Effects of Marijuana Use during Pregnancy on Newborn Cry

BaIT)' M. Les ter

Brown Uuiversity and Emma Ptmdletoll Bradley Hospital

and Women (Hid IHfatlls' H U8'IJilol

Melanje Dreher

University of Miam i

LESTEH, HAI\IIY M ., and DHI.£HEII, MELANI E. Effects of Marijuana Use during Pregnancy a ll Newham Cry. CH ILD DEVELOPMENT, 1989,60, 765-771. The e ffects of matemal marijuana use on the new­born <cry were shldied in Jamaica, where it was possible to rule out confounding factors such as the use of othe r substances and demographic variables that have clouded previous studies and whe re higher dosages may make the e ffects more visible. The acoustic characte ri stics of the cries of 20 infants of marijuana users and 20 controls we re analyzed. The cries of the infants of marijuana users were shorte r, had a higher percentage of dysphonation, a highe r and more variable fundamental freque ncy, and a lower first fonnant than controls. Thcre was also a dose response relation between the first fonnant and marijuana lise. We suggest that heavy marijuana use affects the neurophysiolog­ical integrity of the infant.

ClinicaI studies have reported detrimen­tal effects of marijuana use during pregnancy on fe tal development and neonatal behavior (Fried, 1982; Fried, Watkinson, & Dillon, 1987; Gibson, B.ghurst, & Colley. 1983; Greenland, Staisch, Brown. & Cross, 1982; Hingson e t aI ., 1982; Linn e t aI., 1983). Mari­juana use during pregnancy is associated with a variety of adverse outcomes, including pre­maturity, low birthweight, decreased mater­nal weight gain, complications of pregnancy. difficult labor, congenital abnonnaIities, in­creased stillbirth and perinatal mortality, peri ­natal problems, and poor Brazelton scale scores (Fried, 1982; Fried e t aI., 1987; Gibson et aI., 1983; Green land et aI. , 1982; Hingson e t al. , 1982). Howeve r, pe rhaps because of methodologicaI problems, the shldies are in­consistent, showing one or the other adverse outcome.

In these studies, it has been difficult to control for possible confounding factors that could contribute to adverse fetal outcome, such as the use of alcohol, tobacco and/or other recreational drugs, and socioeconomic variables. Marijuana use and sociodemo­graphic variables such as lower income and education, minority status, and poor pre natal care are interre lated, and assessment of an in­dependent e ffect has been difficult to demon-

strate (Hingson et aI. , 1982; Linn e t aI. , 1983). A related problem has to do with the identifi­cation of users and nonusers (Hingson e t aI. , 1986). Because it is an illegal substance, the reliability of self-report of marijuana and other ilJicit drug use is difficult to establish.

The present study was conducted in Ja­maica to address some of the methodological problems of previous work. In our sample, the use of marijuana was not confounded with the use of other drugs , a lcohol, or tobacco smok­ing. Socioeconomic factors were also con­trolled , with both users and nonusers drawn from the lower socioeconomic sectors of the country. The reliability of marijuana usage was increased by complementing fonnal in­terviews with direct observation and long­tenn monitoring of women in their homes and workplaces.

Also, because of the frequency and amount of usage and the higher concentration of the major psychoactive ingredient, delta-9-tetrahydracannabinol (THC), Jamaica pro­vides the opportunity to study stronger effects than might be observed in the United States. These effects should be easier to measure so that we can begin to isolate specific effects of marijuana use during pregnancy on neonatal outcome.

This work was supported in part by a grant from the March of Dimes to the second author. Send reprint requests to Barry M. Leste r, Division of Child and Adolescent Psychiatry, Bradley Hospital , 1011 Ve te rans Memorial Hospital , East Providence, RI 029 15.

