Abstract
Background
Tobacco has regained the status of the world’s number two killer behind heart/vascular disease. Thirdhand smoke (THS) residue and particles from secondhand smoke (SHS) are a suspected health hazard (e.g., DNA damage) that likely contributes to morbidity and mortality, especially in vulnerable children. THS is easily transported and deposited indoors where it persists and exposes individuals for months, creating potential health consequences in seemingly nicotine-free environments, particularly for vulnerable patients. We collected THS data to estimate infant exposure in the neonatal ICU (NICU) after visits from household smokers. Infant exposure to nicotine, potentially from THS, was assessed via assays of infant urine.
Methods
Participants were mothers who smoked and had an infant in the NICU (N=5). Participants provided surface nicotine samples of their fingers, infants’ crib/incubator, and hospital-provided furniture. Infant urine was analyzed for cotinine, cotinine’s major metabolite: trans-3′-hydroxycotinine (3HC), and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL), a metabolite of the nicotine-derived and tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK).
Results
Incubators/cribs and other furniture had detectable surface nicotine. Detectable levels of cotinine, 3HC, and NNAL were found in the infants’ urine.
Discussion
THS appears to be ubiquitous, even in closely guarded healthcare settings. Future research will address potential health consequences and THS-reduction policies. Ultimately hospital policies and interventions to reduce THS transport and exposure may prove necessary, especially for immunocompromised children.
Keywords: Thirdhand smoke, THS, environmental tobacco smoke, neonatal intensive care unit, NICU
1. INTRODUCTION
Thirdhand smoke (THS) results from secondhand smoke (SHS) and is a distinct public health hazard.[1,2,3] THS-related harm (compared to SHS) has been predicted at 5%-60%,[4] and THS has been related to cardiovascular and lung disease (e.g., via inflammatory cytokines, implicated in diseases like asthma)[5] and hindered respiratory development in animal models.[6] In-vitro studies have reported DNA damage[7] and impaired wound healing.[8]
THS is difficult to remove,[9,10,11] can persist for ≥18 months,[12] reacts with extant compounds, forming new toxicants and carcinogens,[13,14,15,16] and is reemitted slowly over long time periods well after smoking has ceased.[2,3,11,17] Further, smoking outdoors does not fully protect homes/residents from SHS/THS,[17,18,19] as THS dispersal (e.g., smokers’ clothes) and exposure routes (e.g., dermal absorption) are numerous.[10,16,20,21]
Studies find that non-smokers occupying homes vacated by smokers (or staying in non-smoking hotel rooms) had elevated finger nicotine, urine cotinine, and THS-related carcinogens.[10,22] These findings are concerning for premature, low-birth-weight infants exposed to THS. Approximately 50% of infants born <1500 grams will be ventilated in the neonatal ICU (NICU) and 22% will develop bronchopulmonary dysplasia (BPD).[23] Ventilation is life-saving but leads to long-term damage (decreased lung volume)[24] and BPD is associated with increased risk for pneumonia, asthma, repeated hospitalizations, neurodevelopmental problems, and death.[23] Over a quarter of NICU infants are discharged to a home with ≥1 smoker,[18] making this a sizable population at risk for potential THS-related harm. Despite non-smoking policies, SHS levels in hospitals are detectable,[25] as 25–60% of hospitalized smokers and visitors step outside to smoke and then reenter[26,27]. Healthcare provider smoking may contribute as well, as data from 2007 showed 2.3% of physicians, 10.7% of registered nurses, and 19.2% of respiratory therapists smoke or live with a smoker.[28]
This pilot was undertaken to determine whether detectable THS levels (surface nicotine) could be found inside the NICU after smokers visit, which is important as microbes found on NICU surfaces have later been found in premature infants’ intestines.[29] Infant-nicotine exposure, potentially from THS, was assessed via infant urine samples. It is plausible that THS/SHS exposure on discharge from the NICU may contribute to infant morbidity and mortality (e.g.,SIDS)[30,31,32]. This study was designed to provide proof of exposure at birth for vulnerable babies.
2. METHODS
Smoking mothers with an infant (N=5) admitted to a NICU, participating in a study to reduce SHS exposure in their homes, were recruited. Research associates obtained IRB-compliant consent. Participants provided a THS (surface nicotine) wipe of their index finger, infants’ incubator/crib, and a hospital-provided chair/couch (furniture; see Table Note) inside infants’ NICU rooms. Participants consented to infant urine collection and answered smoking-behavior, breastfeeding, and visitation questions.
Table 1.
