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Rheumatology 2001; 40: 123-127
© 2001 British Society for Rheumatology

Mortality associated with cervical spine disorders: a population-based study of 1666 patients with rheumatoid arthritis who died in Finland in 1989

M. H. Neva, R. Myllykangas-Luosujärvi1, H. Kautiainen2 and M. Kauppi3,4,

Department of Orthopaedic and Trauma Surgery, Jyväskylä Central Hospital, Jyväskylä,
1 Department of Medicine, University of Kuopio, Kuopio,
2 Rheumatism Foundation Hospital, Heinola,
3 Department of Rheumatology, Rheumatism Foundation Hospital, Heinola and
4 Department of Medicine, University of Oulu, Oulu, Finland


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 References
 
Objective. To evaluate the mortality associated with cervical spine deformities in rheumatoid arthritis (RA) based on national data.

Methods. The role of rheumatoid disorders of the cervical spine as a cause of death was studied in 1666 subjects who died in Finland in 1989 and had been entitled under the national sickness insurance scheme to receive reimbursed medication for RA. Death certificates and certificates for drug reimbursement of these 1666 patients and the clinical files of 853 patients were examined for the mention of cervical spine disorders. Thereafter, the cervical spine radiographs and detailed clinical histories of patients with diagnosed cervical spine disorder were evaluated separately.

Results. According to the official death certificates, cervical spine disorder was not an underlying, contributory or immediate cause of death in any of these patients. Cervical spine abnormalities had been diagnosed only in 38/853 (4.5%) patients. Cervical spine radiographs from 33 patients were available for examination, and in 17 patients cervical spine deformities were found to be severe enough to be a potential cause of fatal complications. Among these 17 cases, four sudden and four postoperative deaths were recorded (one after cervical spine operation) and three patients were suffering from quadriparesis or paraparesis at the time of death. Among the other 16 patients with cervical spine radiographs, the cervical deformities were less severe and their death histories differed from those of the group with more severe deformities.

Conclusions. Cervical spine disorders in RA should be diagnosed early and treated actively to prevent severe and potentially fatal complications. Deaths caused by these disorders are rare, but they should be remembered when the death certificates are written.

KEY WORDS: Rheumatoid arthritis, Cervical spine, Mortality.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 References
 
Cervical spine involvement is a well-known common feature in rheumatoid arthritis (RA). Anterior atlanto-axial subluxation (aAAS) has been reported to be the most frequent rheumatoid abnormality of the cervical spine, with a prevalence of 19–70% [1]. Atlanto-axial impaction (AAI), i.e. vertical atlanto-axial subluxation, and subaxial subluxations (SAS) have been reported to occur with a frequency of 4–35% and 7–29% respectively [1].

Weissman et al. [2] have reported that patients with aAAS of >=10 mm or with AAI combined with a lesser degree of aAAS have a high risk of spinal cord compression. Furthermore, subaxial changes can cause compression of the nerve root or spinal cord [3, 4]. Therefore, severe cervical spine deformities may lead to serious complications, such as quadriparesis, cerebral infarction, chronic hydrocephalus and even sudden death [5–11]. Mikulowski et al. [10] have reported a high incidence (10%) of fatal medulla compressions in a series of hospital inpatients with RA. Furthermore, several authors have recommended prophylactic operative treatment of severe cervical subluxations to avoid the risk of irreversible neurological deficit and even death caused by spinal cord compression [11–15]. The life expectancy of RA patients has been reported to be shorter than that of the general population [16–18]. However, cervical spine dislocations have not been shown to significantly reduce the expected lifetime in patients with RA [19, 20].

In the present study, we used a unique, unselected material of 1666 RA patients who died in Finland during 1989, collected from national Finnish registers [21]. This series was used to determine epidemiologically the mortality caused by rheumatoid cervical spine deformities.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 References
 
Patients
Since 1966, the sickness insurance act in Finland has provided for the prescription of drugs free of charge for certain chronic diseases, including inflammatory joint diseases (90% of the costs have been reimbursed since the amendment was made in 1987). The national sickness insurance scheme covers the entire population of Finland, and almost all patients with RA take advantage of it [18, 22, 23]. Eligibility requires a comprehensive medical certificate issued by the attending physician, who is usually a rheumatologist, and is approved by an expert adviser on the behalf of the sickness insurance scheme. In 1989, 56175 people were registered for chronic inflammatory rheumatic diseases [18, 23].

Details of the selection of the patients have been described earlier [18, 23]. Briefly, all 48 550 subjects who died in Finland during 1989 were identified by the use of the Finnish population registry. Basic information on the subjects was obtained from the death certificates and from the drug reimbursement certificates. Altogether, 1849 subjects (578 men and 1271 women) who died in 1989 were entitled to specially reimbursed medication for chronic inflammatory rheumatic diseases. The diagnoses were verified from the original medical certificates for drug reimbursement, and 1666 patients with RA (480 men and 1186 women) were identified. The sensitivity of the sickness insurance data has been reported to be approximately 95% in this series [18, 23].

