EFFECTS OF SMOKINGONPREGNANCY

Maternal smoking during pregnancy is associated with decreased
infant birth weight and increased incidence of prematurity, as defined
by weight alone, and may be associated with an increased incidence of
spontaneous abortion, stillbirth, and neonatal death. Changes in the
metabolism of the placenta and in various hematological factors in
the newborn infant have -been found to be associated with maternal
smoking, ibut the mechanism of the effect of smoking on the outcome
of pregnancy remains to be determined.
New studies on the effect of maternal smoking on the outcome of
pregnancy have been published since the review of this topic in the
1967 Report (12). In the 1967 review, the literature cited supported a
relationship between maternal smotig and low birthweight and pre-
maturity in infants. However, the evidence relating the maternal
smoking to fetal or neonatal death was not definitive. The addition
of new studies has reconfirmed the relationship between maternal
smoking and low birth weight and prematurity. The relationship
between maternal smoking and spontaneous abortion, stillbirth, and
neonatal death has been investigated in several studlies. As detailed
below, some of the studies reported a statistically significant increase
in unsuccessful pregnancies in mothers who smoked when compared
with mothers who did not &oke.

EPIDEMIOLOGICAL STUIUES

In a prospective study of more than 2,000 pregnant women, Russell,
et al. (8) examined the effect of the mother's smoking habits and
blood pressure on the outcome of the pregnancy ,and on the birth
weight of the infant. A smoker was defined as one who regularly
smoked five or more cigarettes a day. In each blood pressure category,
the percentage of unsuccessful pregnancies (abortion, stillbirth, neo-
natal death) was higher for smokers. Although fewer smokers were
found in the higher blood pressure cat.egories, women who smoked
and had blood pressure levels equal to, or greater than, 150/100 had
a rate of unsuccessful pregnancy of 31.4 percent as compared to a
rate of 14.5 percent among nonsmokers with the same blood pressure

77


levels. Although the number of women in the two groups was small
(35 and 138, respectively), the difference observed was statistically
significant. For those with blood pressure levels of less than 140/90,
the percentage of unsuccessful birth was 6.5 among smokers and 2.7
among nonsmokers ; for those with blood pressure levels in the range
of 140/90, the percentage was 6.8 among smokers and 4.1 among
nonsmokers.

Extrapolating from his series, Russell (7) estimated that one out of
every five unsuccessful pregnancies in women who smoked regularly
would have been successful if the mother had not smoked regularly
during the pregnancy. This statement implies a cause-and-effect rela-
tionship between maternal cigarette smoking during pregnancy and
abortion and perinatal death. In the absence of proof of a cause-and-
effect relationship, the least that can be said is that on the basis of the
findings of Russell, et al., one out of every five unsuccessful pregnancies
among women who smoke regularly during pregnancy would not have
been unsuccessful if these women had the same risk of unsuccessful out-
come of pregnancy as women who do not smoke.

In keeping with previous findings, Russell, et al., found that the mean
birth weight of the infant was lower for the smoking mothers in each
blood pressure category. Various factors were examined as confound-
ing variables for their possible effect on birth weight and the produc-
tion of spurious associations. These included: social class of consort,
maternal age, parity, maternal height, social class of woman's father,
educational level, age of consort, maternal attitude toward the preg-
nancy, work during pregnancy, and sex of off spring. For each variable,
the smoking effect was clearly distinguished as a separate effect even
when the individual factor was itself associated with smoking (con-
sort's social class, father's social class, and maternal educational level).

A study of increases in the infants' weight. and in their head circum-
ference during the early weeks of life revealed that the babies of smok-
ing mothers grew faster than those of nonsmokers through the sixth
month after birth. However, the mean weight per week of conception
age (duration of pregnancy, plus age after birth) was greater in babies
of nonsmokers through the sixth week after birth, the effect not being
visible at the sixth month examination. These last two findings support
the theory that smoking during pregnancy acts as a retarding influence
on fetal growth and that a catching-up phenomenon begins among the
babies of smoking mothers at birth when the toxic influence is removed.

In a controlled study of 197 premature births among Negroes, Terris,
et al. (9) found a significantly higher prevalence of smoking among
the mothers of premature infants. Prematurity was defined as a birth
weight of 2,500 grams or less.

