Repetitive Transcranial Magnetic Stimulation for Smokers with Schizophrenia: A Systematic Review and Meta-analysis of Six Randomized Controlled Trials

doi:10.21203/rs.3.rs-1460879/v1

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Repetitive Transcranial Magnetic Stimulation for Smokers with Schizophrenia: A Systematic Review and Meta-analysis of Six Randomized Controlled Trials

https://doi.org/10.21203/rs.3.rs-1460879/v1

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Aims

A systematic review and meta-analysis was conducted to evaluate the effects of repeated transcranial magnetic stimulation (rTMS) on smokers with schizophrenia.

Methods

Only Randomized Controlled Trials (RCTs) with rTMS on smokers with schizophrenia were included. The risk of bias of the included studies were assessed using Cochrane Risk of Bias tool. Outcome indicators include changes in smoking behavior, psychiatric symptoms, and depressive symptoms. The meta-analysis was performed using RevMan 5.3 software. The Grading of Recommendations, Assessment, Development and Evaluation (GRADE) system was used to evaluate the quality of the evidence.

Findings

Six RCTs involving 571 smokers were included. The methodological quality results showed that two RCTs were assessed as high risk of bias, three were low, and seven were unclear. The meta-analysis showed that, comparing with sham rTMS, active rTMS significantly decreased the average daily number of cigarettes smoked (6 trials, MD = -8.50, 95% CI [-11.93, -5.06], very low quality) and the FTND score (4 trials, MD= -2.71, 95% CI [-3.22, -2.21], high quality). Meanwhile, rTMS improved the general psychiatric symptoms score (4 trials, MD= -1.89, 95%CI [-3.32, -0.47], moderate quality), and did not relieve the depressive symptoms score (2 trials, MD=-2.90, 95% CI [-8.72, 2.93], P = 0.33, very low quality).

Conclusions

rTMS might provide effective support for smokers with schizophrenia. It could reduce the craving for tobacco and might improve psychological symptoms. However, this conclusion needs more research and high evidence to support.

Repeated Transcranial magnetic stimulation

smokers

schizophrenia

systematic review

meta-analysis

Schizophrenia is a serious chronic mental illness, and its patient symptoms include hallucinations, negative symptoms, cognitive dysfunction, emotional and social withdrawal(1–3). For such patients, in addition to the barriers in the cognitive field, the impairment of body function caused by this disease may bring lifelong disability(2, 4). Moreover, some addictive behaviors of patients with schizophrenia can increase the burden on the body and bring about more serious adverse outcomes, among them, smoking is a common behavior(5). According to reports, the smoking rate among American adults in 2016 was 15.5%, and this proportion reached 60% among patients diagnosed with schizophrenia(6). In china, it is reported that about 59.1% of Chinese male patients with schizophrenia are associated with smoking behavior(7). At the same time, studies point out that schizophrenia is related to a 20% reduction in life expectancy(8). There is no doubt that tobacco dependence will increase the burden on patients. Compared with non-smokers, tobacco use significantly increases the mortality rate of patients with schizophrenia(9, 10). Therefore, more and more psychiatrists begin to pay attention to the problem of co-disease of schizophrenia and tobacco dependence, but such patients often lack subjective will to quit smoking, and the smoking quitting rate is 50% ~ 90% lower than the general people(11).

Current treatments for schizophrenia include antipsychotic medications and psychosocial interventions(2), but in the same trial, these interventions may only focus on psychiatric symptoms and rarely report their effects on smoking behavior. Repeated transcranial magnetic stimulation (rTMS), as a brain stimulation technique, is used to treat a wide range of neurological disorders(12, 13). rTMS is a non-invasive means of stimulating cortical neurones, it does not require surgery or anesthesia, with long-term development, this technology has more mature implementation specifications and safety guidelines(14). In the implementation of rTMS device, it delivers magnetic pulses into the brain cortex, factors such as coil shape, stimulation location, frequency and intensity, number of trains, duration, sessions, etc. are more common variables, they play a role to modulate cortical activity(15). In addition to some evidences indicated that high frequency rTMS could improve negative symptoms in schizophrenia patients(16), there is also evidence that rTMS over the dorsolateral prefrontal cortex (DLPFC) can affect processes involved in nicotine addiction(16, 17). Therefore, there are some clinical trials exploring the treatment effect of rTMS on smokers diagnosed with schizophrenia, but there is very little evidence to verify the effect of rTMS on both psychiatric symptoms and smoking outcomes of such patients.

