARN; if nonrespondents were ineligible in the same proportion as respondents, however, response rates were: 59.7% CARN, 22.6% non-CARN.

Figure 1.

Figure 1

Open in a new tab

Respondent Flowchart

Respondent demographics

Respondents had been practicing for a mean of 21.0 years. Mean age was 52.7 years in 2012 (95% CI 51.6-53.1); mean years in practice were 21.0 (95% CI 19.8-22.0). Other characteristics are in Table 1. Only in gender were CARN and non-CARN respondents different (p=0.04; CARN percent male = 41.9, 95% CI 34.1-50.1; non-CARN, 50.8%, 95% CI 41.5-60.2).

TABLE 1.

Demographic characteristics of respondents

Total (N = 267)
Question Answer n N % 95% CI
Gender Male 122 266 45.9 (39.9, 52.2)
Female 144 266 54.1 (48.0, 60.0)
Geographic area Midwest 70 266 26.3 (20.9, 31.8)
Northeast 45 266 16.9 (12.7, 22.1)
South 88 266 33.1 (27.6, 39.2)
West 59 266 22.2 (17.4, 27.8)
Outside Continental US 4 266 1.5 (0.4, 3.8)
Practice location Urban: inner city 33 266 12.4 (8.7,16.0)
Urban: other 81 266 30.5 (25.1, 36.5)
Suburban 117 266 44.0 (37.7, 50.0)
Rural 35 266 13.2 (9.4, 17.9)
Military 0 266 0.0 -
Practice structure Solo private practice 49 266 18.4 (13.9, 23.5)
Group practice 168 266 63.2 (56.8, 68.7)
University 34 266 12.8 (9.0, 17.3)
Hospital-based 8 266 3.0 (1.3, 5.8)
Other 8 266 3.0 (1.3, 5.8)
Specialty General OB/Gyn 233 266 87.6 (83.6, 91.5)
Gynecology only 15 266 5.6 (2.9, 8.4)
Obstetrics only 8 266 3.0 (1.3, 5.9)
Maternal-fetal Medicine 9 266 3.4 (1.2, 5.6)
Other 2 266 0.8 (0, 1.8)
Primary Race/Ethnicity served White, non-Hispanic 183 266 68.8 (63.5, 74.6)
White, Hispanic 25 266 9.4 (5.9, 13.0)
Asian/Pacific Isl. 11 266 4.1 (1.8, 6.6)
Native American/Alaska native 1 266 0.4 (0.0, 1.1)
African-Amer., non-Hispanic 18 266 6.8 (3.8, 9.8)
African-Amer., Hispanic 6 266 2.3 (0.5, 4.1)
Multiracial 17 266 6.4 (3.5, 9.4)
unsure 4 266 1.5 (0.0, 2.3)
Open in a new tab

Other significant differences between CARN and non-CARN respondents were uncommon and are noted below.

Provider Experience

Answers to questions about provider experience and the other topics that follow are shown in table 2, except where covered in the text. Where applicable, correct answers are marked in the table with the footnote: a. Providers had diagnosed few cases of acute maternal toxoplasmosis, with 80.2% diagnosing none, and only 5.4% over one, in the past five years.

TABLE 2.

Ob/gyn provider experience with, knowledge of, and approach to toxoplasma gondii infection in pregnancy: selected answers