78


Mulcahy, et al. (6) studied the relationship between smoking habits
and the outcome of pregnancy in 3,631 women admitted to the Coombe
Lying-in Hospital in Dublin, Ireland. Besides finding significantly
lower birth weight for infants born to mothers who smoked, they dis-
covered a significant increase in the incidence of neonatal death, still-
birth, and spontaneous abortion. These effects were independent of age
or parity. No significant difference in the rate of congenital abnor-
malities was found between the offspring of the smokers and those of
the nonsmokers.
Kizer (4) studied the effect of maternal smoking on the outcome of
pregnancy in 2,095 patients in Venezuela. He found a significant dim-
inution in the birth weight of infants of smoking mothers and a
higher incidence of premature rupture of the membranes, but did not
find a difference in lthe incidence of abortion or perinatsl mortality.
Duffus, et al. (I) studied the relationship between smoking during
pregnancy and the incidence of albuminuric preeclamptic toxemia in
2,543 married, urban primigravidae attending antenatal clinics in
Aberdeen in 1960. Albuminuric preeclampsia is defined as albuminuria
in pregnancy in which the urine contains at least 0.25 grams of al-
bumin per liter accomhanied by a rise in diastolic blood pressure to 90
mm Hg. or more, on 2 or more days after the 26th week of gestation
or ,progressively during labor. The incidence of albuminuric pre-
eclampsia was lower bin smokers than in nonsmokers. Among the
preeclamptics, however, smokers lost more babies in the perinatal
period than the nonsmokers. The babies of smokers, both normal and
preeclamptic, had a lower mean weight than the babies of nonsmokers.
In the preeclamptic group, a greater percentage of the babies of
smokers weighed less than 5 pounds. These differences are in keeping
with those found in zother studies but do not reach statistical sign&
cance. The implication is that smoking mothers are less likely to be
preeclamptic, possibly by way of blood pressure effects, but are more
likely to have their pregnancies result in perinatal death in the event
t.hey are preeclamptic.
In a study of 5,343 deliveries in Hungary, Fiiliip (8) found a sta-
tistically significant increase in premature births among women who
smoked during their pregnancies, whether the women were married
or unmarried, held a job, or were unemployed. Lacuska, et al. (6)
found a higher frequency of premature births and abortions among
women who smoked during pregnancy than among nonsmokers,
although the differences fell short of statistical significance.
Tokuhata (10) analyzed the fertility history in relation to smoking
in groups of married women who died of breast cancer, genital ca.n-
cer, and various noncancerous diseases. Statistically significant in-
creases in Iboth the rate of infertility (as judged ,by absent of preg-

                                       79


nancy) and in fetal loss (defined as abortions and stillbirths) were
found in smokers who died of noncancerous diseases. These differences
withstood analysis for a number of possible confounding factors.
However, since the sample was made up of women who died in a
certain geographical area in a given amount of time, biases may have
been introduced. Retrospective findings in a group of dead people
are not necessarily the same as findings derived in a prospective study
of a living population.

Although by this time the evidence for reduction in birth weight
of babies born to smoking mothers is overwhelming, a problem that
remains to she solved is why some studies do and others do not appear
to show fetal wastage as measured ,by abortion, stillbirth, and neonatal
death. It may be that the method of selection of the population under
study, especially the degree to which entire obstetrical histories are
included, accounts for this variation.

EXPERIMENTAL STUDIES

Younosxai, et al. (13) compared various hematological factors in
the blood of 16 smoking mothers and newborn infants with those of
16 nonsmoking mothers and their offspring. Both groups of infants
were dehvered at term and appeared clinically well. The smoking
mothers had a mean carboxyhemoglobin saturation of venous blood
of 8.3 percent as compared to 1.2 percent in the nonsmoking mothers.
Corresponding figures for the umbilical vein cord blood were 7.3 per-
cent and 0.7 percent. A mild metabolic acidosis was seen in the infants
of smokers. These infants also had a higher mean capillary hematocrit
than those of the nonsmoking mothers. The authors point out that the
differences, although real, probably are not of clinical significance in
the newborn. However, the effect of chronic exposure of the embryo and
fetus to carboxyhemoglobin levels and other hematological abnor-
malities has not been elucidated.