(Child Development. 1989, 60,765-771. IP 1989 by the Society for Research in Child Development. Inc. AJI rights reserved. 00CI9-392018916004-OO21S01.00J

766 Child Development

Our primary inte rest was in relating ma­ternal marijuana use to the acoll stic characte r­istics of the inbnt's cry. H('search since the 1960s has identified acollstic: characteristics of the infant cry that correlate with medical abnormalities, including cri dll chat , Down syndrome, hype rbiliruhinc llli,l, encephalitis, meningitis, asph yx ia , and variOllS form s of brain damage (Kareli tz & Fisichelli, J962; Lind, Vuore nkoski , Rosenherg, P,utanen, & Wasz-Hockert. 1970; Lind, Wasz-Ho<.:kelt, & Vuorcnkoski , 1965; Ostwald, Phihbs, & Fox, 1968; Vuore nkoski et aI. , J 966; Wasz-Hockelt, Lind , Vuorenkoski , Partanen, & Val anne, 1968) and with f.:'lclors that place the infant at risk fiJI" later handicap. Th ese include pre ma­turity, low birthwe ight, undern utrition, and obstetrical complications (Leste r, 1976, 1984, 1987; Lester & Zeskind, 1979; Michelsson, Sirvio, & Wasz-Hockert, 1977; Te nold et aI., 1974; Zeskind & Lester, 1978). More re­centJ y, acoustic cry characte ri stics of tJl e cry measu re d during the neonat'l l period in te rm and pre te lm inE:mts were re lated to Bayley scale scores at 18 months and McCarthy scores at 5 years (Lester, 1987), The cry is thought to re flect the ne uroph ys iological in­tegrity of the infant and may be use ful in tJle early de tection oftJle infant at risk for adverse developmental outcome,

T he notion that tJle cry is re lated to the neurophysiological status of the infant is based on human and animal studies that led to the development of conceptual mode ls that describe the anatomical and phys iologic basis for the production and neurologic control of the cry. In p articular, the ne urological integ­rity of the infant has been relate d to the stabil­ity of laryngeal coordination and vocal tract mobility (Bosma, Truby, & Lind, 1965; Golub & Corwin, 1984; Lester, 1984, 1987), Brain­stem activity as mediate d by the cranial nerves detennines sound qualities of the cry, including tJle fundamental freque ncy (per­ceived pitch) and the fonnants or resonance frequencies. The acoustically important mus­cles of the larynx, pharynx, nec k, and chest are controlled by the vagal complex; cranial ne rves IX (glossopharyngeal), X (vagal ), XI (accessory), and XII (hypoglossal) ; and by the phrenic and thoracic nerves. Damage to any of these nerves or their nucle i will affect di­rectly the acoustic characteristics of the cry. For example, if the nucle us of the vagus, the tenth cranial ne rve , is damaged, this would alter neural input to the thyroarytenoid, in­duding the vocalis, cricothyroid, and the cri­coarytenoid musd es of the larynx. These muscles de tennine the tension of the vocal folds, which affects the fundam e ntal fre-

fluency of the cry. Similarly, neural input to the vocal tract affects the contour and cross­sectional area of the suprag lottal airway, which de te rmine the form a nt fi'equencies of the cry. In rece nt studies (Hapi sardi , Vohr, Cashore, Pellcker, & Lester, 1989; Vohr, Les­te r, Pellcker, Oh, & Cas hore, 1989), the brain auditory evoked response was re lated to acoustic cry c haracte ri stics, supporting the no­tion that the cry is med iated by brain-ste m activity.

In the drug Iite rahlre , high-pitched cries have been documented in infants of narcotic addicted motJle rs (B linick, Tavolga, & Anto­pol , 1971) and were anecdotally repOIt ed in a study of infants of marijuana use rs (Fried, 1982). \Ve hypothesized that acoustic charac­te ri stics of the cry that have been used to re­flect tJl e ne urophysiological integrity of the infant would corre late with maternal mari­juana use during pregnancy,

Method

The women and the setting,-Pregnant women were recruite d from three rural com­munities in Jamaica. The communities were selected based on the ir representativeness and the presence of rural working-class wome n, a prenatal clinic, and a marijuana- or gunja-using population. One of the commu­nities is the site of the Ethiopian Zion CoptiC Church, a Rastafarian sect that e ndorses the smoking of ganja as the primary sacrament.

The pregnant women were interviewed as part of a larger ethnographic medical an­thropological study of marijuana use in these communities. For the present study, 20 mari ­juana users and 20 nonusers were followed through the birth of their infants. Our primary interest was in the analysis of the acoustic characteri stics of the infants' cries.