Question Answer Total
n N % 95% CI
CLINICAL
How often does a pregnant patient receive counseling in your practice about preventing acute T. gondii infection? (CHECK ALL THAT APPLY) At the initial exam 197 267 73.8 (68.1, 79.0)
At every visit 0 267 0.0 _
When she asks questions 80 267 30.0 (24.5, 35.9)
When she mentions she was ill 20 267 7.5 (4.6, 11.3)
If I consider her at high risk 68 267 25.5 (20.4, 31.1)
Never 8 267 3.0 (1.3, 5.8)
Don't know 5 267 1.9 (0.6, 4.3)
Other 6 267 2.2 (0.4, 4.0)
For each exposure please indicate whether you consider it a risk factor and if so, whether your counseling includes it.
a) Changing cat litter without glovesa Risk factor (RF) 250 263 95.1 (91.7, 97.3)
Counseled on 218 224 97.3 (94.3, 99.0)
b) Permitting a pet cat to go outdoors a Risk factor 201 251 80.1 (75.1, 85.0)
Counseled on 155 180 86.1 (80.2, 90.1)
c) Changing cat litter every few days (vs. daily)a Risk factor 139 257 54.1 (47.8, 60.3)
Counseled on 86 121 71.1 (62.1, 79.0)
d) Petting a cat Risk factor 42 259 16.2 (11.9, 21.3)
Counseled on 27 35 77.1 (60.9, 90.0)
e) Having a litter of kittens at home a Risk factor 55 260 21.2 (16.4, 26.6)
Counseled on 26 40 65.0 (48.3, 79.4)
f) Contact with sand from an uncovered sandbox a Risk factor 198 251 78.9 (73.3, 83.8)
Counseled on 95 166 57.2 (49.3, 64.9)
g) Eating raw or undercooked meata Risk factor 219 263 83.3 (78.2, 87.6)
Counseled on 152 181 84.0 (77.8, 89.0)
h) Eating raw or undercooked oysters, mussels or clams a Risk factor 64 254 25.2 (20.0, 31.0)
Counseled on 35 48 72.9 (58.2, 84.7)
i) Handling raw meat without washing afterward a Risk factor 176 260 67.7 (61.6, 73.3)
Counseled on 91 145 62.8 (54.4, 70.6)
j) Eating unwashed raw fruits or vegetables a Risk factor 87 259 33.6 (27.9, 39.7)
Counseled on 52 74 70.3 (58.5, 80.3)
k) Gardening without gloves a Risk factor 160 260 61.5 (55.3, 67.5)
Counseled on 87 160 61.2 (56.2, 73.0)
l) Exposure to wild pigeon feces Risk factor 72 256 28.1 (22.7, 34.1)
Counseled on 20 57 35.1 (22.9, 48.9)
m) Drinking untreated water from a stream, lake or ponda Risk factor 94 257 36.6 (30.7, 42.8)
Counseled on 38 77 49.4 (37.8, 61.0)
n) Travelling to some foreign countries without taking food and water precautions a Risk factor 165 261 63.2 (57.1, 69.1)
Counseled on 79 127 62.2 (53.2, 70.1)
o) Employment that involves soil exposure a Risk factor 149 260 57.3 (51.1, 63.4)
Counseled on 58 113 51.3 (41.7, 60.8)
p) Living in a home with a cockroach infestation Risk factor 28 261 10.7 (7.3, 15.1)
Counseled on 9 23 39.1 (19.7, 61.5)
How is counseling information provided? (CIRCLE ALL THAT APPLY): Verbally by you 211 267 79.0 (73.7, 83.8)
Verbally by nurse 113 267 42.3 (36.3, 48.5)
Verbally by other office staff 19 267 7.1 (4.3, 10.9)
Pamphlet 44 267 16.5 (12.2, 21.5)
Which of the following laboratories would you use for T. gondii initial screening and confirmatory serologic testing if you felt they were indicated in a pregnant woman? (CHECK ALL THAT APPLY)
    a) Never request this type of serologic testing Initial 21 263 8.0 (4.7, 11.3)
Confirmatory 16 262 6.1 (3.5, 9.7)
    b) A local hospital lab Initial 115 263 43.7 (37.7, 49.7)
Confirmatory 62 262 23.7 (18.7, 29.3)
    c) A commercial lab (e.g., SKB, LabCorp) Initial 145 263 55.1 (48.9,61.3)
Confirmatory 91 262 34.7 (29.0, 40.1)
    d) State or local public health laboratory Initial 24 263 9.1 (5.9, 13.3)
Confirmatory 37 262 14.1 (10.1, 18.9)
    e) Palo Alto Research Institute Initial 5 263 1.9 (0.6, 4.4)
Confirmatory 29 262 11.1 (7.5, 15.5)
    f) Other Initial 3 262 1.1 (0.2, 3.3)
Confirmatory 5 262 1.9 (0.6, 4.4)
    g) Don't know Initial 16 263 6.1 (3.5, 9.7)
Confirmatory 22 262 8.4 (5.3, 12.4)
By total proportion of respondents: How do you decide whether to do serologic screening for acute T. gondii infection in asymptomatic pregnant women? (CIRCLE ONE): If other, what? Do serologic screening in all 10 126 7.9 (3.9, 14.1)
Do serologic screening if there is no previous positive T. gondii IgG test 5 126 4.0 (1.3, 9.0)
Ask about exposures and/or symptoms; do serologic screening if present 70 126 55.6 (46.4, 64.4)
Ask about exposures and/or symptoms; do serologic screening if present AND there is no previous positive T. gondii IgG test 35 126 27.8 (20.2, 36.5)
