Oral Health in Women During Preconception and Pregnancy : Implications for Birth Outcomes and Infant Oral Health The mouth is an obvious portal of entry to the body , and oral health reflects and influences general health and well being . Maternal oral health has significant implications for birth outcomes and infant oral health . Maternal periodontal disease , that is , a chronic infection of the gingiva and supporting tooth structures , has been associated with preterm birth , development of preeclampsia , and delivery of a small-for-gestational age infant . Maternal oral flora is transmitted to the newborn infant , and increased cariogenic flora in the mother predisposes the infant to the development of caries . It is intriguing to consider preconception , pregnancy , or intrapartum treatment of oral health conditions as a mechanism to improve women 's oral and general health , pregnancy outcomes , and their children 's dental health . However , given the relationship between oral health and general health , oral health care should be a goal in its own right for all individuals . Regardless of the potential for improved oral health to improve pregnancy outcomes , public policies that support comprehensive dental services for vulnerable women of childbearing age should be expanded so that their own oral and general health is safeguarded and their children 's risk of caries is reduced . Oral health promotion should include education of women and their health care providers ways to prevent oral disease from occurring , and referral for dental services when disease is present . Introduction A woman 's preconception and pregnancy experience with the two most prevalent diseases of the mouth -- periodontal disease and dental caries -- not only influences her own oral health status but also may increase her risk of other diseases such as atherosclerosis -LSB- 1 -- 4 -RSB- , rheumatoid arthritis -LSB- 5 -RSB- , and diabetes -LSB- 6 -RSB- , impact pregnancy outcome -LSB- 7 -- 9 -RSB- , and her offspring 's risk of developing early and severe dental caries -LSB- 10 -- 13 -RSB- . Although largely preventable through evidence-based interventions , both periodontal disease and caries in women of childbearing age are highly prevalent , particularly among low-income women and members of racial and ethnic minority groups . In addition , both periodontal disease and caries are typically asymptomatic for long periods of time with only intermittent painful exacerbations . The combination of high prevalence , insufficient treatment rates , missed preventive opportunities , and intermittent symptoms led the US Surgeon General to publish a report in 2001 on oral health in America characterizing dental and oral disease as a `` silent epidemic '' -LSB- 14 -RSB- . Socioeconomic factors , lack of resources to pay for care , barriers to access to care , and lack of public understanding of the importance of oral health and effective self-care practices all represent underlying reasons cited for observed inadequacies in oral health . An important oral condition affecting many pregnant women is periodontal disease . Periodontal disease is a destructive inflammatory condition of the gingiva and bone that supports teeth . It is most commonly associated with a gram-negative anaerobic infection of these structures . Fluid that bathes the tooth at the gingival margin , known as gingival crevicular fluid , often contains inflammatory mediators and oral pathogens associated with periodontal disease . The mechanisms underlying this destructive process involve both direct tissue damage resulting from plaque bacterial products , and indirect damage through bacterial induction of the host inflammatory and immune responses -LSB- 15 -RSB- . Destructive periodontal disease affects up to 15 % of the population of childbearing age , with a relatively high proportion of pregnant women demonstrating some degree of periodontal disease -LSB- 7 , 8 , 16 -RSB- . Advancing age , smoking , and diabetes are risk factors for the development of periodontal disease -LSB- 17 -RSB- . Whereas periodontal disease is a chronic , local oral infection , systemic inflammation may also occur -LSB- 15 -RSB- . The second oral disease important to women of childbearing age because of its maternal-child health associations is dental caries . Dental caries is the pathologic process by which teeth `` decay '' and develop `` cavities . '' It occurs when acid is produced at the tooth surface by cariogenic bacteria in the dental plaque that metabolize dietary carbohydrates . Acquisition of these cariogenic bacteria , dietary practices that govern the caries process , use of fluorides that dampen the caries process , and utilization of dental care all link mothers ' and children 's experience with tooth decay through biological , behavioral , and social pathways . Is maternal oral health linked to pregnancy outcome ? Preterm birth Preterm birth , delivery at less than 37 weeks ' gestation , occurs in approximately 12 % of all births -LSB- 18 , 19 -RSB- . Prematurity is the leading cause of neonatal morbidity and mortality in non-anomalous infants -LSB- 20 -RSB- . There are numerous and heterogeneous factors associated with preterm birth , such as low maternal body mass index , maternal smoking , and maternal infections -LSB- 21 -RSB- . In 1996 , Offenbacher and colleagues -LSB- 7 -RSB- first reported a potential association between maternal periodontal disease and delivery of a preterm/low birthweight infant . In a case-control study of 124 pregnant women , they observed that women who delivered at less than 37 weeks ' gestation or an infant < 2500 g had significantly worse periodontal disease than control women . The adjusted odds ratio for delivery of a preterm , low birth weight infant was ∼ 7 ; these data led the authors to conclude that periodontal disease may represent a previously unrecognized and clinically significant risk factor for delivery of a preterm low birth weight infant -LSB- 7 -RSB- . Extrapolation from these data suggested that 18 % of the preterm , low birth weight infants born annually might be attributable to periodontal disease , and thus account for a significant proportion of the $ 5.5 billion annual hospital costs associated with the care of preterm/low birthweight infants . In a subsequent case-control study , Dasanayake et