The causes of death of these 1666 patients were classified by the statistical office of Finland according to the rules of the World Health Organization, using the ninth revision of the International Classification of Diseases. The final code for the death was not always the same as that given in the death certificate. The six main causes of death in our patients were cardiovascular diseases (48.3%), neoplasms (16.6%), musculoskeletal diseases (11.3%), respiratory diseases (8.4%), gastrointestinal diseases (4.0%) and accidents or intoxication (3.2%) [23]. Autopsy had been performed in 453 cases.

Death certificates and certificates for drug reimbursement were evaluated for all 1666 patients (Fig. 1Go). In addition, hospital records of patients who had died of cardiovascular diseases, neoplasms, RA, respiratory diseases, gastrointestinal diseases, accidents or intoxication, genitourinary diseases, infections, amyloidosis or central nervous system diseases and those of patients who had mental diseases or were treated in the Rheumatism Foundation Hospital (altogether 853 patients) were collected from hospitals throughout Finland. The clinical notes were examined for the mention of cervical spine disorders. Thereafter, all cervical spine radiographs that were available and the detailed clinical histories of the patients with diagnosed cervical spine disorder were evaluated separately.



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  		FIG. 1. Schematic presentation of the distribution of patients among the study groups.

 

Radiographic evaluation
Anterior AAS was diagnosed if the distance between the anterior aspect of the dens and the posterior aspect of the anterior arch of the atlas was more than 3 mm when measured from the lateral view radiographs taken during flexion. AAI was diagnosed using the Sakaguchi–Kauppi (S-K) method, which was developed especially for screening purposes. It divides the condition into four grades (grade I, normal; grades II–IV, abnormal) [24]. SAS was diagnosed if a cervical vertebra had moved more than 3 mm in relation to the next cervical vertebra when measured from the posterior line of the vertebral bodies. The posterior atlantodental interval (PADI) is the shortest distance between the posterior aspect of the dens and the anterior aspect of the posterior atlas arch [12]. If PADI is <=14 mm, the risk of medulla compression has been reported to be high [12].

To investigate whether the extent of changes in the cervical spine correlates with the death history, the patients were divided into three groups on the basis of the radiographic evaluation of the cervical spine. In the high-risk group, the cervical spine changes were considered to be severe enough to carry a high risk of fatal complications. The high-risk criteria were similar to those indicating a high risk of spinal cord compression: aAAS >=10 mm, aAAS 8–9 mm+AAI grade III, AAI grade IV, SAS >6 mm, or PADI <=14 [2, 10, 12, 13, 25]. In the low-risk group, the radiographic findings were less severe. Patients with a diagnosed cervical spine disorder, whose radiographs were destroyed after death and were thus not available, formed the third group. Classification of cases in the high and low-risk groups was made without any knowledge of the clinical history.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 References
 
According to the official death certificates, rheumatoid destruction of the cervical spine was not an underlying, contributory or immediate cause of death in any of the 1666 patients with RA who died in Finland in 1989.

A cervical spine disorder was diagnosed in 38 patients (nine males and 29 females; mean age 68 yr, range 39–90 yr) according to the clinical files of 853 patients. Thus, the prevalence of rheumatoid cervical spine disorders was only 4.5%. Six patients had undergone a cervical spine operation and one of them had been operated on three times.

Cervical spine radiographs were available for 33 of these 38 patients. Twenty-five patients (76%) had aAAS >3 mm and five of these cases were regarded as severe (i.e. >=10 mm) (Table 1Go). Twenty-two patients (66%) had AAI grade II–IV, of whom eight had extremely severe AAI (grade IV). SAS >3 mm was observed in 14 patients (42%), and six of these had severe SAS (>6 mm). PADI <=14 mm was found in four patients. In 17 cases (52%) the cervical spine changes (at least one abnormality, often several simultaneously) were found to be severe enough to carry a high risk of fatal complications, and these patients formed the high-risk group. Sixteen patients had less severe changes in their cervical spine radiographs, and these were classified as having a low risk of fatal complications (low-risk group). There were five patients with diagnosed rheumatoid cervical spine deformity but for whom no cervical spine radiographs were available; these patients formed the third group (no radiographs available).


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  		TABLE 1. Demographic data, cervical spine changes and history of operations in 38 RA patients with a diagnosed cervical spine abnormality

 
There were no apparent differences in the gender, age or official causes of death between these groups (Table 2Go). The clinical histories of the patients in the high-risk group contained more evidence of possible complications caused by the cervical spine changes than did the histories of patients in the low-risk group (Table 3Go). In the high-risk group, three patients had quadriparesis or paraparesis, which might have been caused by rheumatoid cervical spine deformity. In addition, four patients died suddenly, one died due to a brain stroke, one patient died soon after a cervical spine operation and a further three patients also died postoperatively.