Other patient request, in torchb testing, ultrasound findings; state-mandated in OR since 1977; if prior positive IGG flu titer 7 126 5.6 (2.3, 11.1)
Which of the following would you use as a serologic test to confirm a screening result suggestive of acute T. gondii infection in a pregnant woman? (CIRCLE ALL THAT APPLY): T. gondii IgG and IgM (+/− any other answer) 55 264 20.8 (16.1, 26.2)
T. gondii titer only 21 264 8.0 (5.0, 11.9)
Other 123 264 46.6 (40.5, 52.8)
Don't know 65 264 24.6 (19.4, 29.8)
If you were to make a diagnosis of acute maternal T. gondii infection in a pregnant woman AT 14 WEEKS gestation, which of the following would you do INITIALLY? (CIRCLE ALL THAT APPLY):* Make a presumptive diagnosis 31 264 11.7 (8.1, 16.3)
Begin antimicrobial therapy 38 264 14.4 (10.4, 19.2)
Perform amniocentesis for Toxoplasma PCR as soon as clinically safe to perform 20 264 7.6 (4.7, 11.5)
Perform amniocentesis for Toxoplasma PCR around 18 weeks gestation 8 264 3.0 (1.3, 5.9)
Consult specialist 243 264 92.0 (88.1, 95.0)
Other 9 264 3.4 (1.6, 6.4)
Don't know 9 264 3.4 (1.6, 6.4)
If you were to make a diagnosis of acute maternal T. gondii infection in a pregnant woman AT 23 WEEKS gestation, which of the following would you do INITIALLY? (CIRCLE ALL THAT APPLY): Make a presumptive diagnosis 39 264 14.8 (10.7, 19.6)
Begin antimicrobial therapy 22 257 8.6 (5.3, 12.3)
Perform amniocentesis for Toxoplasma PCR as soon as possible 25 264 9.5 (6.2, 13.7)
Consult with a specialist, e.g., in infectious disease or perinatology 247 264 93.6 (89.9, 96.2)
Other 6 264 2.3 (0.8, 4.9)
Don't know 7 264 2.7 (1.1, 5.4)
If you were to make a diagnosis of FETAL toxoplasmosis, after explaining the options, which of the following would you be most likely to recommend as INITIAL management? (CIRCLE ONE): Antimicrobial treatment for toxoplasmosis 29 263 11.0 (7.5, 15.5)
Immediate fetal ultrasound 27 263 10.3 (6.9, 14.6)
Termination of pregnancy 2 263 0.8 (0.0, 2.7)
Consultation with an infectious disease specialist or perinatologist 222 263 84.4 (79.5, 88.6)
Do not make a recommendation, only explain options 8 263 3.0 (1.6, 6.4)
Other 4 263 1.5 (0.4, 3.9)
Don't know 7 263 2.7 (1.1, 5.4)
For each characteristic, circle the type of serologic test to which it applies. (CIRCLE ONE):
    Frequent false positives T. gondii IgG 16 253 6.3 (3.7, 10.2)
T. gondii IgM a 20 253 7.9 (4.7, 11.7)
Both 32 253 12.6 (9.0, 17.7)
Neither 28 253 11.1 (6.9, 14.9)
Not sure 157 253 62.1 (56.3, 68.7)
    Frequent false negatives T. gondii IgG 4 254 1.6 (0.4, 4.1)
T. gondii IgM 11 254 4.3 (1.9, 7.2)
Both 24 254 9.4 (6.3, 14.0)
Neithera 35 254 13.8 (9.6, 18.5)
Not sure 180 254 70.9 (65.2, 76.7)
    A true positive indicates infection within the past 3-6 months T. gondii IgG 15 252 6.0 (3.4, 9.7)
T. gondii IgM 108 252 42.9 (36.6, 49.2)
Both 41 252 16.3 (11.7, 21.1)
Neithera 9 252 3.6 (1.7, 6.7)
Not sure 79 252 31.3 (25.9, 37.8)
    A true positive indicates infection within the past 12-18 months T. gondii IgG 73 245 29.8 (23.9, 35.7)
T. gondii IgMa 16 245 6.5 (3.8, 10.4)
Both 37 245 15.1 (10.9, 20.3)
Neither 25 245 10.2 (6.7, 14.8)
Not sure 94 245 38.4 (32.4, 45.0)
    A true positive indicates infection at some point in the past T. gondii IgG a 161 256 62.9 (56.9, 69.2)
T. gondii IgM 5 256 2.0 (0.7, 4.6)
Both 28 256 10.9 (7.6, 15.8)
Neither 1 256 0.4 (0.0, 2.2)
Not sure 58 256 22.7 (18.1, 28.9)
How effective do you believe treatment with spiramycin for a pregnant woman with acute T. gondii infection is in preventing congenital toxoplasmosis? (CIRCLE ONE): Highly effective (70-100%) 28 263 10.6 (7.2, 15.0)
Moderately effective (40-70%) 56 263 21.3 (16.5, 26.8)
Somewhat effective (10-40%) 21 263 8.0 (5.0, 12.0)
Weakly effective or not effective 4 263 1.5 (0.4, 3.9)
Not known or controversiala 19 263 7.2 (4.4, 11.1)
Don't know 135 263 51.3 (45.1, 57.5)
What does the Toxoplasma IgG avidity test help determine? (CIRCLE ONE):* Whether T. gondii infection occurred in the last 3-4 monthsa 33 260 12.7 (8.9, 17.4)
Whether T. gondii infection occurred in the last 6-12 months 18 260 6.9 (4.2, 10.7)
Whether T. gondii infection actually occurred but not when it occurred 47 260 18.1 (13.6, 23.3)
Other: 2 260 0.8 (0.0, 2.8)
Don't know 160 260 61.5 (55.3, 67.5)
Open in a new tab
a