al. studied 55 pairs of women . Logistic regression indicated that mothers with ` healthy gingiva ' were at lower risk for low birth weight infants -LSB- 22 -RSB- . Women in both of these case-control studies were examined at the end of pregnancy or after delivery , which does not convincingly prove an antecedent exposure and thus causality . Despite this limitation , these early studies led to the hypothesis that periodontopathic bacteria , primarily Gram-negative anaerobes , may serve as a source for endotoxin and lipopolysaccharides , which then increases local inflammatory mediators including PGE2 , and cytokines , and that this increases systemic inflammatory mediators that can then lead to preterm birth -LSB- 23 -RSB- . Additionally , Jeffcoat et al. -LSB- 9 -RSB- examined the relationship between maternal periodontal disease and spontaneous preterm birth among 1313 pregnant women , and found that moderate/severe maternal periodontal disease identified early in pregnancy was associated with an increased risk for spontaneous preterm birth , independent of other traditional risk factors -LSB- 9 -RSB- . Despite these compelling data , it is important to recognize that other studies have failed to demonstrate any association between maternal periodontal disease and preterm birth . In a case control study conducted in London , Davenport et al. -LSB- 24 -RSB- examined 236 infants born at < 37 weeks ' gestation or < 2500 g and compared them to a random sample of 507 control infants born at ≥ 38 weeks ' gestation and weighing ≥ 2500 g . The authors found no evidence for an association between delivery of a preterm , low birth weight infant and periodontal disease and somewhat surprisingly , found that deeper mean tooth pocket depths at delivery was associated with a reduction in the risk of delivery of a preterm , low birth weight infant -LSB- 24 -RSB- . The authors surmised that these discrepant findings might be due at least in part to racial differences in study populations . In a follow-up longitudinal study of 3738 women , Moore et al. -LSB- 25 -RSB- found no association between maternal periodontal disease and preterm birth . However , there was an increase in second trimester fetal loss rates among women with periodontal disease -LSB- 25 -RSB- . In an effort to better understand the possible mechanism behind the association between periodontal disease and preterm delivery , Offenbacher and colleagues -LSB- 23 -RSB- measured gingival crevicular levels of PGE2 and IL-1ß in 48 mothers who delivered preterm , low birth weight infants compared to control women and discovered that gingival crevicular fluid levels of PGE2 were significantly higher in case compared to control women . Furthermore , among the primiparous women delivering preterm , low birth weight infants , a significant inverse association was demonstrated between birthweight and gestational age and gingival crevicular PGE2 levels -LSB- 23 -RSB- . It is not yet clear whether the relationship between periodontal disease and adverse pregnancy outcomes is causal or is a surrogate for another maternal factor . As further evidence to support the concept that maternal oral health is important for normal pregnancy outcome , other investigators have examined the effect of antepartum treatment of periodontal disease on preterm birth risk . Three published studies of antepartum versus delayed -LRB- postpartum -RRB- treatment of maternal periodontal disease demonstrate promise for this intervention for preterm birth prevention . The effect of periodontal interventions on pregnancy outcome was assessed in a prospective study designed to examine the relationship between periodontal disease and preterm low birthweight infants in a cohort of young , minority , pregnant and postpartum women . Of 164 women for whom birth outcome data were available , 74 were subjected to oral prophylaxis during pregnancy , and 90 received no periodontal treatment . The preterm/low birthweight rate was lower among women who received periodontal treatment compared to those who did not -LRB- 13.5 % vs. 18.9 % -RRB- -LSB- 26 -RSB- . Lopez et al. conducted a randomized clinical trial to assess the impact of periodontal treatment initiated during pregnancy versus delayed until postpartum on preterm low birthweight infant rates . The incidence of preterm/low birthweight infants in the antepartum treatment group was 1.8 % -LRB- 3/163 -RRB- and in the delayed/postpartum group was 10.1 % -LRB- 19/188 -RRB- , -LRB- odds ratio -LSB- OR -RSB- 5.5 , 95 % confidence interval -LSB- CI -RSB- 1.7 -- 18.2 , P = 0.001 -RRB- . Multivariable logistic regression analysis showed that periodontal disease was the strongest factor related to delivery of a preterm/low birthweight infant -LRB- OR 4.7 , 95 % CI 1.3 -- 17.1 -RRB- -LSB- 27 -RSB- . The data from these two studies suggest that treatment of periodontal disease during pregnancy could reduce preterm/low birthweight infant rates -LSB- 26 , 27 -RSB- . In a pilot intervention trial designed to assess the feasibility of conducting a trial to determine whether treatment of periodontal disease reduces the risk of spontaneous preterm birth , Jeffcoat et al. found that among women at high risk for preterm birth and presence of periodontal disease , scaling and root planning therapy initiated during pregnancy is tolerated by pregnant women and may reduce spontaneous preterm birth -LSB- 28 -RSB- . Other adverse pregnancy outcomes Preeclampsia is a hypertensive disorder of pregnancy responsible for significant , maternal and fetal morbidity and mortality . Preeclampsia affects up to 5 % of pregnant women -LSB- 29 -RSB- . The etiology of preeclampsia remains elusive . The underlying pathology may be related to a generalized intravascular hyperinflammatory state -LSB- 29 -RSB- . Some investigators have hypothesized a potential role for maternal periodontal disease as a risk factor for preeclampsia . In a retrospective analysis of data collected as part of the Oral Conditions and Pregnancy Study , Boggess et al. reported that women were at higher risk for preeclampsia if they had severe periodontal disease at delivery -LRB- adjusted odds ratio 2.4 , 95 % confidence interval 1.1 , 5.3 -RRB- , or if they had periodontal disease progression during pregnancy -LRB- adjusted odds ratio 2.1 , 95 % confidence interval 1.0 , 4.4 -RRB- -LSB- 