Marijuana consumption was de tennined by fonnal interview and by direct observation of the women in their communities during so­cial activities, and conRnned by key infor­mants in the communities. From the inter­view, the frequency and quantity of marijuana consumption were detennine d by trimester as well as overall. Marijuana was consumed both by smoking what are referred to as "ci­gars" and by brewing marijuana tea. The ci­gars contain approximately five times the quantity of marijuana as the marijuana ciga­rette common in the United Slates. In addi­tion, the concentration of THe per gram in Jamaican marijuana is three to four times higher than that of domestic marijuana (Ed­monson, 1985), When marijuana is smoked,

50% of the THe is ahsorbed into the blood­stream, in contrast to .5%- Hl% absorption through oral ingestion (Nahas, 1979). Our esti­mates of marijuana lise included the fre­quency and quantity of both cigars and tea.

The two groups of mothers, 20 users and 20 nonusers , were from lowe r socioeconomic families as determined by income and occu­pation. The two groups were also similar in tenns of age (15-35 f(Jr smokers, 16-37 for nonsmokers), gravida (1-7 for smokers, 1-8 for nonsmokers), and parity (1-6 for smokers, 0-8 for nonsmokers) and in the use of other drugs, alcohol, or tobacco, which was re­ported as rare or occasional. This was also confinned by direct -observation.

The nonusers reported that they did not smoke marijuana cigars or drink marijuana tea during pregnancy. They felt that marijuana may be hannful to their infants, based on warnings from the "old people" about babies born "viled up" with "black mouths," " mashed up brains," and "cracked skin."

All of the women in the user group smoked marijuana cigars from the first trimes­ter, and 15 smoked during all three trimesters. The reported frequency of smoking marijuana in this !,,'TOUp ranged from 1- 10 cigars per day (M = 4.15) and 2-71 per week (M = 18.68). Marijuana tea was consumed by 16 of the mothers starting in the first trimester. Mari­juana tea consumption was reported as 1-8 cups per week (M = 5.47). The frequency of marijuana use during pregnancy in this sam­ple is substantially higher than in U.S. studies (Fried, 1982; Gibson et a!., 1983; Greenland et a!., 1982; Hingson et a!., 1982; Linn et a!., 1983).

The interviews showed that many of the users were aware of the potential halm of marijuana smoking to the fetus. However, they reported that smoking controlled first tri­mester nausea and vomiting, reduced fatigue, and helped them sleep better and relax. The influence of the Rastafarian sect has also in­creased the social status of marijuana smok­ing. Women who smoke have been given the title "roots daughter," which signifies a woman who has "good brains" and who can smoke "hard as a man."

Characteristics of the infants.-The in­fants were all born in hospital at term (ges ta­tional age ranged from 38 to 42 weeks). Birth­weights averaged 3,096 grams in the group of infants of nonsmokers (range, 2,455-3,830 grams) and 3,206 grams in the group of infants of smokers (range, 2,367-3,901 grams). There was one low-birth weight infant «2,500

Lester and Dreher 767

grams) in each group. Apgar scores were re­ported as > 7 for all infants , although the reli ­ability of these scores was questionable. All of the infants we re judged to be healthy. None were sent to the special care nursery, and no abnonnalities were noted.

en} recording and analysis.-The cry was recorded and analyzed using previously established procedures (Lester, 1987). The cry was tape-recorded at home on the fourth or fifth day after birth. The infant was placed in a supine position with the microphone held 15 em from the infant's mouth. Standard newborn reflexes were used to elicit the cry. The first 10 sec of the cry were used for acous­tic analysis. The cry was analyzed using a computer-extraction system developed in col­laboration with Physiologic DiagnostiC Ser­vice (PDS, Inc.; Cambridge, MA). The cry is filtered at 5 Hz and digitized at 10 kHz. The Fast Fourier Transfonn is used to compute the log magnitude spectrum for each 25-msec block of the cry. Summary variables are com­puted across the 25-msec blocks . The follow­ing summary variables were used for the pres­ent study:

Duration: Average amount of time (sec) of each cry phonation that occurs during the expiratmy phase of respiration.

Percent dysphonation: Proportion of the cry blocks in which the signal is inhannonic. This is a measure of the amount of turbulence or "noise" in the cry.