True risk factor for T. gondii transmission

b

Toxoplasmosis, Other (syphilis, varicella-zoster, parvovirus B19), Rubella, Cytomegalovirus (CMV), and Herpes.

*

Differences between CARN and non-CARN respondent answer distributions significant at p< .05; see text for description

Risk Factors and Counseling

Most respondents (73.8%) provided prenatal toxoplasmosis counseling at the first visit, including 30.0% when the patient asked questions and 25.5% when they considered the patient high-risk. Well-recognized risk factors included changing cat litter without gloves (95.1%), contact with sand from an uncovered sandbox (78.9%), and eating raw or undercooked meat (83.3%). Less-known factors included changing cat litter every few days compared to daily (54.1%), having a litter of kittens at home (21.2%), and gardening without gloves or employment involving soil exposure (61.5%, 57.3%, respectively). feces). Among providers who considered an exposure a risk factor, prevalence of including it in counseling varied (39.1-97.3%).

Among those who identified gardening without gloves as a risk factor, CARN and non-CARN providers were significantly (p= .04) more likely to include it in counseling.

Overall, 6.4% of providers answered four or fewer risk factor questions correctly, 40.1% five to eight, 47.9% nine to twelve, and 5.6% more than 12. Among providers answering nine or more questions correctly, often-missed risk factors were eating raw or undercooked oysters, mussels or clams (35.8%); eating unwashed raw fruits or vegetables (55.0%); and drinking untreated water from a stream, lake or pond (55.0%).

Screening and Diagnosis

Forty-two point six percent of providers (95% CI 36.7%-48.6%) reported ever seroscreening for acute T. gondii infection in asymptomatic pregnant women. Of these, 55.6% reported deciding who to screen by asking about risk factors; 27.8% also required absence of a previous positive serology. Respondents who seroscreened generally did so once, either as early as possible (70.5%; 95% CI 64.9%-80.2%) or if indicated by signs/symptoms or exposure (16.0%; 95% CI 10.2%-23.5%).

Providers’ mean estimate of the laboratory cost of their screening approach was $182.50. CARN providers estimated significantly (p=.02) higher costs ($224.17, 95% CI $163.17- $285.16 compared to $126.94, 95% CI $80.95- $172.94). Of providers who ever seroscreened asymptomatic pregnant women, 59.1% (95% CI 50.7%-67.5%) used T. gondii IgG and IgM (estimating a mean cost of $199.35); 24.2% (95% CI 17.2%-34.5%) IgG only (with or without “T. gondii titer”, a term interpretable as referring to tests which do not discriminate between IgG and IgM); 2.3% (95% CI 0.5%-6.5%) IgM only (with or without “T. gondii titer”), 7.6% (95% CI 3.7%-13.5%) “T. gondii titer” only, 0.8% (95% CI 0.0%-4.2%) IgA, and 6.1% (2.7%-11.6%) did not know.

Among approaches to confirmation, most common were answers containing both IgG and IgM (20.8%), T. gondii titer only (8.0%), and ‘don't know’ (24.6%); 46.6% took other approaches. Toxoplasma avidity was included by 9.7%. Eleven point one percent of respondents would send confirmatory testing (vs 1.9% initial testing) to the Palo Alto Research Institute's Toxoplasma Serology Laboratory, a nonprofit institution offering expert testing.

Approach to Acute Maternal and Fetal T. gondii infection

Given a diagnosis of acute maternal T. gondii infection at 14 weeks or 23 weeks gestation, most providers (92.0% and 93.6% respectively) would consult a specialist. Fewer would begin antimicrobial therapy (14.4% and 8.6%) or perform amniocentesis (7.6% and 9.5%). For fetal toxoplasmosis, 84.4% would consult with an infectious disease specialist, 11% begin antimicrobial treatment, 10.3% perform immediate fetal ultrasound, and 0.8% recommend termination. In the case of acute maternal infection at 14 weeks, CARN respondents were significantly more likely (p=.01) to begin antimicrobial therapy.

Provider knowledge about toxoplasmosis testing options

Most respondents were not sure which screening test gives frequent false positives (62.1%; IgM is correct); or false negatives (70.9%; no widely used test is correct). Only 7.2% correctly stated that the effectiveness of spiramycin against maternal-fetal T. gondii transmission is unknown or controversial (51.3% did not know), and 12.7% that the Toxoplasma avidity test determines whether maternal T. gondii infection occurred in the last 3-4 months. CARN members were significantly more likely (p=.03) to answer this question correctly.

Provider opinions on standardized screening approaches

Eighty-nine percent of respondents were opposed (1 or 2 on a 5-point scale) to universal monthly toxoplasmosis screening in pregnancy, 72% to universal screening once per trimester, and 43% to universal screening once in each pregnancy (with 34% in favor). Eighty-one percent favored screening only for patients with risk factors or recent clinical signs or symptoms, consistent with reported practice (see above). (Those favoring risk-factor-based screening answered risk factor questions correctly in proportions similar to all respondents).

For the scenario of state-mandated universal monthly screening, often-cited benefits were improved patient knowledge about and avoidance of exposure to T. gondii risk factors (40.8%) and identification of toxoplasmosis infections without known risk factors (40.5%). Often-cited disadvantages were false-positive results leading to unnecessary workup and/or treatment with potential side effects (72.6%) or unnecessary anxiety (65.8%), and lack of evidence of cost-effectiveness (70.7%).

Provider sources of information

The most-cited sources of information on advances in OB/GYN infectious disease care used by respondents were ACOG publications (37.9% first choice; 82.8% among top 3 choices), followed by journals (24.1%; 53.1%) and UpToDate (14.6%; 43.4%); 53.4% also listed CME activities with any ranking. Sources favored by respondents (first, second or third choice) for ACOG to help physicians develop the skills to manage acute toxoplasmosis in pregnancy were updating ACOG guidelines on screening and management (81.4% and 71.7% respectively), feature articles in newsletters (30.1%), CME monographs (26.4%) and online CME (20.3%).