30 -RSB- . In a case-control study , Canakci et al. found that pre-eclamptic patients were 3.5 -LRB- 95 % CI = 1.1 -- 11.9 -RRB- times more likely to have periodontal disease than normotensive patients -LSB- P < 0.01 -RRB- -LSB- 31 -RSB- . In a study of 30 pregnant women , significantly higher periodontal probing depth and clinical attachment level scores were found among preeclamptic women compared with non-preeclamptic women . Gingival crevicular fluid levels of PGE2 , TNF-α , and IL-1β levels were all significantly higher in the preeclamptic group -LSB- 32 -RSB- . Further study on the maternal and fetal inflammatory responses to chronic oral infection and on placental pathology in women with periodontal disease is needed to determine whether the relationship between periodontal disease and preeclampsia is causal or simply associative . If the relationship between maternal periodontal disease and preeclampsia risk proves causal in nature , then prevention of periodontal disease before pregnancy or treatment of periodontal disease during pregnancy may represent a novel approachs to the prevention of preeclampsia . Is maternal oral health linked to children 's experience with tooth decay ? Cariogenic bacteria are typically acquired by young children through direct salivary transmission from their mothers -LSB- 10 -RSB- . Factors influencing transmission are the levels of these bacteria in maternal salivary reservoirs , frequency and efficiency of transmission , and the child 's receptivity to implantation , which is largely diet dependent . Additional factors include timing of transmission , which is affected by the window of infectivity and the age of the child , and the composition and flow of the child 's saliva . The earlier the transmission and the more caries-supportive the diet , the earlier and more substantial the transfer will be . For this reason , mothers who have themselves experienced extensive tooth decay and therefore most likely harbor high titers of mutans streptococci in their saliva will more effectively transmit this infection vertically , thereby putting their young children at elevated risk for early childhood caries . Although maternal cariogenic bacteria can be isolated in the pre-dentate infant 's mouth -LSB- 11 -RSB- , these organisms become established in the dental plaque on the tooth surface only after teeth first appear at around six months of age . Because oral flora tends to remain stable over time , a woman 's cariogenic flora before and during pregnancy anticipates her flora during the child 's first years of life as well as the likelihood of transmitting infection early to her offspring . The lag time between infection and expression of a discernable cavity in a tooth depends upon additional factors , including the frequency of simple carbohydrate exposure in a child 's diet , oral hygiene , and exposure to fluorides . The evidence that caries is frequently established as a pathologic process in the mouths of very young children is strong , as 28 % of US children , over 4 million toddlers and preschoolers , experience one or more frank cavities by ages 2 -- 5 years -LSB- 33 -RSB- . Given the biological and behavioral pathways that govern intergenerational transmission of caries activity , disease management , and use of dental care , it is not surprising that disparities in dental caries among adults are mimicked among their children . As with adults , children of color and children of low-income families experience substantially more extensive and severe disease and less treatment than their peers without these risk factors -LSB- 33 -RSB- . Fortunately , despite the high prevalence of caries in women and children , this disease is readily preventable or manageable though early and regular dental care , exposure to fluoridated water , use of appropriate topical fluorides including those in toothpastes , application of sealants to primary teeth , and adoption of a health-promoting diet like that suggested in the Dietary Guidelines for Americans -LSB- 34 -RSB- . Is preconception preventive oral health care the answer ? It is intriguing to consider preconception , pregnancy , or intrapartum treatment of oral health conditions as a mechanism to improve women 's oral and general health , pregnancy outcomes , and their children 's dental health . Evidence is currently weakest for interventions that seek to reduce the incidence of preterm low birth weight through oral care . The mechanism of periodontal disease-associated adverse pregnancy outcomes is as yet unclear , and althoughit is hypothesized that if the ` insult ' occurs early -LRB- either at conception or implantation -RRB- the risk is greater , no direct evidence to confirms that this is the case . However , given the strong relationship between oral health conditions and periodontal disease and general health and well-being , oral health care should be a goal in its own right for all individuals . If treatment of periodontal disease is going to impact pregnancy outcomes , then it is likely that the therapy will be of greatest benefit before or in very early pregnancy . The science supporting interventions before , during , and after pregnancy to reduce caries transmission is much stronger . Educational and behavioral interventions that reduce caries activity through appropriate use of fluorides , dietary guidelines , chlorhexidine gels and varnishes , and xylitol -LSB- 35 -RSB- , can reduce a woman 's caries activity and salivary cariogenic flora , thereby improving her own oral health and , at the same time , also reducing the risk of transmission to her offspring . In two landmark Swedish studies -LSB- 12 , 13 -RSB- , children of mothers who had their cariogenic oral flora suppressed were less likely to experience cavities , more likely to develop cavities later if they were affected , and had fewer cavities than children of control mothers . Pregnancy is itself often regarded as an opportune time for anticipatory guidance and oral health education , and is a suitable time , particularly during the second trimester , for dental repair . Access to oral health care during pregnancy The CDC 's Pregnancy Risk Assessment Monitoring System -LRB- PRAMS -RRB- reported that only 23 -- 43 % of pregnant women received dental care during their pregnancies -LSB- 36 , 37 -RSB- -- a rate only half to