Evidence-based research has strongly promoted the development and progress of various disciplines, especially in clinical practice(18, 19).

This study aims to target smokers with schizophrenia, using systematic reviews and meta-analysis methods to comprehensively analyze the treatment effects of rTMS technology on the psychiatric symptoms and smoking behavior of such patients, in order to provide guidance and basis for clinical practice.

This systematic review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines(20).

Data Sources and Search Strategy

We searched Cochrane Library, PubMed, EMbase, Web of Science, Chinese Biomedical Databases until July 2021. The supplementary search was completed by searching the WHO International Clinical Trials Registry Platform (ICTRP), Clinical Trials, as well as references of the relevant articles. The search strategy for all databases was as follows: (Smok* OR Tobacco OR Raucher OR ‘Yaman Ibrahim’ OR cigarette OR nicotine OR ‘pimp stick’ OR ‘Indian weed’ OR ‘nicotiana tabacum’) AND (schizophrenia OR Skhizein OR schizophrenic) AND (“transcranial magnetic stimulation” OR brain stimulat* OR rTMS) AND (random* OR blind).

Inclusion and Exclusion Criteria

Only RCTs with the following criteria were included: 1) Population: Smokers with schizophrenia, regardless of the age, the sex and occupation. 2) Intervention: The treatment group received real rTMS, with no limitation on frequency, stimulation location and duration. The control group received sham stimulation. 3) Outcomes: Each study reported an outcome related to smoking and psychological symptoms. Smoking outcomes included changes in the number of daily cigarettes and Fagerstrom Test of Nicotine Dependence (FTND) score(21). Psychological symptoms included psychiatric and depressive symptoms, these symptoms were measured by different scales, such as Positive and Negative Syndrome Scale (PANSS)(22) and Montgomery Asberg Depression Rating Scale (MADRS)(23).

Studies that were duplicate reports or with insufficient data, such as protocols, conference proceedings or abstracts were excluded.

Study Selection and Data Extraction

Literature screening and data extraction were conducted by two reviewers independently. Any disagreements were resolved by discussion. According to the eligibility criteria, the screening proceeded by reading titles, abstracts and full-texts.

Data extraction was achieved using a pre-designed data extraction table, two independent reviewers extracted the following information: 1) General information of the included studies, such as first authors, publication year, implementing country. 2) Participants characteristic, including sample size, age, sex, number of smoking. 3) Interventions, including stimulation frequency, pulses, interval, duration of rTMS. 4) Outcome indicators reported by different RCTs, including outcomes related to smoking and psychological symptoms.

Quality Assessment

Two reviewers used the Cochrane Risk of Bias tool(24) to assess the risk of bias of the included trials in seven domains, including random sequence generation, allocation concealment, blinding of participants and personnel, blinding of outcome assessment, incomplete outcome data, selective reporting and other sources of bias. Each domain was judged as “yes”, “no” or “unclear” according to the information provided in the studies. If all the domains were “yes”, the study was judged to be at low risk of bias, and if one or more domains was “no”, the study was judged to be at high risk of bias. Otherwise, the study was judged to be at unclear risk of bias(25–27).

Data Synthesis and Analysis

RevMan 5.3 was used for meta-analysis of the outcomes. If the variable was dichotomous outcome, it was analyzed with odds ratio (OR) value, and the mean difference (MD) was used to pool the continuous outcomes. The 95% confidence interval (CI) with the P-value was used to determine the effect size. Chi-squared test and I-squared (I²) tests were used to assess the statistical heterogeneity, P < 0.05 and I² > 50% was considered to indicate high heterogeneity in the results and a random-effect model was selected; otherwise, a fixed-effect model was selected. We also performed subgroup and sensitivity analyses to explore the potential sources of heterogeneity and evaluate the stability of the results. Funnel plots were constructed to investigate publication bias when the number of the included studies was more than nine.

Assessment of the quality of evidence

We used the GRADE system (28) to assess the certainty (quality) of evidence associated with specific outcomes and constructed a summary of findings table. Five downgrading factors were considered to conduct evidence level, including study limitations (design of the included studies), consistency of effect (heterogeneity of the combined effect size), imprecision (the width of the confidence interval of the combined effect size), indirectness (an indirect or direct comparison) and publication bias. For different outcome indicators with meta-analysis, considering the above five downgrading factors, based on their severity, the quality of evidence can be downgraded by one level (serious), two levels (very serious), or not (not serious). Finally, the certainty (quality) of evidence for every outcome was classified as high, moderate, low, or very low (29).