Comparison with prior years

Ninety point four percent of 1998 respondents had diagnosed no acute cases of toxoplasmosis in the past year, compared to 92.1% (95% CI 88.8%-95.3%) of 2012 respondents. Fifty-three point four percent of 2006 respondents compared to 73.8% (95% CI 68.1%-79.0%) of 2012 respondents reported providing risk factor counseling at the initial pregnancy visit. When counseling, similar proportions of respondents included handling cat litter in 2012 and 2006 (92.5% and 99.6%); 41.9% and 65.4% respectively (compared to 67.6% in 1998) included gardening. (In both cases the 2012 question added “without gloves”).

While only 8.8% of 2006 respondents had heard of the Toxoplasma avidity test, 50.8% of those who had, and who identified an answer for the time frame for infection it suggested, answered correctly (the past 3-4 months); in comparison, 12.7% of all 2012 respondents identified time frame correctly, where 61.5% chose “don't know”.

Associative Analysis

Providers in the Northeast were 2.02 times (95% CI 1.31-3.72; p = .025) more likely than those in the West to ever screen for acute maternal toxoplasmosis in asymptomatic pregnant women (59.1% vs. 29.3%). Female providers were 1.48 times (95% CI 1.00-2.17; p=.047) more likely to do so than male providers (63.1% vs. 42.6%). With both covariates included, region remained significant (1.98; 95% CI 1.30-3.67; p = .028); gender did not (1.45; 95% CI 0.98-2.15; p = .062). Other associations were not significant.

Discussion

Fetal toxoplasmosis is an uncommon but potentially serious complication of pregnancy. An estimated 89% of women of childbearing age are susceptible to acute T. gondii infection (not previously infected) [5], with roughly 400—4000 [6-9] newborns born with congenital T. gondii infection annually in the United States.

An increasing majority of obstetricians counsel pregnant women about risk factors for toxoplasmosis. While exposures from cat litter, sandboxes and raw meat were well-recognized, other risk factors for transmission via domestic cats, gardening, travel without food and water precautions, and soil exposure were less recognized. This is important given the importance of outdoor exposure of domestic cats [10], soil exposure [11] and travel [12] as risk factors for infection. Awareness of the Toxoplasma avidity test remains uncommon. Availability of comparison over time was limited by the substantial changes in the 2012 survey compared to prior years, but practitioner knowledge about toxoplasmosis does not appear to have increased substantially.

Changing cat litter daily can virtually eliminate its potential for T. gondii transmission, as oocysts require 1-5 days to become infectious [13,14]. T. gondii from infected feces can survive in soil for over a year [15] and contaminate hands, fruits or vegetables, or water. Pregnant women can minimize exposure risks by eating only washed produce and when gardening, wearing gloves and washing hands afterward, removing dirt under the nails.

Roughly half of providers sometimes seroscreened asymptomatic pregnant women, most commonly based on risk factors; the most-preferred approach among our respondents was seroscreening only for patients with risk factors or recent signs or symptoms. For diagnoses of acute maternal T. gondii infection or fetal toxoplasmosis, respondents favored specialist consultation.

No approach to toxoplasmosis screening or management is universally endorsed. One expert group in the United States, Montoya et al. [16], recommends screening all pregnant women for IgG and IgM early in the first trimester; 59.1% of respondents who screened used both tests. Depending on results, this group recommends following up initial positive results by retesting (for example, when IgG-negative, IgM-positive) or sending samples to the Palo Alto Medical Foundation Toxoplasma Serology Laboratory (IgG and IgM both positive), where Toxoplasma avidity testing may be used. Eleven point one percent of our survey respondents would send confirmatory testing to this laboratory.

Montoya et al.'s approach takes into account properties of the screening tests: IgM has a high false-positive rate (reported specificities range between 49.2% [17] and 98.6% [18,19]). A true positive indicates infection within the past 12-18 months (in some cases T. gondii IgM can persist for up to two years [20].) A true positive IgG result indicates infection at some point in the past; of questions about test characteristics, this was the only one answered correctly by most respondents.

In contrast, another expert group, Gilbert and others [21] and the Society of Obstetricians and Gynecologists of Canada (SOGC) [22], recommend screening only in cases of high suspicion, such as suggestive maternal symptoms or high-risk exposures (consistent with the answers of 87.4% of respondents). Several countries have considered but not adopted universal screening [.23—27] Reasons include both costs and such possible harms [28] such as unnecessary treatment due to overdiagnosis and pregnancy terminations. Followup has also proven challenging: late initial testing and poor compliance with screening intervals has led to delayed therapy in France [29] and Austria [30].

The Healthcare Blue Book cites $30 for physician-ordered Toxoplasma IgG testing and $35 for Toxoplasma IgM as reimbursement levels typically accepted from insurers [31] - considerably lower than respondents’ estimates. Awareness of the Toxoplasma avidity test remains low. Often this test can help distinguish whether infection occurred in the past 3-4 months [32-34], a useful feature for first-trimester diagnoses given the long persistence of IgM.

Most providers indicated they would seek expert help after diagnosing acute maternal T. gondii infection. This is a clearly reasonable approach. In such cases, they recommend fetal ultrasound as soon as possible and amniotic fluid PCR at 18 weeks gestation to determine fetal infection. If maternal infection was diagnosed before 18 weeks gestation, they recommend treatment begin with spiramycin until PCR and ultrasound results are available. Then, if either is positive, treatment switches to pyramethamine sulfadiazine and folinic acid (though others question its superiority to spiramycin for this or any indication); if negative, [22,35,36], spiramycin should be started or continued. If instead maternal infection is diagnosed after 18 weeks gestation, pyramethamine sulfadiazine and folinic acid are the default treatment until and unless PCR and ultrasound are negative, in which case either pyramethamine sulfadiazine with folinic acid or spiramycin can be continued untill delivery.