Participant | ||||||
---|---|---|---|---|---|---|
| ||||||
Characteristic (Measure) | 1 | 2 | 3A | 3B | 4 | 5 |
Cigarettes Today | NC | 0 | 8 | 3 | 0 | 1 |
Wash Hands after Last Cigarette | NC | N/A | No | No | N/A | Yes |
Wash Hands during Visit | No | No | No | No | No | No |
Smoked While Pregnant | No | No | Yes | Yes | No | |
Typical Cigarettes per Day | 5 | 0A | 20 | 5 | 0A | |
Days of Visitation (out of Last 7) | NC | 7 | 0 | 1 | 7 | 7 |
Day of Life/Infant HospitalizationB | 46 | 22 | 34 | 55 | 9 | 11 |
Visitation Minutes (on Study Visit) | 60 | 180 | 140 | 90 | 45 | >180C |
Infant Held at Visit | No | Yes | Yes | Yes | Yes | Yes |
Protective Gown Worn at Visit | NC | No | Yes | Yes | No | Yes |
Protective Gloves Worn at Visit | NC | No | No | No | No | No |
# of Other Household Smokers | 2 | 4 | 2 | 2 | 2 | |
Do Other Household Smokers Visit | NC | Yes | Yes | Yes | Yes | |
Indoor Home Smoking Allowed | No | Yes | Yes | Yes | No | |
Smoking Allowed Inside Car | Yes | Yes | No | Yes | Yes | |
Breastfed Infant in Last 10 days | No | No | No | No | Yes | Yes |
Feeding Type at VisitD | Bottle | Bottle | Bottle | Bottle | BottleD | Breast |
Index Finger and Furniture Data | ||||||
Index Finger Nicotine (ng) | NC | 44 | 1160 | 4,960 | 90 | 818 |
Crib/Incubator (μg/m2) | <LOD | 0.3 | 0.2 | NC | 0.2 | 0.2 |
Furniture (μg/m2) | 0.3 | 2.5 | 5.5 | 34.2 | 1.2 | 3.4 |
Infant Urine Data | ||||||
Cotinine (ng/ml) (LOQ=0.05) | NC | 0.17 | 0.36 | NC | 0.37 | 5.01 |
3HC (ng/ml) (LOQ=0.1) | NC | 0.63 | 0.46 | NC | <LOQ | 31.58 |
NNAL (pg/ml) (LOQ=0.25) | NC | 0.47 | 1.64 | NC | 1.58 | 12.38 |
Note. Participant 3’s visit 1 is labeled as “3A” and visit 2 is labeled as “3B”. Participant 1’s crib/incubator result was below the limit-of-detection (LOD; 0.1 μg/m2). The incubator measurement was not repeated for participant 3’s second measurement (i.e., PPT3B). “Cigarettes Today”=Cigarettes smoked on the day of the assessment; “Wash Hands after Last Cigarette”=On the day of the assessment, did the participant report washing their hands after their most recent cigarette; “Wash Hands during Visit”=On the day of the assessment, did research staff observe the participant washing their hands; “N/A”=Not applicable; “Days of Visitation”=Number of days visited out of the last 7 days (not including the day of the visit); “Visitation Minutes (on Study Visit)”=Number of minutes visited on the day of sample collection; “Infant Held at Visit”=Did staff observe the participant holding the infant on the day of the assessment; “Protective Gown (or Gloves) Worn at Visit”=Did the staff observe the participant wearing protective gowning/gloves on the day of the assessment; “NC“=Not collected; “# of Other Household Smokers”=Number of other smokers who live in the household; “Feeding Type at Visit”=Was the infant bottle fed or breastfed on the day of the assessment. “Furniture” = A hospital-provided couch or chair. For couches, the inner material was 100% polyurethane foam and the outer upholstery was made of 90% vinyl and 10% urethane. For chairs, the inner material was 90% polyurethane foam and 10% polyester fiber and the outer upholstery was made of 100% Paloma leather.
Participants 2 and 5 reported smoking fewer than 1 cigarette a day.
All 5 infants were admitted to the NICU on their date of birth.
Participant 5 was rooming with her infant since the infant’s admission.
On the day of the assessment, participants 1–3 were bottle fed formula and participant 5 was breastfed. We did not assess whether the fluid in the bottle was expressed breastmilk or formula for participant 4.
THS-surface-nicotine wipes were collected with standardized procedures;[10,17,22,33]. Briefly, a 10cm × 10cm template was taped to the arm of the couch or chair and a screened cotton wipe, doused with a distilled-water and 1%-ascorbic-acid solution was used to wipe inside the template. For cribs, the top railing was measured and wiped. Wipe values were standardized and reported in micrograms per meter squared (μg/m2), except for finger wipes and “blanks” (i.e., no sample is taken but all other procedures are followed), which are reported in nanograms (ng/wipe). Surface nicotine was quantified using established methods.[34] The limit-of-detection (LOD) for surface nicotine is 0.1 μg/m2.[33] Participant 3′s infant’s room was sampled twice.