Welch, et al. (16) reported that the placentas from women who
smoked during pregnancy show a much greater ability to hydroxylate
benxo( a)pyrene than the placentas from women who did not smoke
during pregnancy. The placentas from women reporting similar
cigarette consumption varied greatly in the degree of BP hydroxylase
activity. However, no information is available on the brand of ciga-
rettes smoked or the degree of inhalation, differences which may result
in different dosages of BP. It bs possible, but not likely, that car-
cinogens in tobacco smoke reach the fetus in significant amounts. The
ultimate effect of the exposure of the human fetus to carcinogenic
substances is unknown.

Becker, et al. (I) studied the effect of subcutaneous injections of
increasing doses of nicotine on groups of pregnant rats and their off-

80


spring. They found that the rati receiving nicotine injections con-
sumed less food and gained less weight than control animals and that
the magnitude of this effect increased when the dcse of nicotine was
greater. Whexxas no other differences were found in the rats receiving
lower dosages, those receiving 3.0 mg./kg. or 5.0 mg./kg. daily had
offspring which differed from thoee of the controls in being lighter,
having a longer gestation, a higher mortality rate during the first 48
hours of life, and a fetal appearance.

CITED REFERENCES

(I) BECXEX, R. F., LITTLE, C. R D., &~a, J. E. Experimental studies on nico-
   tine absorption in rats during pregnancy. III. Effect of subcutaneous
   injection of small chronic doses upon mother, fetus, and neonate. Amer-
   ican Jourmul of Obstetrics and Gynecology lCQ(7) : Q57-988, April 1,lQtM.
(8) DUFFUS, G. M., MACGIUIVBAY, I. The incidence of preeclamptic toxaemia iu
   smokers and non-smokers. Lancet l(755Q) : 994-995, May ll,lQ68.
(3) ~WL~P, T. fiber Frtihgeburten alleinstehender berufstiltiger Frauen. Sante
  Puhlique 8(4) : 381-3Q4,1967.

(4) m S. Influencia de1 habit0 de tumar sobre el embararo, parto y recien
   nacido. Revista de Obstetricia y Ginecologia de Venemeia Z(4) : 696
   643,1987.

(5) LACUSKA, A., BORURICKY, F., m, S. Fajcenie a gestacia. (Smoking and
   pregnancy.) Ceskoslovenska Gynekulogie 33(3) : lQ7-!ZOQ, 1988.
(6) MIJLCAHY, R., KNAGQE, J .F. Effect of age, parity, and cigarette smoking on
   outcome of pregnancy. American Journal of Obstetrics and Gynecology
   lOl(6) : 344-349, July 15,lQtXL

(7) RUSEELL, C. 5. Another hazard of smoking. New Scientist 41(631) : 6486,
   January Q,lQ6Q.

(8) RUSSELL, C. S., TAYIOE, R, LAW, C. E. Smoking in pregnancy, maternal
   blood pressure, pregnancy outcome, baby weight and growth, and other
   related factors. A prospective study. British Journal of Preventive and
    Social Medicine 22(3) : 119lZ8, July lQ63.
(9) Tuum, M., GOLD, E. M. An epidemiologic study of prematurity. I. Relation
   to smoking, heart volume, employment, and physique. American Journal
   of Obstetrics and Gynecology lQ3(3) : 358370. February 1, 1969.
(IO) TOKUHATA, G. K. Smoking in relation to infertility and fetal loss. Archives
   of Environmental Health l?(3) : 355-339, September 1968
(11) U.S. PUBLIC! mm SEBVICE. The Health Consequences of Smoking. A
   Public Health Service Review: 1987. Washington, U.S. Department of
   Health, EMucation, and Weifare, Public Health Service Publication No.
   16Q6,1Qe7.1QQ pp.

(12) WELCH, R. M., HAIUUSO~, Y. E., Goaam, B. W., POPPEBS, P. J., FIICWEB, M.,
   CONVEY, A. H. Stimulatory effect of cigarette smoking on the hydroxy&
   tion of 3,4-benzpyrene and the N-dimethylation of 3-methyl-&monomethyl-
   aminoazobenzene by ensymes in human placenta. Clinical Pharmacology
   and Therapeutics 10(l) : lQQ-109, January-February 1989.

(IS) Y.OU~WSZAI, M. K., KACIC, A, HAWOBTH, J. C. Cigarette smoking during
   pregnancy : The effect upon the hematocrit and acid-base baiance of the
   newborn infant. Canadian Medical Association Journal QB(5) : 197-200,
    August. 3.1968.