The efficacy of spiramycin, which most providers reported not knowing, is uncertain; comparisons with historical controls suggest benefit [37-39] while more recent nonrandomized studies [40] suggest it may decrease sequelae only [41,42]. Spiramycin is available in the United States from the FDA Division of Special Pathogen and Immunologic Drug Products under an Investigational New Drug license, at 301-827-2335.

The higher prevalence of seroscreening asymptomatic pregnant women among providers in the U.S Northeast is consistent with an increased prevalence of toxoplasmosis exposure in this region [43] (29.2%, vs. 22.5% nationally in 1988-1994).

Limitations of our study include the use of self-reported data and the low survey response rates, all potentially causing overestimation of practitioner knowledge. The many comparisons between CARN and non-CARN respondents may have caused discovery of spurious differences. The Clopper-Pearson method may not fully account for any intracluster correlation within the provider groups in which survey recipients were selected, but given the method used for composing these groups, intracluster correlation should be minimal, with any resulting underestimation of variance also countered by using sandwich estimators for variance.

Continuing education for providers on T. gondii prevention, diagnosis, and treatment is needed. Updated ACOG guidelines addressing these issues would be of particular benefit. However, additional evidence is needed on the magnitudes of expected benefits, harms and costs of routine screening, and comparative effectiveness of alternative antibiotic regimens against maternal-fetal transmission and sequellae.

Acknowledgments

This study is funded in part by grant UA6MC19010, through the U.S. Department of Health and Human Services, Health Resources and Services Administration, Maternal and Child Health Research Program.

Footnotes

a

“Acceptable” screening methods included checking both IgG and IgM; checking IgG alone repeatedly (allowing ascertainment of seroconversion); or checking IgM if then confirmed with IgM and IgG.

Ethical Standards

This manuscript does not contain clinical studies or patient data.