two-thirds of US women 's overall use of dental services -LRB- 67 % -RRB- -LRB- 14 -RRB- . The PRAMS data revealed that overall , pregnant women covered by Medicaid were 24 % -- 53 % less likely to obtain a dental visit during pregnancy than women who are privately insured . Similarly , women who initiated prenatal care later than the first trimester , who did not intend the pregnancy , and who were poor were also less likely to obtain care -LSB- 36 -RSB- . In contrast , the Behavioral Risk Factor Surveillance System -LRB- BRFSS -RRB- revealed that 70 % of pregnant women in the years 1999 and 2002 had received a dental visit in the prior 12 months -LSB- 38 -RSB- . One possible explanation for the higher level reported by BRFSS is that it includes three or more months of pre-pregnancy time , during which dental care utilization would be expected to reflect the national norm for women . However , in contrast to recognized disparities in dental care utilization -LSB- 33 -RSB- , race and ethnicity were not significantly associated with dental care during pregnancy in the BRFSS study . The authors suggest that , `` the prevalence of dental visits ... probably reflects factors such as prevailing attitudes toward dental care , provider availability and practice norms , and salient features of medical and dental care delivery within the state . '' Overall , women covered by Medicaid were 24 % -- 53 % less likely to obtain a dental visit during pregnancy than women who are privately insured . Similarly , women who initiated prenatal care later than the first trimester , who did not intend the pregnancy , and who were poor were also less likely to obtain care . An important additional consideration is that dentists are reportedly reluctant to provide care to pregnant women because of concern about possible risks -LSB- 39 -RSB- . Current practice typically limits non-urgent dental treatment of pregnant women to the second trimester , as there is concern about possible teratogenic consequences during the first trimester and about the woman 's comfort in the dental chair during the third trimester . A single study relating antepartum dental radiography with full term low birth weight raised concern about the safety of dental care during pregnancy -LSB- 40 -RSB- , but was criticized for its methodology . Neither professional associations nor government agencies have promulgated any authoritative guidance regarding dental care of pregnant women , although multi-center NIH clinical trials are underway that will determine the impact of dental care for periodontal disease during pregnancy on preterm low birth weight outcomes . Currently , the New York State Department of Health is developing `` Guidelines for Prenatal Care , Oral Health , and Child Health Professionals '' that promotes routine use of dental care during pregnancy . Independent of pregnancy , the presence and source of dental insurance coverage is an important predictor of dental care utilization with publicly insured adults experiencing higher levels of oral diseases but less access to dental care . Medicaid is particularly significant to dental care of pregnant women as this program covers approximately 1/3rd of births in the US . However , states vary widely in adult Medicaid dental coverage , and at present only 7 jurisdictions providing comprehensive care to eligible adults . In contrast , low income pregnant women seeking dental services find themselves with no coverage in 8 states , coverage for only relief of pain or infection in 18 states or eligible for a limited range of services in 18 states . Three states -LRB- UT , LA , CA -RRB- have recently expanded dental benefits specifically to pregnant women in anticipation of reduced rates of unfavorable pregnancy outcomes . Pregnancy may be the only time that some low-income woman can readily obtain dental care as some state Medicaid programs provide adult dental coverage only to pregnant women or enhanced coverage during pregnancy . Conclusions and future directions Data are emerging to support a role for maternal periodontal disease as an infectious risk factor for preterm birth and other adverse outcomes of pregnancy . The prevalence of periodontal disease and the possibility of preterm birth prevention by treatment of oral infection make this a novel approach to improve the health and well being of our mothers and their soon-to-be born children . Further studies to better understand the mechanism of periodontal disease-associated preterm birth will enable us to tailor treatment to those women who might benefit the most . Data on the relationship between maternal and child experience with dental caries is well established . Therefore , regardless of the potential for improved oral health to improve pregnancy outcomes , public policies that support comprehensive dental services for vulnerable women of childbearing age should be expanded , so not only their own oral and general health is safeguarded but also so that their children 's risk of caries is reduced . Particularly if NIH trials confirm that treating pregnant women for periodontal disease reduces the incidence of unfavorable birth outcomes , the Centers for Medicare and Medicaid Services should build on its September 2004 coverage expansions for pregnant women by stimulating the states to similarly expand oral health services for pregnant women . The power of prevention needs to be brought to bear , as both periodontal disease and caries are overwhelmingly preventable through well recognized strategies including regular and effective home care for periodontal disease and use of fluorides and sealants for caries . To the degree that pregnancy provides a `` teachable moment '' in self-care and future child-care , prenatal education should universally adopt an oral health component . This educational intervention should prioritize those mothers who have suffered significantly from dental caries so that they can learn to effectively prevent transfer of this disease to their children . To be effective , oral health promotion must first seek to educate women and their health care providers about the importance of oral health and must promote an understanding of their ability to prevent and manage both periodontal disease and caries and to thereby limit the personal and intergenerational consequences of both conditions .