81


CHAPTER 5

Smoking and Noncancerous
        Oral Disease

Contents

summery_--------------------------------------------- 86
Epidemiological and Cliqical Studies-- __ ___ _ ____ ___ ________    85

Cited References ____________________--------------------    88

83


,SMOKING AND NONCANCEROUS ORAL DISEASE

`Phe previous reports have not presented findings on noncancerous
oral disease. Several recent studies have made a review appropriate at
this time. This review of the available literature leads to the conclusion
that ulceromembrsnous gingivitis, alveolar bone loss, and stomatitis
nicotina are more commonly found among smokers than among non-
smokers. The influence of smoking on periodontal disease and gingivitis
probably operates in conjunction with poor oral hygiene. In addition,
there is evidence that smoking may he associated with edentulism and
delayed socket healing. While further experimental and clinical studies
are indicated, it would appear thatnonsmokers have an advantage over
smokers in terms of their oral health.

EPIDEMIOLOGICAL AND (hmx~ &mn.~&~

Periodontal disease is a chronic destructive process affecting the sup-
porting structures of the teeth (gingiva, periodontal fibers, and alveo-
lar bone). It is generally considered inflammatory in nature. Solomon,
et al. ($1) studied data on 3,552 nonsmokers and 3,639 smokers, all
white and between the ages of 20 and 79. He found that periodontal
disease occurred without significant statistical difference in male and
female nonsmokers of the same age, but that smokers of both sexes had
a higher prevalence of the disease. The prevalence in female smokers
paralleled that in male smokers in the younger age groups but re-
sembled that of the nonsmokers in the older age groups. The authors
believe that this difference is related to increased smoking in younger
women.

Brandtzaeg, et al. (8) examined 206 Norwegiun Army recruits be-
tween the ages of 19 and 25 and found a trend toward increased perio-
dontal disease with increased smoking. However, when an analysis of
covariance was performed, most of the changes in periodontal disease
severity were accounted for by changes in oral hygiene. This finding
suggests that tobacco consumption may influence the periodontal tis-
sues but only with accompanying changes .in oral hygiene.
A seemingly contradictory paper reporting on ,periodontal diseases
in 8,206 Ceylonese was published by Waerhaug ($6). He found to-
bacco smokers to have less periodontal disease than nonsmokers. He

05


pointed out, however, that for many individuals the alternative to
smoking tobacco is chewing betel nuts, which is associated with even
more periodontitis than cigarettes. Thus, tobacco users are relatively
better off.
The relationship of smoking to gingivitis, the initial stage of perio-
dontal disease, has also been studied. Arno, et al. (6) examined 1,346
employees of a manufacturing company in Oslo and found that to-
bacco smoking was associated with an increase in the prevalence of
gingivitis. However, its importance as compared with that of oral hy-
giene was not a dominating one. Ludwick, et al. (16) studied 2,577
naval en&tees at the Great Lakes Naval Training Center and found
no relationship between smoking and simple marginal gingivitis, but
a significant one between smoking and ulceromembranous gingivitis
(necrotizing ulcerative gingivitis, Vincent's gingivitis, trenchmouth).
This is an acute form of periodontal disease of apparent sudden onset,
characterized by ulceration of the tips of the interdental papillae, gin-
gival bleeding, pain, and foul odor. In the United States and Europe, it
occurs primarily in adolescents and young adults. Bacteria, local fac-
tors, systemic factors, and psychogenic factors have been suggested
as contributing to its etiology (10).
Pindborg's study (17) of 1,433 Danish Royal Marines between the
ages of 16 and 28 revealed that the prevalence of chronic marginal gin-
givitis was not affected by smoking, but that the prevalence of ulcero-
membranous gingivitis was much greater in smokers than nonsmokers.
A second study by Pindborg (16) of 3,505 Danish military personnel
confirmed these findings : nonsmokers had a prevalence of ulceromem-
branous gingivitis of 2.2 percent, while for those who smoked 10 g. or
less of tobacco daily, the prevalence was 7.0 percent, and for more than
10 g. a day it was 9.5 percent.
Smitt (No) found a prevalence of ulceromembranous gingivitis of
2.5 percent in Dutch Navy recruits. In those who smoke 50 g. of to-
bacco for a week or more, the prevalence was 10.5 percent.
Frandsen, et al. (9) investigated the correlation between the form
of tobacco used and occurrence of gingivitis in Danish Marines. He
found that 1,848 cigarette smokers and 273 pipe smokers had essentially
the same rates of simple marginal and ulceromembranous gingivitis.
Arno, et al. (I) and Herulf (11) have investigated alveolar bone
changes in smokers. Arno studied 728 men between the ages of 21 and
45 and found that alveolar bone loss, measured as the percentage of
maximum height adjacent to the me&l and distal surfaces of each
tooth present, was higher among those with high tobacco consumption.
The author sugge&d that tobacco consumption is a complicating fac-
tor in periodontal disease and when accompanied by poor oral hygiene