Study Selection

A flow chart of the records screening process for identified of the studies included in this review is shown in Fig. 1. A total of 284 related articles were retrieved, of which 257 were excluded because the titles or abstracts were irrelevant to the topic. For the remaining 27 records, we requested and read the full-texts. 21 did not meet the inclusion criteria. Finally, Six trials(28–33) were included in this review.

Study Characteristics

The general characteristics of the included trials were shown in Table 1. Six trials published from 2014 to 2020 involving 345 schizophrenic smoker were included, with 175 participants in the experimental group and 170 participants in the control group. The baseline number of cigarettes smoked per day in the experimental and control groups ranged from 18 to 31, and the duration of the intervention ranged from three to eight weeks. The main outcomes were the number of cigarettes smoked per day, FTND score, PANSS score and MADRS score

Table 1

General characteristics of the included studies
Study ID	Country	Sample(T/C)	Average age (T/C)	Gender (male/female)	Number of cigarettes /day (T/C)	Treatments	Control	Stimulation site	Duration	Outcomes
DU Q-L2017	China	30/30	30.41 ± 6.57 34.59 ± 10.66	60/0	18.56 ± 6.68 19.04 ± 8.64	10 Hz, 15 sessions, 20 minutes/day, 30 s intertrain interval, 20 stimulation/10 s, 2000 pulses	Sham rTMS	Left DLPFC	1, 2, 3 weeks; 6 week follow-up	①②③
Fan Y-Y2015	China	28/27	35 ± 11 31 ± 8	55/0	31.2 ± 8.2 30.5 ± 8.3	10 H Z, 20 sessions, 10 pulses/s, 5 s duration, 10 s interval, 15 m in treatment/day. 3 000 pulses	Sham rTMS	Left DLPFC	1, 2, 4 weeks; 8 week follow-up	①②
Huang W-L2019	China	19/18	40.58 ± 3.01 39.39 ± 3.03	37/0	22.37 ± 3.93 22.50 ± 5.00	10 Hz, 20 sessions, 20 pulses/s, 10s stimulation time, 30s intertrain interval, 42000 pulses	Sham rTMS	Left DLPFC	3 weeks	①②③
Cao WT-2020	China	38/36	23.00(21.00,32.25) 28.50(25.25,32.75)	74/0	30.68 ± 7.95 29.50 ± 6.58	10 Hz, 20 sessions, 10 s duration, 10 stimuli/s, 30 s inter-train interval, 2000 stimulus pulses	Sham rTMS	Left DLPFC	1, 2, 4 weeks; 8 week follow-up	①②
Radovan-P2014	Czech Republic	18/17	30.4 ± 6.56 34.58 ± 10.66	35/0	18.56 ± 6.68 19.06 ± 8.64	10 Hz, 21 sessions, 10 s duration, 30 s inter-train interval, 21 sessions, 42,000 pulses/course	Sham rTMS	Left DLPFC	3 weeks	①
Wang J2018	China	42/42	/	84/0	31.2 ± 7.8 30.8 ± 8.4	10 Hz, 20 sessions, 10 pulses/s, 5 s stimulation, interval for 10 s, 15 min/time, 3 000 pulses	Sham rTMS	Left DLPFC	1, 2, 3, 4 weeks; 8 week follow-up	①②
rTMS: Repeated Transcranial Magnetic Stimulation; DLPFC: Dorsolateral Prefrontal Cortex;
①Daily Number of Cigarettes Smoked; ②PANSS score; ③MARDS score

Risk of Bias

For 6 included studies, one study were evaluated as high risk of bias because of non-random sequence generation and incomplete outcome date. Three studies were evaluated as low risk of bias. The remaining two studies were evaluated as unclear bias risks because of unclear report for random number generation, allocation concealment, blindness, and other sources of bias information. (Fig. 2)

Meta-analysis

Daily Number of Cigarettes Smoked

Six studies involving 345 participants reported the daily number of cigarettes smoked. The meta-analysis of random effects showed that, compared with the sham stimulation, active rTMS significantly decreased the daily number of cigarettes smoked (MD= -8.50, 95% CI [-11.93, -5.06], P<0.05). (Fig. 3)

FTND Score

Four studies involving 273 participants reported the FTND score. The meta-analysis of fixed effects showed that, compared with the sham stimulation, active rTMS significantly decreased the FTND score (MD= -2.71, 95% CI [-3.22, -2.21], P<0.05). (Fig. 4).