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O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O 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O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O B I O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O


Recruiting Injection Drug Users : A Three-Site Comparison of Results and Experiences with Respondent-Driven and Targeted Sampling Procedures Several recent studies have utilized respondent-driven sampling -LRB- RDS -RRB- methods to survey hidden populations such as commercial sex-workers , men who have sex with men -LRB- MSM -RRB- and injection drug users -LRB- IDU -RRB- . Few studies , however , have provided a direct comparison between RDS and other more traditional sampling methods such as venue-based , targeted or time/space sampling . The current study sampled injection drug users in three U.S. cities using RDS and targeted sampling -LRB- TS -RRB- methods and compared their effectiveness in terms of recruitment efficiency , logistics , and sample demographics . Both methods performed satisfactorily . The targeted method required more staff time per-recruited respondent and had a lower proportion of screened respondents who were eligible than RDS , while RDS respondents were offered higher incentives for participation . Introduction Injection drug users -LRB- IDU -RRB- remain an important population in the study of HIV/AIDS . The Centers for Disease Control and Prevention -LRB- CDC -RRB- estimates that 31.8 % of cumulative male U.S. AIDS cases through 2004 and 40.7 % of female cases were exposed through injection drug-use or male-to-male sexual contact and injection drug use .1 Unfortunately traditional sampling methods are inadequate when the population of interest consists of individuals who perform illegal or stigmatized behaviors . Injection drug users are one such population . Traditional probability-based sampling methods require the development of a sampling frame enumerating the entire population . This is prohibitive for these ` hidden ' populations because their size is unknown , and their members are often reluctant to participate in studies due to legal issues or social stigmatization .2,3 Because of these difficulties , a number of alternative sampling methods have historically been employed to study hidden populations , including injection drug users .4 These methods have included convenience sampling , time/space or venue-based sampling and chain-referral methods . Chain-referral or `` snow-ball '' sampling5 ,6 methods involve selection of an initial set of members of the target population , or ` seeds ' , who provide information on , or referrals for , subsequent waves of respondents . The number of waves and potential referrals , as well as the seed selection methods , may vary . Versions of these methods have proven successful at quickly and easily identifying members of hidden populations .7 -- 9 However , results obtained are thought to be biased by the initial seed selection method as well as characteristics of the respondents ' social network and have generally been classified as convenience samples .6,10,11 Another method proposed by Watters and Biernacki3 known as targeted sampling -LRB- TS -RRB- has had some success in recruiting injection drug users .12 Targeted sampling requires extensive ethnographic and formative research to describe the area and population of interest and to identify appropriate locations within that area for inclusion in a sampling plan .13 Existing secondary data sources are also reviewed to further describe the target population and geographic areas of interest . Qualitative data in the form of focus groups and in-depth interviews with key informants may be conducted to gain a more complete understanding of the population of interest as well as to identify possible specific locations for sampling . These locations are then systematically mapped and ethnographic observations are conducted . Based on all of this information a sampling frame of locations is developed and weighted by the density of observed indicators . Locations are randomly selected and recruitment is conducted within the selected locations . Targeted sampling , as well as other time -- space or venue-based sampling methods , may be biased to the extent that members of the population of interest do not attend the venues or areas that have been identified . Heckathorn10 ,14,15 has recently proposed a modified chain-referral method called respondent-driven sampling -LRB- RDS -RRB- as a promising strategy in surveying hidden populations . This approach retains the advantages of chain-referral sampling in terms of ease of respondent identification and recruitment while allowing population estimates and inferences to be made .10,15 Initial seeds are identified from known members of the population or through key informants . Information about the respondent 's social network is collected , and seeds are provided with a set number of coupons for distribution to recruits within their own network . Eligible recruits are interviewed and provided coupons for distribution to the next ` wave ' . Recruitment continues in this way until the desired sample size is reached . Network information is then used to derive asymptotically unbiased population estimates for variables of survey interest . RDS has been shown to be a useful strategy for the recruitment of drug users .16 -- 18 To date , however , no direct comparison of RDS with other sampling methods has been made in terms of the ability to recruit hidden populations such as IDUs , the `` representativeness '' of sample characteristics , and the practicality of administration .2,4 The objective of the current study is to compare and contrast RDS and TS methods on demographics , recruitment efficiency , and logistic concerns . Materials and Methods Three sites in large Metropolitan Statistical Areas -LRB- MSA -RRB- -LRB- Detroit , Houston and New Orleans -RRB- that participated in the CDC-funded National HIV Behavioral Surveillance among injecting drug users -LRB- NHBS-IDU -RRB- conducted a pilot investigation comparing RDS and TS . Each site assessed the feasibility of recruiting at least 100 eligible IDUs utilizing RDS and TS methods over an 8-week period in late 2004 . What follows is a brief presentation of the strategies used by each site to locate and recruit potential respondents using RDS and TS methods . Targeted Sampling Formative Research Extensive ethnographic and formative research was conducted at all sites prior to sampling . Each site completed a thorough review of secondary data sources dealing with the IDU population . Data were compiled