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  		TABLE 2. Official main causes of death in 38 RA patients with a diagnosed cervical spine abnormality

 

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  		TABLE 3. Clinical history of the last weeks before death in 38 RA patients with a diagnosed cervical spine abnormality

 


   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
References
 
In patients with RA the cervical spine structures are often affected by rheumatoid inflammation [1, 26]. The stabilizing ability of the cervical ligaments of the spine may deteriorate, leading to subluxations of the cervical vertebrae [26]. Rheumatoid inflammatory pannus may also cause compression of the spinal cord and other neural tissues [12]. Because of the cervical spine instability, trivial traumas in this region may be dangerous and even cause sudden death [26, 27]. Furthermore, chronic compression of nervous and arterial structures may cause myelopathy, hydrocephalus and vascular infarctions of the central nervous system [4–7, 15]. These complications may be directly fatal or they may cause paraparesis or quadriparesis, thereby reducing the ability to move and causing other life-threatening complications [17].

There have been some previous reports of fatal cervical spine complications [8, 9, 17, 19, 28]. Mikulowski et al. performed autopsies on 104 hospital in-patients with RA [10]. They reported 10% mortality for cervical spine disorders. This percentage is high, but interestingly it is similar to the percentage of RA patients fulfilling the radiographic indications for cervical spine operations in a population-based study [25] and in a 20-yr follow-up study [29]. These results suggest that, on average, 10% of patients with long-lasting RA have a high risk of cervical spine complications.

We have studied the cervical spine mortality of all RA patients who died during a period of 1 yr in Finland, using national registers. Death certificates of these 1666 patients were evaluated. Surprisingly, not a single death was officially recorded as having been caused by cervical spine disorder. Four hundred and fifty-three autopsies had been performed, but it must be noted that the evaluation of the upper cervical spine is not routinely included in an autopsy because of technical difficulties [10].

The clinical records of 853 of these 1666 patients were carefully examined. Cervical spine deformity had been diagnosed in only 38 (4.5%) patients. This percentage is unexpectedly low compared with previous reports [1, 25, 29]. Radiological findings in 45% of these patients were severe enough to fulfil common indications for operation [12, 13, 25, 29]. It is probable that most of the less severe changes and even some of the severe disorders were not diagnosed. Furthermore, the incidence of cervical spine disorders in the group of 813 patients whose clinical files were not evaluated is not known. However, the fact that patients who died of RA or amyloidosis and who were treated in the Rheumatism Foundation Hospital were included in the group of 853 patients indicates that the patients in this group suffered from more severe RA than those in the other group, and most probably also had more cervical spine changes.

Vandenbroucke et al. [17] reported only one death from cervical spine disorder in their series of 165 deaths. However, 16 additional patients died from complications of immobilization. In our high-risk group, three patients had paraparesis or quadriparesis. Only one patient in the low-risk group had quadriparesis, and his last cervical spine radiographs had been taken 4 yr before his death. Thus, his cervical spine abnormality may have progressed after the radiography. In these four patients the paresis was probably caused by cervical spine disorder and spinal cord compression. Therefore, the cervical spine destruction is likely to have been at least a contributory cause of some of the deaths. In the high-risk group there were two additional non-ambulant patients, but it is impossible to determine whether cervical spine disorders had contributed to the immobilization of these patients.

One patient died soon after a cervical spine operation and six patients (three in the high-risk group) died soon after other operations. These operations were mostly urgent, and naturally the postoperative mortality in patients with severe disease is high. However, intubation for general anaesthesia carries a risk in patients who have severe cervical spine deformity [27, 30, 31]. The possibility of cervical spine complications during these operations cannot be excluded.

In previous reports, cervical spine disorders have not been shown to reduce the expected lifetime significantly in patients with RA [19, 20]. Our results are in agreement with these studies, but underline the notion that in individual cases rheumatoid cervical spine may cause fatal complications. Officially, cervical spine disorder was not a cause of death in any of the RA patients who died in Finland during 1989. However, a more detailed evaluation has shown that disorders of the cervical spine seem to be associated with at least some deaths. The number of diagnosed cervical spine disorders was surprisingly low, strongly suggesting that some cases, possibly even severe cases, were not diagnosed. Taken together, our present results stress the importance of early diagnosis and active treatment of cervical spine disorders in RA to prevent later severe and even fatal complications. In addition, these disorders should be remembered as possible causes of death when the death certificates are written.


   Acknowledgments
 
We thank Dr Pia Isomäki for valuable comments on the manuscript.


   Notes
 
Correspondence to: M. Kauppi, Department of Rheumatology, Rheumatism Foundation Hospital, 18120 Heinola, Finland. Back


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

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Submitted 29 September 2000; Accepted 2 September 2000


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