PANSS score

The meta-analysis of the four types of PANSS scores was included. The results showed that compared with the control group, no significant difference was found in the positive symptom score (P = 0.44) and the negative symptom score (P = 0.05). A significant difference between the two groups was found in the general symptom score (4 trials, MD= -1.89, 95%CI [-3.32, -0.47]). This difference was also shown in the PANSS total score, but it was not very obvious (P = 0.08). (Fig. 5)

MADRS score

Two studies involving 97 participants reported the MADRS score. The meta-analysis of random effects showed that, compared with the sham stimulation, active rTMS did not relieve the patient's depressive symptoms (MD= -2.90, 95% CI [-8.72, 2.93], P = 0.33). (Fig. 6).

The certainty of evidence

As shown in Table 2, a summary of evidence findings was conducted, a total of seven outcomes were analyzed. The FTND score, positive symptom score, and the negative symptom score were rated as high certainty. PANSS general syndrome score was rated as moderate certainty due to imprecision (a wide CI), and PANSS total score was rated as very low certainty due to inconsistency (a high statistical heterogeneity) and imprecision. The daily number of cigarettes smoked (one high risk of bias and inconsistency) and MADRS score (inconsistency and imprecision) were both rated as very low certainty.

Table 2

Summary of evidence findings
Outcomes	Anticipated absolute effects^* (95% CI)		Relative effect (95% CI)	№ of participants (studies)	Certainty of the evidence (GRADE)
Outcomes	Risk with Sham rTMS	Risk with Active rTMS	Relative effect (95% CI)	№ of participants (studies)	Certainty of the evidence (GRADE)
Cigarettes per day	The mean number was 0	MD 8.62 lower (11.93 lower to 5.06 lower)	-	345 (6 RCTs)	⨁◯◯◯ VERY LOW ^a,b
FTND score	The mean FTND score was 0	MD 2.71 lower (3.22 lower to 2.21 lower)	-	273 (4 RCTs)	⨁⨁⨁⨁ HIGH
psychiatric syndrome - PANSS positive syndrome score	The mean positive syndrome score was 0	MD 0.28 lower (1.01 lower to 0.44 higher)	-	255 (4 RCTs)	⨁⨁⨁⨁ HIGH
psychiatric syndrome - PANSS negative syndrome score	The mean negative syndrome score was 0	MD 1.02 lower (2.07 lower to 0.02 higher)	-	255 (4 RCTs)	⨁⨁◯◯ LOW ^b
psychiatric syndrome - PANSS general syndrome score	The mean general syndrome score was 0	MD 1.89 lower (3.32 lower to 0.47 lower)	-	255 (4 RCTs)	⨁⨁⨁◯ MODERATE ^c
psychiatric syndrome - PANSS total score	The mean total score was 0	MD 1.7 lower (3.6 lower to 0.21 higher)	-	171 (3 RCTs)	⨁◯◯◯ VERY LOW ^b,c
MADRS score	The mean MADRS score was 0	MD 3.92 lower (8.72 lower to 2.93 higher)	-	97 (2 RCTs)	⨁◯◯◯ VERY LOW ^b,c
*The risk in the intervention group (and its 95% confidence interval) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: Confidence interval; MD: Mean difference
GRADE Working Group grades of evidence High certainty: We are very confident that the true effect lies close to that of the estimate of the effect Moderate certainty: We are moderately confident in the effect estimate: The true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different Low certainty: Our confidence in the effect estimate is limited: The true effect may be substantially different from the estimate of the effect Very low certainty: We have very little confidence in the effect estimate: The true effect is likely to be substantially different from the estimate of effect
Explanations
a. Downgrade by one level due to the existence of high-risk bias studies
b. Downgrade by two levels due to high statistical heterogeneity
c. Downgrade by one level due to a wide confidence interval (CI)

Summary of Results

From the results of meta-analysis, rTMS had a relative effect on smoking behavior. For changes in the number of cigarettes, active rTMS reduced the number of cigarettes per day better than sham stimulation, which had a certain enlightenment. At the same time, the differences in FTND scores also indicated the advantages of active intervention. However, for the evaluation of smoking behavior, in addition to the above indicators, the abstinence rate could better reflect the effect of the intervention. Due to the limitations of the number of included studies (only six trials) and report characteristics (almost no mention of abstinence rate), we could not evaluate the effect of rTMS on abstinence rate well. In general, these existing indicators have a certain reference value, which will help future research to make deeper explorations. For psychiatric symptoms, different PANSS scores had obvious differences. For example, for a single positive symptom and negative symptom, there is no obvious difference between the active stimulation and the control group. For the general symptom score and total score of PANSS, active rTMS had certain superiority. We assess that a small number of studies may have contributed to this instability and obvious differences, so it is necessary to expect more studies. For the MADRS score, it reflected the treatment effect of rTMS on depression for schizophrenia smokers, the meta-analysis did not showe the advantage of active stimulation. However, since only two studies had reported this indicator, we still look forward to including more studies to investigate this phenomenon.