Fundamental frequency (fa): Frequency of vocal fold vibration; it is what we hear as voice pitch. Both the median and the range of fa were computed. FO is determined by sub­glottal pressure and by vocal fold tension from the intrinsic muscles of the larynx.

First fonnant (Fl): The formants are the resonance frequencies that occur as a result of the filtering by the vocal tract. Fl is deter­mined by the contour and cross-sectional area of the supraglottal airway. Both the median Fl and the range of Fl were computed.

Results

The means and standard deviations of the six acoustic cry variables for the smokers and nonsmokers are shown in Table 1. The cry characteristics of the smokers and nonsmok­ers were compared by multivariate analysis of variance (MAN OVA) of the six dependent cry variables. The MANOV A was statistically sig­nificant, F(6) = 11.78, p < .001, with signifi­cant univariate effects observed for five of the six cry variables. The cries of the infants of

768 C hild D e velopm e n t

TARLE I

(;IIY C II AJl ACTElll STr CS IN I NFA NTS OF MAIIIJ lI AN A

S~!oKEI\S ANI) NONS MOK EIIS

S M()KE HS N ()NS MOKEII S (N = 20) (N = 20)

C RY M EASti ll E ;-"·f can

Durat ion . ... ....... 29.85 Pe rcent dysp honation . 24.45 A verage fO . 457.50 Range ro. 429.55 Ave rage Fl .. " . . . . .. 1114.85

mothe rs who smoked marij uana we re shorte r in duration , F( 1.38) = 6.02, p < .02, a nd h ad a h ighe r pe rcentage of d ysphonatio ll , F(l,38) = 16.10, p < .003, a h igh e r m e dia n fO, F(I ,38) = 5.07, p < .03, a wide r range of 1'0, 1'(1 ,38) = 24 .02, p < '(X)O l , and a lowe r median 171 , F(I ,38) = 16.10, p < .n003, than th e c ries of the infants of nonsmoke rs. The median corre­lation among the s ix acoustic variables was r = .15 (range, r = .003 10 - .35).

To detennine possib le dose-response re ­lations, Pearson corre lation coefficie nts we re computed be tween the cry variables and the numbe r of cigars pe r week and the numbe r of cigars pe r day. Significant correlations we re found for the cry measure of med ia n Fl (F ig. 1). The freque ncy of marijuana smoking was inversely corre lated with the median F I of the cry. As shown in Figure I , a lower FI in the cry was related to more marijuana smok­ing pe r day, ". = - .58, p < .01. A lowe r FI was also re lated to more marijuana smoking pe r wee k, ". = - .52, p < .02. There was no re lation be tween marijuana tea ingesti on

SI) Mean S I)

13.67 43. 15 20.02 15.52 5.05 4.68 90 .15 405.50 50.44 79.79 195.70 40.67

326.29 1454.10 HJ 1.10

(numbe r of cups pe r day o r week) and the c ry measures.