References

  • 1.Jones JL, Dietz VJ, Power M, Lopez A, Wilson M, Navin TR, Gibbs R, Schulkin J. Survey of obstetrician-gynecologists in the United States about toxoplasmosis. Infect Dis Obstet Gynecol. 2001;9:23–31. doi: 10.1155/S1064744901000059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Jones JL, Krueger A, Schulkin J, Schantz PM. Toxoplasmosis Prevention and Testing in Pregnancy, Survey of Obstetrician–Gynaecologists. Zoonoses Public Health. 2009;57:27–33. doi: 10.1111/j.1863-2378.2009.01277.x. [DOI] [PubMed] [Google Scholar]
  • 3.ACOG Practice Bulletin: Perinatal Viral and Parasitic Infections No. 20. Int J Gynecol Obstet. 2000;76:95–107. [PubMed] [Google Scholar]
  • 4.US Census Bureau [10 June 2013];Census Regions and Divisions of the United States. https://www.census.gov/geo/www/us_regdiv.pdf.
  • 5.Jones JL, Kruszon-Moran D, Sanders-Lewis K, Wilson M. Toxoplasma gondii infection in the United States, 1999–2004, decline from the prior decade. Am J Trop Med Hyg. 2007;77:405–410. [PubMed] [Google Scholar]
  • 6.Alford CA, Jr, Stagno S, Reynolds DW. Congenital toxoplasmosis: clinical, laboratory, and therapeutic considerations, with special reference to subclinical disease. Bull N Y Acad Med. 1974;50:160–181. [PMC free article] [PubMed] [Google Scholar]
  • 7.Kimball AC, Kean BH, Fuchs S. Congenital toxoplasmosis: a prospective study of 4,048 obstetric patients. Am J Obstet Gynecol. 1971;111:211–218. doi: 10.1016/0002-9378(71)90892-1. [DOI] [PubMed] [Google Scholar]
  • 8.Guerina NG, Hsu HW, Meissner HC, Maguire JH, Lynfield R, Stechenberg B, Abroms I, Pasternack MS, Hoff R, Eaton RB, Grady GF, New England Regional Toxoplasma Working Group Neonatal serologic screening and early treatment for congenital Toxoplasma gondii infection. N Engl J Med. 1994;330:1858–1863. doi: 10.1056/NEJM199406303302604. [DOI] [PubMed] [Google Scholar]
  • 9.Lopez A, Dietz V, Wilson M, Navin TR, Jones JL. Preventing congenital toxoplasmosis. MMWR Recomm Rep. 2000;49:37–75. [PubMed] [Google Scholar]
  • 10.Lopes AP, Cardoso L, Rodrigues M. Serological survey of Toxoplasma gondii infection in domestic cats from northeastern Portugal. Vet Parasitol. 2008 Aug 17. 2008;155(3-4):184–9. doi: 10.1016/j.vetpar.2008.05.007. doi: 10.1016/j.vetpar.2008.05.007. [DOI] [PubMed] [Google Scholar]
  • 11.Cvetković D1, Bobić B, Jankovska G, Klun I, Panovski N, Djurković-Djaković O. Risk factors for Toxoplasma infection in pregnant women in FYR of Macedonia. Parasite. 2010;17(3):183–6. doi: 10.1051/parasite/2010173183. [DOI] [PubMed] [Google Scholar]
  • 12.Anand R, Jones CW, Ricks JH, Sofarelli TA, Hale DC. Acute primary toxoplasmosis in travelers returning from endemic countries. J Travel Med. 2012;19:57–60. doi: 10.1111/j.1708-8305.2011.00564.x. doi: 10.1111/j.1708-8305.2011.00564.x. [DOI] [PubMed] [Google Scholar]
  • 13.Dubey JP. Toxoplasmosis. J Am Vet Med Assoc. 1994;205:1593–1598. [PubMed] [Google Scholar]
  • 14.Dubey JP, Miller NM, Frenkel JK. The Toxoplasma gondii oocyst from cat feces. J Exp Med. 1970;132:636–662. doi: 10.1084/jem.132.4.636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Lélu M, Villena I, Dardé ML, Aubert D, Geers R, Dupuis E, Marnef F, Poulle ML, Gotteland C, Dumètre A, Gilot-Fromont E. Quantitative estimation of the viability of Toxoplasma gondii oocysts in soil. Appl Environ Microbiol. 2012;78:5127–5132. doi: 10.1128/AEM.00246-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Montoya JG, Remington JS. Management of Toxoplasma gondii Infection during pregnancy. Clin Infect Dis. 2008;47:554–566. doi: 10.1086/590149. [DOI] [PubMed] [Google Scholar]
  • 17.Liesenfeld O, Press C, Montoya JG, Gill R, Isaac-Renton JL, Hedman K, Remington JS. False-positive results in immunoglobulin M (IgM) Toxoplasma antibody tests and importance of confirmatory testing: the Platelia Toxo IgM Test. J Clin Microbiol. 1997;35:174–178. doi: 10.1128/jcm.35.1.174-178.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Wilson MJ, Remington S, Clavet C, Varney G, Press C, Ware D. Evaluation of six commercial kits for detection of human immunoglobulin M antibodies to Toxoplasma gondii. J Clin Microbiol. 1997;35:3112–3115. doi: 10.1128/jcm.35.12.3112-3115.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Liesenfeld O, Press C, Montoya JG, Gill R, Isaac-Renton JL, Hedman K, Remington JS. False-positive results in immunoglobulin M (IgM) Toxoplasma antibody tests and importance of confirmatory testing: the Platelia Toxo IgM Test. J Clin Microbiol. 1997;35:174–178. doi: 10.1128/jcm.35.1.174-178.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Gras L, Gilbert RE, Wallon M, Peyron F, Cortina-Borja M. Duration of the IgM response in women acquiring Toxoplasma gondii during pregnancy: implications for clinical practice and cross-sectional incidence studies. Epidemiol Infect. 2004;132:541–548. doi: 10.1017/s0950268803001948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Gilbert R, Petersen E. Toxoplasmosis and pregnancy. 2013 UptoDate Online. Accessed 16 October 2013. [Google Scholar]
  • 22.Paquet C, Yudin MH. Toxoplasmosis in Pregnancy: Prevention, Screening, and Treatment. J Obstet Gynaecol Can. 2013;35:78–79. doi: 10.1016/s1701-2163(15)31053-7. [DOI] [PubMed] [Google Scholar]
  • 23.Peckham C. [5 August 2013];Screening for toxoplasmosis. Expert review for United Kingdom policy. 2011 http://www.screening.nhs.uk/policydb_download.php?doc=138.