and synthesized from several sources including number of persons living with HIV/AIDS who have IDU as a reported mode of exposure , archival census data and findings from previous published and unpublished research . A total of 81 in-depth interviews were conducted with individuals who had knowledge of local injection drug-use communities . Those interviewed included local HIV prevention personnel and community planning group members as well as law enforcement representatives and current or former injectors . Ten focus groups with a total of 78 injection drug users were also conducted in order to provide specific knowledge about local injection habits and behaviors . These structured interviews were designed to provide a fuller understanding of the injection community at large as well as to solicit locations for possible sampling areas . Sites also utilized information on areas that had been previously identified by ethnographers with knowledge of the local IDU community or had been used in other local IDU studies . Area Identification and Recruitment Field observations of the possible sampling areas were systematically conducted at varying times of day and week over the course of 5 months -LRB- March -- July 2004 -RRB- . Field staff conducted ethnographic observations within each area and recorded any IDU indicators that were present . IDU indicators included physical objects such as used syringes , baggies , balloons or injection works/equipment as well as behavioral indicators such as copping activity , loitering or commercial sex work . Sites used a combination of ethnographic research , secondary data analysis , key informant interviews , and field observations to form expected yield ratings to identify areas where injection drug use was likely to occur and where potential survey respondents could be recruited . Based on highest expected yield rating , Detroit and Houston identified four and ten sampling areas , respectively , within seven ZIP codes . For these sites line based enumeration was then used to approach possible respondents . New Orleans identified 35 sampling areas within 16 ZIP codes of high , medium and low expected yield . These ZIP codes were stratified by the expected yield , and order of ZIP codes was then randomly selected without replacement at the beginning of each 2-week period . Interviewers approached all individuals within each of the prescribed three block sampling areas within each ZIP code . Respondent-Driven Sampling Seed Selection and Recruitment Possible seeds were identified through key informant referrals and street outreach . Seeds were purposefully selected to maximize diversity on race , sex and drug of choice . Each seed was screened , and eligible seeds were interviewed using the NHBS-IDU instrument and provided with a $ 20 cash value incentive . Each initial seed was provided with three recruitment coupons and instructed to give them to individuals they knew injected drugs . Seeds were also informed that they would be compensated with $ 10 cash value for each person that they recruited . Peer-recruited respondents returning these coupons were then screened for eligibility , interviewed and provided with three coupons they were instructed to give to someone who they knew injected drugs . They were told that they would be compensated $ 10 for each person they recruited . A specialized coupon tracking system database was used to track referrals and facilitate incentive provision . Analysis All RDS participants were asked to provide information about the size and characteristics of their social networks from which they would draw potential recruits . Specifically , each participant was asked to report the number , sex and race/ethnicity of injectors they knew and had seen in the past 6 months . Relationship of the respondent to the recruiter -LRB- e.g. , friend , injection partner , sex partner etc. -RRB- was also assessed . This information along with data from the coupon tracking system was analyzed using Respondent-Driven Sampling Analysis Tool -LRB- RDSAT -RRB- software -LRB- RDSAT -LRB- computer version -RRB- . Version 5.4.0 . Ithaca , New York : Volz E , Heckathorn DD ; 2005 -RRB- to provide estimated population proportions and confidence intervals for age , sex and race/ethnicity variables . Participants All participants provided informed consent and were carefully screened for eligibility criteria . Eligibility criteria for study participation were that the respondent was at least 18 years of age , was resident of the study MSA and had injected illicit drugs within the past 12 months . Targeted Sampling In Detroit 273 individuals were approached during TS . Two hundred twenty one individuals agreed to participate and were screened for eligibility . Of TS screened participants , 54 % -LRB- n = 120 -RRB- were found to be eligible and completed the survey . In Houston 174 individuals were approached during TS . One hundred forty eight respondents agreed to participate and were screened for eligibility . Of TS screened participants , 65 % -LRB- n = 97 -RRB- were found to be eligible and completed the survey . In New Orleans 560 individuals were approached during TS . Three hundred eighty-nine respondents agreed to participate and were screened for eligibility . Of TS screened participants , 35 % -LRB- n = 137 -RRB- were found to be eligible and completed the survey . Respondent-Driven Sampling Six seeds were approached in Detroit for participation , and three of those individuals completed the survey and agreed to be seeds . One hundred sixty-nine recruitment coupons were distributed by Detroit during RDS over nine waves of recruitment ; 106 of those individuals returned and were screened for eligibility . Of RDS screened participants , 96 % -LRB- n = 102 -RRB- were found to be eligible and completed the survey . Thirteen seeds were approached in Houston for participation , and one additional seed was recruited after being interviewed in the targeted sampling component . Of the 14 seeds recruited , 1 was found to be ineligible . One hundred sixty-eight recruitment coupons were distributed during RDS over seven waves of recruitment ; 62 of those individuals returned and were screened for eligibility . Of RDS screened participants , 77 % -LRB- n = 48 -RRB- were found to be eligible and completed the survey . Ten seeds were approached in New Orleans for participation , and two of those individuals completed the survey and agreed to be seeds . Three hundred sixteen recruitment coupons were distributed during RDS over 19 waves of recruitment ; 133 of those individuals returned and were screened for eligibility . Of RDS screened participants , 