Urine samples (collected on the day of wipe collection) were analyzed for cotinine (nicotine’s primary metabolite), 3′-hydroxycotinine (cotinine’s primary metabolite; 3HC), and 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL; metabolite of the nicotine-derived and tobacco-specific carcinogen, 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone [NNK]).[7] Urine was extracted via syringe from 2 cotton pads placed in the infants’ diapers.[35] Published methods were used for quantifying cotinine, 3HC,[36] and NNAL.[37] The limit-of-quantification (LOQ) of NNAL is 0.25 picograms (pg)/ml; cotinine’s LOQ is 0.05 ng/ml; and 3HC’s LOQ is 0.1 ng/ml.
3. RESULTS
All 5 infants were admitted to the NICU on their date of birth. All values have been adjusted by subtracting out nicotine found in blanks (M=2.6 ng/wipe). All participants reported living with other smokers, that other smokers visited the infant, and allowing smoking inside their homes or cars or both.
There was greater variability across other factors likely to be associated with surface nicotine and urine outcomes (see Table). Participants tended to report light smoking (<10 cigarettes/day)[38,39] and most participants visited daily. Participant 1’s, 2’s, and 3’s infants were hospitalized for ≥3 weeks and all reported discontinuing or never initiating breastfeeding. Participant 4’s and 5’s infants were hospitalized <2 weeks and both reported current breastfeeding. Participants 2 and 4 did not smoke on the day of measurement and had low finger nicotine levels; whereas, participants 3 and 5 smoked on the collection day and had greater finger nicotine levels.
Surface nicotine levels of all incubators/cribs were similar and within the lower range of surface nicotine found inside smoking households that ban indoor smoking.[17] THS levels on furniture tended to be much higher and were similar to average levels generally observed in smoking households that ban indoor smoking. However, the one repeated furniture measurement taken (participant 3) was substantially higher at the 2nd measurement and suggested a value closer to a home that allows indoor smoking[17] (see Supplementary Figure 1).
Data for infant urine cotinine, 3HC, and NNAL were all >LOQs for each respective metric, except participant 4’s 3HC. Participants 2, 3, and 4 had highly similar cotinine, 3HC, and NNAL values. Participant 5’s infant was still breastfeeding and had greater cotinine, 3HC, and NNAL values (see Table).
4. DISCUSSION
For NICU infants visited by smokers, THS may be transported to and adhere to surfaces in the NICU at levels which are similar to those found in households where smokers reside. Further, this pilot study of NICU infants from smoking households were exposed to measurable levels of nicotine and a known carcinogen (NNK), raising the possibility of exposure due to THS reemission (off-gassing). These findings demonstrate that exposure is taking place in at least one NICU and raises the possibility that such exposure contributes to morbidity and premature mortality in vulnerable babies. Results warrant confirmation and more complete assessment of NICU micro-environments, sources of contamination, and their relationships to home environments to which children are discharged.
A majority of samples had surface nicotine levels above the LOD and one had a level commonly found in households that permit indoor smoking. Surface nicotine levels on infants’ incubators/cribs tended to be lower than furniture levels. Infants receive a new, thoroughly cleaned incubator every 30 days, which is not true of furniture. Other possibilities for lower levels include increased cleaning attention for cribs/incubators or relatively little time spent at the crib’s side in favor of sitting on the furniture. The greater levels on NICU furniture could suggest that clothing worn by visitors is transferring much of the THS residue.
These data have implications for further research and policies. For example, whether NICU exposures will cause acute or long-term harm is unknown. However, there is no safe level of SHS[40] and whether there is a safe level of THS exposure for immuno-compromised infants is yet to be verified by large, long-term epidemiological studies.
NICUs often require visitors to wash/sanitize their hands, wear protective gowns or gloves, and take other precautions before entering the NICU. We only recorded data on these practices on the day of the assessment, and incomplete use of protective gowns/gloves and handwashing by study participants was observed. Two (of five) participants smoked on the assessment day and only one reported washing their hands since their most recent cigarette. Research staff did not observe any glove use or handwashing. Studies show handwashing policies are not universally enforced (e.g., a review of hand washing in 65 ICUs reported 40% median compliance)[41] and it is unknown whether hand washing or sanitization significantly reduces the amount of nicotine transported. Further research on the effectiveness of these procedures for reducing THS is clearly needed.