  • 24. [5 August 2013];UK National Screening Committee policy on toxoplasmosis screening in pregnancy (updated December 2011) http://www.screening.nhs.uk/toxoplasmosis.
  • 25.Rudin C, Boubaker K, Raeber PA, Vaudaux B, Bucher HC, Garweg JG, Hoesli I, Kind C, Hohlfeld P. Toxoplasmosis during pregnancy and infancy, a new approach for Switzerland. Swiss Med Wkly. 2008;138(Suppl 168):1–8. doi: 10.4414/SMW.2008.w30271. [DOI] [PubMed] [Google Scholar]
  • 26.Röser D, Nielsen HV, Petersen E, Saugmann-Jensen P, Nørgaard-Pedersen PB. Congenital toxoplasmosis—a report on the Danish neonatal screening programme 1999–2007. J Inherit Metab Dis. 2010;33(Suppl 2):S241–S247. doi: 10.1007/s10545-010-9124-4. [DOI] [PubMed] [Google Scholar]
  • 27.Miron D, Raz R, Luder A. Congenital toxoplasmosis in Israel: to screen or not to screen. Isr Med Assoc J. 2002;4:119–122. [PubMed] [Google Scholar]
  • 28.Khoshnood B, De Vigan C, Goffinet F, Leroy V. Prenatal screening and diagnosis of congenital toxoplasmosis: a review of safety issues and psychological consequences for women who undergo screening. Prenat Diagn. 2007;27:395–403. doi: 10.1002/pd.1715. [DOI] [PubMed] [Google Scholar]
  • 29.Cornu C, Bissery A, Malbos C, Garwig R, Cocherel C, Ecochard R, Peyron F, Wallon M. Factors affecting the adherence to an antenatal screening programme: an experience with toxoplasmosis screening in France. Euro Surveill. 2009;14:21–25. [PubMed] [Google Scholar]
  • 30.Sagel U, Kremer A, Mikolajczyk RT. Incidence of maternal Toxoplasma infection in pregnancy in Upper Austria, 2000-2007. BMC Infect Dis. 2011;11:348. doi: 10.1186/1471-2334-11-348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Toxoplasma gondii Antibodies, IgM, Quantitation; Toxoplasma gondii Antibodies, IgG. The Healthcare Blue Book; [2 February 2014]. www.healthcarebluebook.com. [Google Scholar]
  • 32.Hedman K, Lappalainen M, Seppala I, Makela O. Recent primary Toxoplasma infection indicated by a low avidity of specific IgG. J Infect Dis. 1989;159:736–740. doi: 10.1093/infdis/159.4.736. [DOI] [PubMed] [Google Scholar]
  • 33.Hedman K, Lappalainen M, Seppala I, Makela O. Recent primary Toxoplasma infection indicated by a low avidity of specific IgG. J Infect Dis. 1989;159:736–740. doi: 10.1093/infdis/159.4.736. [DOI] [PubMed] [Google Scholar]
  • 34.Roberts A, Hedman K, Luyasu V, Zufferey J, Bessieres JH, Blatz RM, Candolfi E, Decoster A, Enders G, Gross U, Guy E, Hayde M, Ho-Yen D, Johnson J, Lecolier B, Naessens A, Pelloux H, Thulliez P, Petersen E. Multicenter evaluation of strategies for serodiagnosis of primary infection with Toxoplasma gondii. Eur J Clin Microbiol Infect Dis. 2001;20:467–474. doi: 10.1007/pl00011289. [DOI] [PubMed] [Google Scholar]
  • 35.Cortina-Borja M, Tan HK, Wallon M, Paul M, Prusa A, Buffolano W, Malm G, Salt A, Freeman K, Petersen E, Gilbert RE, European Multicentre Study on Congenital Toxoplasmosis (EMSCOT) Prenatal treatment for serious neurological sequelae of congenital toxoplasmosis: an observational prospective cohort study. PLoS Med. 2010;7:e1000351. doi: 10.1371/journal.pmed.1000351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Gratzl R, Sodeck G, Platzer P, Jäger W, Graf J, Pollak A, Thalhammer T. Treatment of toxoplasmosis in pregnancy: concentrations of spiramycin and neospiramycin in maternal serum and amniotic fluid. Eur J Clin Microbiol Infect Dis. 2002;21:12–16. doi: 10.1007/s10096-001-0644-6. [DOI] [PubMed] [Google Scholar]
  • 37.Desmonts G, Couvreur J. Congenital toxoplasmosis: a prospective study of the offspring of 542 women who acquired toxoplasmosis during pregnancy. In: Thalhammer O, Pollak A, Baumgarten K, editors. Perinatal medicine: proceedings of the 6th European Congress, Vienna. Thieme Publishers; Stuttgart, Germany: Georg: 1979. pp. 51–60. [Google Scholar]
  • 38.Forestier F. Les foetopathies infectieuses: prevention, diagnostic prenatal, attitude pratique. Presse Med. 1991;20:1448–54. [PubMed] [Google Scholar]
  • 39.Couvreur J, Desmonts G, Thulliez P. Prophylaxis of congenital toxoplasmosis: effects of spiramycin on placental infection. J Antimicrob Chemother. 1988;22:193–200. doi: 10.1093/jac/22.supplement_b.193. [DOI] [PubMed] [Google Scholar]
  • 40.Thiébaut R, Leroy V, Alioum A, Binquet C, Poizat G, Salmi LR, Gras L, Salamon R, Gilbert R, Chêne G. Biases in observational studies of the effect of prenatal treatment for congenital toxoplasmosis. Eur J Obstet Gynecol Reprod Biol. 2006;124:3. doi: 10.1016/j.ejogrb.2005.07.019. [DOI] [PubMed] [Google Scholar]
  • 41.Foulon W, Villena I, Stray-Pedersen B, Decoster A, Lappalainen M, Pinon JM, Jenum PA, Hedman K, Naessens A. Treatment of toxoplasmosis during pregnancy: a multicenter study of impact on fetal transmission and children's sequelae at age 1 year. Am J Obstet Gynecol. 1999;180:410. doi: 10.1016/s0002-9378(99)70224-3. [DOI] [PubMed] [Google Scholar]
  • 42.Gilbert RE, Gras L, Wallon M, Peyron F, Ades AE, Dunn DT. Effect of prenatal treatment on mother to child transmission of Toxoplasma gondii: retrospective cohort study of 554 mother-child pairs in Lyon, France. Int J Epidemiol. 2001;30:1303. doi: 10.1093/ije/30.6.1303. [DOI] [PubMed] [Google Scholar]
  • 43.Jones JL, Kruszon-Moran D, Wilson M, McQuillan G, Navin T, McAuley JB. Toxoplasma gondii Infection in the United States: Seroprevalence and Risk Factors. Am J Epidemiology. 2001;54:357–365. doi: 10.1093/aje/154.4.357. [DOI] [PubMed] [Google Scholar]

RESOURCES