and unfavorable systemic background may help speed up the destruc-
tion of the supporting tissues of the teeth.
Herulf measured interdental honey septa in 389 men and 215 women
at the Institute of Dentistry in Stockholm. He, too, found a significant
relationship between smoking and bone loss.

The relationship between cigarette smoking and edentulism has been
studied by Summers, et al. (@) in a sample of residents of Tecumseh,
Mich. Information on 324 dentulous and 34 edentulous people revealed
that among males in both groups those with the greatest evidence of
periodontal disease smoked significantly more cigarettes than those
with medium or little evidence of the disease. Solomon, et al. ($1)
found significantly more edentulism and advanced periodontal disease
in both men and women who smoked cigarettes than in nonsmokers
of the same age.

Jackson (BY) has cited heavy smoking as a factor in delayed.healing
of tooth sockets after extraction.

Stomatitis nicotina is a form of palatal leukoplakia (4). It is charac-
terized by raised umbilicated pap&s with small central red depres-
sions located primarily -on the soft palate and the posterior region of
the hard palate. The papules represent blocked palatal mucus gltlnns
and the red depressions are their inflamed duct orifices. Saunders (18)
notes that the lesions begin as tiny red dots and may progress very
rarely to ulceration. Although it sometimes occurs $n cigar and ciga-
rette smokers, stomatitis nicotina is found most frequently in pipe
smokers (4, 6, 19). According to Chapman, et al. (4)) pipe smoking
points a stream of smoke directly onto the palate, thereby allowing
longer contact between it and the smoke than in other forms of tobacco
use. The condition disappears with the cessation of smoking (6,7: 8,
l&18,19,@) , though Kerr (13) warns that healii may be slow, some-
times requiring months before no lesions are present..
Thoma ($3) observed a patient who wore dentures for over 40
years and showed lesions of stomatitis nicotina only on the part of the
palate that was not covered by the prosthesis. He concluded that the
changes were due to local surface rather than to systemic intluences.
Lewis (14)) Saunders (18)) and Thoma, et al. (94) advise biopsy
to rule out malignancy in advanced cases. Forsey, et al. (8) feel that
no association between stomatitis nicotina and cancer has been
demonstrated.

87

260-228 -7'


CITED REFERENCES

(1) Amo, A., SCHEI, O., L~VDAL, A., WAEBHAUO, J. Alveolar bone loss as a func-
   tion of tobacco consumption. Acta Odontologica Scandinavica 17: 3-10,
   1959.

(9) Asrio, A., WABBHAUQ, J., LOVDAL, A., SCHEI, 0. Incidence of gingivitis as
   related to sex, occupation, tobacco consumption, toothbrushing, and age.
   Oral Surgery, Oral Medicine, and Oral Pathology ll(6) : 537-5Q5, June
   1958.

(3) BB~HDTZAEQ, P., JAMISON, H. C. A study of periodontal health and oral
  hygiene in Norwegian army recruits. Journal of Periodontology 35 : 302-
   301, July-August 1964.

(4) CEAPM~~, I., MALKIX?, IM. Palatal leukoplakia in a female Cigarette smoker.
   Contribution to study of tobacco-induced epitheiial hyperplasia in human
   beings. New York State Journal of Medicine 61(l2) : 20442046, June
   15, 1961.