This initial, post-hoc study has limitations. For example, the half-life of NNAL in adults is approximately 10–16 days[42] and the half-life for infants (and how long in utero exposure takes to wash out) is unknown. Thus, some (or all) of the infants’ NNAL may have come from in utero exposure via the mother. Cotinine has a much shorter half-life of 16–22 hours, which is similar for adults and infants,[43,44] but less understood in premature infants. Further, this small sample is unable to tease out the influence of other variables including previous-room-occupant smoking, staff smoking, visitation frequency/length (including visitation by other household members), and breastfeeding (particularly for 2 participants). Also, we assessed infant rooms where the mother was a smoker (and other smokers visited), which likely have greater levels of nicotine deposits than infants visited by non-smokers. Residual nicotine adhesion and dynamics differ across surface type [e.g., 12,45]. Surface-nicotine variability has been found across settings, including dashboards sampled in rental cars (interquartile range [IQR]: 0.1–3.1 μg/m2 [designated-smoking cars]; 0.0–1.2 μg/m2 [designated non-smoking cars])[46]; homes (IQR: 0.7–13.7 μg/m2)[19]; and, hotels show significant variability based on indoor-smoking-ban policies. For example, non-smoking hotels (IQR: 0.0–3.4 μg/m2) have the least surface nicotine, and non-smoking (IQR: 0.0–10.3 μg/m2) and smoking rooms (IQR: 7.3–353.2 μg/m2) in hotels without complete bans tend to have the greatest surface nicotine. Finally, research should quantify the cumulative amount of THS that is absorbed by ongoing contact, as much of the health effect may be due to a relatively large “dose” achieved by cumulative exposure. These data raise questions that require replication with rigorous methodology in larger samples.
5. CONCLUSION
This research highlights THS’s pervasiveness, even in closely guarded healthcare settings. Future work is needed to understand exposures and health consequences in such a vulnerable population. Indeed, the death rate among NICU infants is high[18] and the role of environmental carcinogens is unknown. It may be important to implement hospital policies and interventions to reduce THS exposure, even ahead of causal data given the potential risks for NICU patients. Extending smoke-free policy definitions to include THS could have the added benefit to hasten the elimination of SHS in other environments.[31]
Supplementary Material
WHAT THIS PAPER ADDS.
Thirdhand smoke (THS) contamination is unexplored in non-smoking, protected medical environments visited by smokers.
THS is estimated to take weeks to months to degrade in controlled environments.
Infants cared for during extended stays in neonatal intensive care units (NICUs) are protected from secondhand smoke but exposure to THS is unknown.
This study demonstrated that THS is deposited in rooms of NICU infants visited by smokers.
Data showed that NICU infants are exposed to nicotine and nicotine-derived, tobacco-specific carcinogens, raising the possibility of exposure due to THS reemission in the NICU.
These data justify more formal research documenting acute and cumulative THS exposure, sources of exposure, means of prevention, and associations with morbidity/mortality for NICU infants.
Acknowledgments
The authors wish to thank Maleeha Arshad, Mary MacGregor, Maria Ortiz, Mackenzie Spellman, Jennifer Meeks, Lora Bunge, and Rose Young for their help initiating and conducting the study. Kayo Watanabe and Dana Datuin assisted with the surface nicotine analysis. Additionally, the authors would like to thank the staff of the Children’s Memorial Hermann Hospital.
FUNDING
This work was supported by the National Heart, Lung, and Blood Institute (R01 HL107404, PI=A.L. Stotts; R01 HL103684-02, PI=M.F. Hovell) and the National Institute on Drug Abuse (P30 DA012393; PI=Reese T. Jones) at the U.S. National Institutes of Health, and Department of Health and Human Services. This work was also supported by the California Consortium on Thirdhand Smoke, California Tobacco-Related Disease Research Program (20PT-0184; PIs=N.L. Benowitz & P. Jacob) and the California Tobacco-Related Disease Research Program (TRDRP) for “Certifying Smoke-Free Used Cars: Effects on Value and Consumer Behavior” (21RT-0142; PI=G.E. Matt).
Footnotes
COMPETING INTERESTS
The authors have no competing interests to declare.
Contributor Information
Thomas F. NORTHRUP, Email: Thomas.F.Northrup@uth.tmc.edu.
Amir M. KHAN, Email: Amir.M.Khan@uth.tmc.edu.
Peyton JACOB, III, Email: Peyton.Jacob@ucsf.edu.
Neal L. BENOWITZ, Email: Neal.Benowitz@ucsf.edu.
Eunha HOH, Email: EHoh@mail.sdsu.edu.
Melbourne F. HOVELL, Email: MHovell@mail.sdsu.edu.
Georg E. MATT, Email: GMatt@mail.sdsu.edu.
Angela L. STOTTS, Email: Angela.L.Stotts@uth.tmc.edu.
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