88 % -LRB- n = 118 -RRB- were found to be eligible and completed the survey . Materials The standardized NHBS-IDU questionnaire was administered to all eligible participants . This 68-item questionnaire on HIV risk behaviors , requiring approximately 40 min , includes items on demographic characteristics , drug use , sexual risk behaviors , access to and use of health care and utilization of HIV prevention services . Variables of interest for this study included respondent demographic information , time required for survey completion , and cost of each survey . Results Sample Characteristics Demographic characteristics of the samples obtained for each site by method are presented in Tables 1 , 2 , and 3 . Local HIV surveillance data on persons living with HIV/AIDS who have injection drug use as a reported mode of exposure are presented for comparison purposes only . Chi-square tests indicated no significant association of sampling method and gender for any site -LRB- Detroit : , P = 0.33 ; Houston : , P = 0.38 ; New Orleans : , P = 0.23 -RRB- . No significant association between age and sampling method was found -LRB- Detroit : , P = 0.52 ; Houston : , P = 0.14 ; New Orleans : , P = 0.23 -RRB- . Two sites showed significant association between race/ethnicity and sampling method -LRB- Detroit : , P = 0.42 ; Houston : , P = 0.01 ; New Orleans : , P < 0.0001 -RRB- . Table 1Demographic characteristics of Detroit IDUs obtained through RDS and TS , and persons living with HIV/AIDS who are injection drug users -LRB- PLWH/A-IDU -RRB- TSRDSRDS pop . estimates , % -LRB- 95 % CI -RRB- PLWH/A-IDU , -LRB- % -RRB- Race/ethnicityN % N % African American101949696 -- 91White 0011 -- 5Hispanic1111 -- 3Other6622 -- 0Sex/genderMale7469717163 -LRB- 52 -- 75 -RRB- 61Female3431242437 -LRB- 25 -- 48 -RRB- 39TransgenderAge18 -- 3421220.1 -LRB- 0.2 -- 0.7 -RRB- 435 -- 442423202017 -LRB- 7 -- 27 -RRB- 2245 -- 546560545451 -LRB- 40 -- 67 -RRB- 4755 +1716242432 -LRB- 16 -- 43 -RRB- 27Table 2Demographic characteristics of Houston IDUs obtained through RDS and TS , and persons living with HIV/AIDS who are injection drug users -LRB- PLWH/A-IDU -RRB- TSRDSRDS pop . estimates , % -LRB- 95 % CI -RRB- PLWH/A-IDU , -LRB- % -RRB- Race/ethnicityN % N % African American42522745 -- 69White22281423 -- 20Hispanic10121932 -- 10Other6700 -- 1Sex/genderMale5367467776 -LRB- 45 -- 96 -RRB- 56Female2025122024 -LRB- 4 -- 55 -RRB- 44Transgendera6823Age18 -- 342634122014 -LRB- 0.1 -- 31 -RRB- 1735 -- 442228254141 -LRB- 33 -- 86 -RRB- 4045 +3039244045 -LRB- 5 -- 60 -RRB- 43aFemale and transgender categories were combined for purposes of Houston 's RDS analyses.Table 3Demographic characteristics of New Orleans IDUs obtained through RDS and TS , and persons living with HIV/AIDS who are injection drug users -LRB- PLWH/A-IDU -RRB- TSRDSRDS pop . estimates , % -LRB- 95 % CI -RRB- PLWH/A-IDU , -LRB- % -RRB- Race/ethnicityN % N % African American12589675877 -LRB- 64 -- 90 -RRB- 65White54342920 -LRB- 9 -- 34 -RRB- 33Hispanic11223 -LRB- 0.1 -- 3 -RRB- 2Othera9613110Sex/genderMale11985948174 -LRB- 58 -- 88 -RRB- 76Female1914221926 -LRB- 12 -- 42 -RRB- 24Transgender21Age18 -- 343726342927 -LRB- 15 -- 43 -RRB- 1635 -- 444431262227 -LRB- 12 -- 44 -RRB- 3545 -- 544029443839 -LRB- 21 -- 57 -RRB- 3755 +191412107 -LRB- 2 -- 13 -RRB- 12aHispanic and other race/ethnicities were combined for purposes of New Orleans ' RDS analyses . Also presented are the population estimates and confidence intervals obtained by RDSAT . No RDS population estimates were calculated for race/ethnicity for Detroit or Houston due to lack of cross-group recruitment -LRB- e.g. , only African Americans were recruiters of other race/ethnicities in Detroit -RRB- . For each RDS estimate presented , equilibrium was achieved . Cost Effectiveness Across all sites 47 % of TS-screened respondents were found to be eligible IDUs , while 89 % of screened respondents in RDS were eligible IDUs . TS required an average of 214 h performing ethnographic observation and mapping plus an average of approximately 2 h and 9 min of staff time locating , screening and interviewing each recruit -LRB- total = 4 h and 6 min per recruit -RRB- while RDS required approximately 1 h and 13 min per recruit . TS methods provided each participant with an average of $ 20 in incentives , while RDS recruits received an average of $ 26.68 . RDS incentives did not total $ 50 for every participant because some respondents did not produce the maximum of three recruits , and some recruiters did not return to receive the added incentives for recruitment efforts . Logistics Staffing requirements were similar for both methods , and sites were able to use the same staff to conduct RDS and TS concurrently . Some differences were evident as a result of method selection . Targeted sampling was conducted in the field while RDS was usually conducted from a single storefront . Interviewers reported that this led to a more controlled environment when using RDS . Increased privacy , comfort and perceptions of safety were reported , while distraction level decreased . Weather was also more of a concern with TS while interviewing outdoors . Discussion The use of multiple sources of ethnographic data was beneficial in identifying high-yield TS recruitment areas because areas with the highest number of eligible recruits were often not necessarily areas with obvious drug use indicators but areas identified through HIV surveillance or key-informant interviews . However , even with good ethnographic information , many areas that were expected to be high-yield were not , and less than half of all individuals approached were found to be eligible . This led to low interviewer morale in Detroit , where the interviewers were paid per interview completed . It also led to some bias in recruitment in Houston , where interviewers made the decision to recruit only individuals who looked like injection drug users on one particularly unsuccessful recruitment day . The sample characteristics of those recruited through TS may not reflect the general IDU population but rather the population found during the recruitment times . New Orleans included low density areas and randomized area selection in the hopes of assembling a diverse sample , reflective of the general IDU population . However , this did not happen . The sample characteristics were reflective of the population found during recruitment times , and the sample may have missed less visible injectors , such as those with steady day time employment or child care responsibilities and those who remain indoors during the day or only come out at night . Houston and Detroit had similar problems . One