(5) CHAPMAN, I., REDI~H, C. H. Tobacco-induced epithelial proliferation in
   human subject. Long-term effects of pipe smoking on epithelium of hard
   palate. Archives of Pathology 70(2) : 183-140, August 1980.
(6) DECHAUE, M., GBELLI!Z, M., PAYEN, J. Leucoplasie papulense chez les
   fumeurs ou sbomatlte nicotinique. Presse Medicaie 6Q(56) : 2533-2536,
   December 26.1961.

(7) El tabaco y la mucosa oral. Odontoiatria 12 (10) : 61Q-621, October 1985.
(8) Foas~~, R. IL, SULLIVAN, T. J. Stomatitis nicotina. Archives of l?ermatol-
   ogy83(6) : 948-950, JunelQ61.

(9) ~%ANDEEN, A., PINDBOBO, J. J. Tobacco and gingivitis. III. Difference in the
   action of cigarette and pipe smoking. Journal of Dental Besearch 28(5) :
   464465,1Q49.

(IO) G&&NT, D. A., STILBB, I. B.. Evawrr, F. G. Necrotiaing ulcerative gingivitie.
   Chapter 18. In: Orban's Periodontics. A Concept--Theory and Practice.
   3d edition. St. Louis, C. V. Mosby Co., 1988. &. 236298
(II) HEBULF, G. On the margixW aleolar lidge in studenta : A roentgenographic
   study. Acta Genetica et StaUstica Medica 2(3) : 256-288, lf%l.
(28) JACKSON, J. A. Heavy smoking-a factor in delayed socket healing. Na-
   tional Dental Association Quarterly : 15-13, October lQf30.
(19) EEZB, D. A. Nicotine stomatitis. Journal of the Michigan State Dental
   sodety 39: 90-91, May 1948.

(14) Lmvze, A. B. Directs of smoking on oral mucosa. Oral Surgery, Oral Medi-
   cine, and Oral Pathology 8( 10) : 102&l&X4, October 1066.
(25) LVDWICK, W., MAsam M. Relation of dental Caries experience and gin-
   givitis to cigarette smoking in malea 17 to 21 years old (at the Great Lakea
   Naval Training Center). Journal of Dental Research 31(3) : 31Q-322,
    June lQ32.

(16) PINDBOBQ, J. J. Gimvitie in military personnel with spedal referenc!e to
   nlceromembranons gfngl~itla Odontologisk Tidskrift H(6) : 403400,
    1!361.

(17) Pm~nom?, J. J. !l'obacc~ and gingivitis. I. Statistical examination of the
   significance of tobacco in the development of ulceromexnbranous gingi-
    vitis and fn the formation of calcuius. Journal of De&xl Regear& 26:
   !281-!264,1947.

88


(18) SAUSDQW, W. & NicoMke &omatiMa of the palate. Annala of Ofdow,
   Rhinology and Laryngology 57 : 618-627,1956.
(IS) SCEWABTZ, D. L. Stomatitis nicotina of the palate. &port of two caaea
   Oral Surgery, Oral Medicine, and Oral Pathology 20(S) : 205-214
   September 1955.
(20) Saarrr, P. A. E. 9. Some clinical and epidemiological aepecta of Vincent'S
   gingiviMs. Dental PracMtioner and Dental Record 15(S) : 281-288, April
    1988.
(81) SOLOMON, H. A.. PBIOBE, R. L., BBO~~, I. D. J. Cigarette smoking and peri-
   odontal dieeaae. Journal of the American Dental AeaociaMon 77 (5) : lOSl-
   1084, November 1958.
(2%) SnMWS8, C. J., OBBBMAM, A. AaeociaMon of bra1 disease wi& 12 se&ted
   variables : II. Edentnlism: Journal of Dental Research 47 (4) : 594-5@
   August 1958.
(83) THOMA, IL H. Stomatitis nicotina and its effect on the palate. American
   Journal of Orthodontics and Oral Surgery 27(l) : 38-47, January 1941.
(24) TEOMA, K. H., GOLDMAN, H. M. Oral Pathology, 5th ed., 1950. St. Louis,
    C. V. Mosby Co. Pp. 955-958.
(25) ~ABBEAUO, J. Prevalence of periodontal disease in Ceylon. Ae8ociation with
   age, sex, oral hygiene, socioeconomic factore, vitamin de5cienciee, mal-
   nutrition, betel and tobacco coneumptidn, and ethnic group. Final repok
   Acta Odontologica Scandinavica 23 (2) : !B5-231,lQtW.