Regarding the quality (risk of bias) of the included studies and the certainty of the evidence, the final results also showed some obvious characteristics. Risk of bias is often used to evaluate the methodological design of trials, especially for randomized controlled trials, random number sequence generation, conceal allocation, and blinding have shown importance in this type of research(34, 35). For the included studies, most of them did not have more detailed reports on some designs, so we cannot make judgments, and the unclear reports will obviously affect the overall evidence level. For the certainty of the evidence, different levels were rated according to some factors. We can see that some outcomes were downgraded due to very serious inconsistency, because of the high statistical heterogeneity in the synthetic analysis. For the degradation caused by imprecision, it may be that few studies and small sample size led to a wide confidence interval.

Future research

Based on the results of this review, we have some suggestions for future research. First, for rTMS technology, there are some important variables worth noting, such as frequency, stimulation site, session, and duration. Due to the limited number of studies included in this review, we did not perform correlation analysis on the different parameters of these variables (such as high frequency and low frequency). However, clarifying the differences between the parameters of each variable is the basis for providing the best intervention and the highest evidence. Therefore, in future trials, some multi-arm design trials can be conducted, to explore the impact of different frequencies (such as 1, 10, and 20 HZ), stimulation sites (such as left and right DLPFC), session, and duration (symptom reported at different stages, follow-up, etc.) on the target population.

Second, from the perspective of the methodological quality of the included studies and evidence level, on the one hand, it is recommended that future RCTs should follow scientific guidance and have clear reports on the design process. On the other hand, judging from the included studies, the sample size is relatively small, resulting in an inaccurate effect size that reduces the level of evidence. Therefore, in future studies, it is necessary to include more patients to expand the sample size. At the same time, there should be more clear reports on the health characteristics of patients. For example, for smokers, in addition to schizophrenia, they may also be accompanied by symptoms such as depression, anxiety, and insomnia. If the implementer has a clear diagnosis of these symptoms and pays attention to the changes in these symptoms during the intervention process, it can support the production of more high-quality evidence.

Limitations

Some limitations of this review need to be clarified. First, the few studies included in this review will weaken the level of evidence, and we cannot ignore the possibility of missing studies that meet the criteria. Since Chinese studies occupies a large proportion, possible language bias should also be considered. Second, the existence of high statistical heterogeneity seriously affects the quality of evidence for some outcomes. Although we performed a sensitivity analysis by removing each study, and the results are stable. Even if we fully consider these factors when judging the level of evidence, we still cannot rule out other sources of heterogeneity. Third, for smoking behavior, although the number of cigarettes per day and FTND score have dropped significantly, their support for rTMS on smoking cessation evidence is weak.

The results of this review show that rTMS can affect smokers diagnosed with schizophrenia, it can reduce the number of cigarettes and tobacco cravings in patients. It is possible to improve psychiatric symptoms, but the effect of suppressing depression was not found.. However, the few included studies suggest that we need more studies in the future to verify existing conclusions.

Acknowledgments

None.

Funding

This research is supported by the National Natural Science Foundation of China (Project No. 72074103); the Fundamental Research Funds for the Central Universities：lzujbky-2021-ct06、lzujbky-2021-kb22.

Disclosure Statement

The authors declare that there is no conflict of interests.

Data availability

The data used/analysed in this study is publicly available.

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No competing interests reported.

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Repetitive Transcranial Magnetic Stimulation for Smokers with Schizophrenia: A Systematic Review and Meta-analysis of Six Randomized Controlled Trials

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Abstract

Aims

Methods

Findings

Conclusions

Figures

Introduction

Methods

Data Sources and Search Strategy

Inclusion and Exclusion Criteria

Study Selection and Data Extraction

Quality Assessment

Data Synthesis and Analysis

Assessment of the quality of evidence

Results

Study Selection

Study Characteristics

Risk of Bias

Meta-analysis

Daily Number of Cigarettes Smoked

FTND Score

PANSS score

MADRS score

The certainty of evidence

Discussion

Summary of Results

Future research

Limitations

Conclusion

Declarations

References

Additional Declarations

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