solution might be to extend recruitment hours into the night or start very early in the morning , but this would further increase security concerns . TS offered less control in the working environment , compared to RDS . Safety was a concern : The interviewers tended to spread out in the targeted area and the interviewing process drew the attention of others . Groups often gathered to inquire about the interview and the incentive , heightening security concerns . Weather was also an important factor in recruitment success , as fewer individuals were on the streets during hot , cold , or rainy days , and the spring and summer of 2005 was particularly noteworthy , weather-wise . Overall the RDS storefront was preferable to conducting TS outdoors . Participants often scheduled interview appointments and came to a central location for their interviews . Adequate staffing and office space were essential . It was found to be best to have a general waiting area , private interview spaces for each interviewer , and an area for obtaining participants ' coupon information and providing incentives . In addition , all sites concurred that a single staff person to monitor the flow of participants entering , waiting , and exiting the facility would have provided even more control of the environment . RDS success depends largely on the effective recruitment of seeds , an inter-connectedness of injection drug use networks , and the willingness of seeds and their recruits to travel to an interview location . Community partnerships were also important in the recruitment of successful seeds . In Detroit , seeds were recruited from two needle exchange locations in the city at the recommendation of staff familiar with the individuals ' ability to recruit others . This worked well in Detroit , where three of six recruited seeds led to the recruitment of 106 eligible IDUs . In Houston , the initial seeds were recruited from outreach workers who were conducting other research studies in drug-using populations . This was problematic , as some of these initial seeds were not actually linked to the injection drug using community but rather spent their days recruiting participants for these other research projects . These `` research hustler '' seeds were often very good at recruiting individuals -LRB- for money -RRB- , just not at recruiting eligible individuals . This resulted in very short referral chains since few of their recruits were eligible . In New Orleans , staff were only able to successfully recruit two seeds . Eight others identified through key informants agreed to participate but never came to the field location to be interviewed . The two seeds that were interviewed represented the two subgroups of the overall sample , as described in the formative research . One seed was an older African American male , the other a younger white female . The race/ethnicity and age differences between the New Orleans RDS sample -LRB- 29 % white , 19 % under 25 -RRB- and the TS sample -LRB- 4 % white , 5 % under 25 -RRB- may have reflected the characteristics of the two seeds ' networks rather than methodological differences . Based on lessons learned in this pilot , when NHBS-IDU shifted to full implementation , the sites made several adjustments to the RDS protocols . In New Orleans , prior to the discontinuation of the project due to Hurricane Katrina , seeds were recruited from among participants who were known to interviewers from the TS pilot and who encouraged others to be interviewed . Second , two field offices were established ; one was close to downtown and easily accessible by public transportation and the other was near a large public housing project in an area that yielded high eligibility rates in TS . Finally , transportation tokens were purchased and made available to participants who came to the field office in an attempt to ease the burden of travel on respondents . In Houston , successful seeds were individuals the interviewers/outreach workers found during the formative work for the targeted pilot . These were influential individuals or gatekeepers within small communities of injection drug users , often the individuals who were first to approach staff and inquire why interviewers were entering their geographic space . Discontinuing RDS recruitment required some special considerations . While targeted sampling may easily stop on any given date or after a pre-determined number of participants have been recruited , the coupons distributed to potential RDS subjects represent a commitment on the part of the researcher . It was therefore important to carefully decrease the number of coupons distributed and shorten the coupon validity period so that recruitment would continue even as the end of the study date approached . Ending the distribution of coupons too early may result in not meeting the recruitment goal -LRB- in this case 100 participants -RRB- , while ending it too late may lead to a disgruntled public . Overall , both RDS and TS proved effective in recruiting IDUs in the three pilot MSAs . Although no claim as to the actual representativeness of the obtained samples is made , both methods yielded samples that were similar in terms of many demographic characteristics -LRB- such as age , race and sex -RRB- as well as drug of choice -LRB- not presented here -RRB- . Demographic results of the samples from both methods also compared favorably to each city 's Census and HIV surveillance data from injection drug users . All three sites were able to reach the goal of 100 respondents in TS . Issues with initial seed selection and time constraints most likely resulted in the failure of one site to recruit 100 respondents with RDS . Total cost efficiency for the two methods was also comparable . Extensive formative research and low screened-to-eligible respondent ratios resulted in larger person-hour expenditures for TS , while RDS required higher incentive payouts to participants . Logistical concerns did differ considerably between the two methods . While RDS provided a more controlled interview environment , recruitment success seemed to be affected by the ability to identify quality seeds . Quality of ethnographic assessment and size and cultural qualities of the MSAs also affected targeted sampling success . While more research is needed in assessing the methodological impact of choice of sampling method in identifying hidden populations , these experiences should provide researchers some insight into the some of the practical strengths and weaknesses of these two methods .

O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O

sampling methodology
respondent-driven sampling
targeted sampling.