Discussio n

Marijuana smoking during pregnancy in Jamaica appears to affect the acoustic charac­te ri sti cs of the newborn cry. In other studies, these acoustic characte ristics have bee n re­lated to pe rinatal ri sk factors and to later de­velopme ntal outcome (Leste r, 1987; Leste r & Boukydis, 1985). The lowe r average first for­mant (1,11 4 vs. 1,454 Hz) in the infa nts o f marijuana smoke rs is note worthy because it is almost a fuI1 standard de viation lowe r than what we find in normal infants in the United States using the same me thods of cry record­ing and analysis. For example, in unpub­lished dat..1. from a nonnative sample of over 1,200 infants, the ave rage Fl is 1,393 Hz (SO = 311 ). The Fl measure also sugges ted a dose-response re lation. Mothe rs who smoked more marijuana during pregnancy had infants w ith lower first fonnant cries . Fl can be low for anatomical reasons that re late to the con-

~~~,~ege~~F_'~__________ __________________________________ , 2000 I

1500

t--1000

500

2 3 4 6 6 7 B

Number Cigars/day

r • - .58, p ( .01 S€If'lea A

FIC. I.-Corre lation between ave rage first fomlant of cry and numbe r of marijuana cigars per day

I .. ~

figuration of the vocal tract or due to motor innervation of the supraglottal ainvay that re­Rects neural control. This could indicate re­spiratory involvement. Linn et a1. (1983) reported a higher rate of malformations of the respiratory tract in infants of marijuana users, although other confounding variables may have been involved. Our other findings of in­creased dysphonation or rurbulence and shorter cry durations related to marijuana use could also suggest respiratory involvement.

We also found a higher fundamental fre­quency (fO) and a wider range in fO related to maternal marijuana use. Clinically, we would hear this as a higher-pitched and more vari­able cry. In a previous study, although the cry was not recorded, Fried (1982) reported that one-third of the infants of marijuana smokers and none of the controls had high-pitched cries.

Neural mediation through the ninth, tenth, eleventh, and twelfth cranial nerves and the thoracic and phrenic nerves plays a large role in the control of the cry, including fO and the fonnants (Lester, 1987). The role of the brain stem appears to be in the mechanics of cry production. Higher centers are in­volved in the configuration and triggering of the specific vocal pattern. The distress call in monkeys is mediated by the limbic system (MacLean & Newman, 1987), which includes the hypothalamus, important in the control of emotions such as crying. Buchwald and as­sociates recently showed that in cats, e lectri­cal stimulation of the hypothalamus produces distress calls similar to the spontaneous calls of the same animal (Altafullah, Shipley, & Buchwald, 1987). In other animal studies, THC has been found to cause changes in the limbic system in monkeys (McIsaac, Fritchie, Idanpaan-Heikkila, Ho, & Englert, 1971) and in rats (Landfield, Cadwallader, & Vinsant, 1987). It is possible that some of the effects on the cry observed in the present srudy were due to direct effects of THe on brain stem or higher regions.

It is important to interpret these effects in light of the amount of marijuana ingested by these mothers. Considering the concentration of THC (three to four times stronger than in the United States) and the amount of mari­juana in a typical Jamaican "cigar" (five times as much as the United States), even at the same frequency of marijuana use as in the United States, these Jamaican women were probably exposed to 15-20 times as much marijuana as women that have been studied in the United States.

Lester and Dreher 769

Also, compared to studies conducted in the United States, we were better able to con­trol for demographic factors and the use of other substances. We were also able to obtain a more reliable estimate of marijuana use be­cause of its cultural acceptance in Jamaica, which also made it possible to include several validity checks on maternal self-report.

Acoustic characteristics of the cry have been used as a measure of the neurophysio* logical status of the infant. Our findings pro­vide evidence that maternal marijuana smok­ing during pregnancy presents a toxic threat to the biological integrity of the infant. It has been suggested that marijuana could be clas­sified among the psychotropic drugs that act as "behavioral teratogens" (Nahas, 1979). We usually think of teratogens as agents that cause physical malformations, such as thalido­mide, or more recently the fetal alcohol syn· drome (Jones, Smith, Ulleland, & Streissguth, 1973). However, some agents have been found to have functional sequelae, such as growth retardation and behavioral deficits, in the absence of physical malformations (Hutchings, 1983). Behavioral teratology re­fers to research deaHng with these functional effects, as, for example, in the case of the neo­natal withdrawal syndrome in infants of nar­cotic addicted mothers (Finnigen, 1981). The high-pitched cry has already been identified as part of this syndrome (Blinick et a!., 1971). Fried et a!. (1987) found that prenatal mari­juana exposure was associated with symptoms similar to mild narcotic withdrawal. Our find­ings extend the effects on the cry to maternal marijuana use and support the classification of marijuana as a behavioral teratogen.

Agents taken during pregnancy can affect infant functioning because of direct effects on the central nervous system or indirectly as al­tered behavior affects the developing parent­infant relationship. In previous work, the cry has been described as a biosocial phenome­non (Lester, 1984); biological effects refer to the cry as a measure of CNS integrity. Social effects refer to the effects of cry characteristics on how parents perceive the infant, which af­fects parenting behavior. In the context of the current study, it is likely that the significance of the acoustic characteristics of the cry for infant functioning and development may lie in its biosocial significance. As a measure of the neurophysiological integrity of the infant, the cry reflects the direct effects of marijuana on the CNS and may predict later develop­mental outcome. Indirect effects of marijuana are mediated by the effects of cry characteris­tics on the developing parent-infant relation-

770 Child Development

ship, which can also afled developmental outcome.

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