Review part 2: Human herpesvirus-6 in central nervous system diseases

Chronic fatigue syndrome (CFS) is a debilitating chronic illness [Fukuda et al., 1994] that often begins suddenly with a “flu-like” illness. Patients with CFS have great functional impairment [Komaroff et al., 1996]. The cost to the U.S. economy from lost productivity alone (not including medical care costs) is $9 billion annually [Reynolds et al., 2004].

While the pathogenesis of CFS is unknown, there is abundant evidence of an underlying biological process. In comparison to various health and disease control groups, patients with CFS have abnormal findings in the CNS and autonomic nervous system, evidence of chronic activation of various parts of the immune system, and disordered energy metabolism.

CNS abnormalities have been found using MRI [Buchwald et al., 1992; Schwartz et al., 1994a; Lange et al., 2001; de Lange et al., 2005], functional MRI [Tanaka et al., 2006], SPECT [Schwartz et al., 1994b; Schmaling et al., 2003], and positron-emission tomography (PET) [Yamamoto et al., 2004]. Neuroendocrine studies reveal hypofunction of corticotropin releasing hormone (CRH) neurons in the hypothalamus [Demitrack et al., 1991], disruption of both serotonergic and noradrenergic hypothalamic pathways [Demitrack et al., 1992; Cleare et al., 1995], and of growth hormone secretion [Moorkens et al., 2000]. Typically, these abnormalities are in patterns opposite to those seen in major depression. Cognitive testing has revealed abnormalities [Tiersky et al., 1997; Daly et al., 2001; Deluca et al., 2004] that are not explained by concomitant mood disorders [Marcel et al., 1996]. Autonomic nervous system testing has found abnormalities—particularly postural orthostatic tachycardia syndrome, neurally mediated hypotension, and heart rate variability during head-up tilt testing [Bou-Holaigah et al., 1995; Freeman and Komaroff, 1997; Stewart, 2000; Naschitz et al., 2002].

The immunological findings described most commonly in CFS are impaired function of natural killer cells, increased numbers of CD8+ cytotoxic T cells that bear antigenic markers of activation on their cell surface, and increased production of various pro-inflammatory and TH2 cytokines [Komaroff, 2006]. Many of these cytokines can produce symptoms characteristic of CFS: fatigue, fevers, adenopathy, myalgias, arthralgias, sleep disorders, cognitive impairment, and mood disorders.

Many recent studies of patients with CFS have identified disorders of energy metabolism [Myhill et al., 2009], increased allostatic load [Maloney et al., 2009], and increased oxidative and nitrosative stress [Maes and Leunis, 2008].

Cases of CFS can follow in the wake of well-documented infection with several infectious agents, and may be more likely when the symptoms of acute infection were most severe [Hickie et al., 2006]. The first large study on the possible role of HHV-6 in CFS included 259 patients with a “CFS-like” illness (the case definition had not yet been developed) and age- and gender-matched healthy control subjects. Primary culture of lymphocytes showed active replication of HHV-6 in 70% of the patients versus 20% of the control subjects (P < 10 −8) [Buchwald et al., 1992].

Some subsequent studies have employed only serological techniques that do not distinguish active from latent infection. The results have been mixed: a slight preponderance has showed an association between CFS and HHV-6 infection [Ablashi et al., 2000; Reeves et al., 2000; Hickie et al., 2006].

In contrast, other studies have employed assays that can detect active infection: PCR of serum or plasma, IgM early antigen antibodies, and primary cell culture. Most of these studies have shown an association between CFS and active HHV-6 infection [Patnaik et al., 1995; Secchiero et al., 1995; Wagner et al., 1996; Zorzenon et al., 1996; Ablashi et al., 2000; Nicolson et al., 2003], whereas a few have not [Koelle et al., 2002; Reeves et al., 2000]. The number of patients in the studies that have found an association between CFS and active HHV-6 infection (N = 717) is much larger than the number in studies that have failed to find an association (N = 48).

Several observations, summarized above, together suggest that active infection with HHV-6 may cause some cases of CFS. First, active infection with HHV-6 is present in a substantial fraction of patients with CFS. Second, HHV-6 is tropic for the nervous system and immune system cells, and CFS is characterized by neurological and immunological abnormalities. Clinical studies with antiviral drugs that have in vitro activity against HHV-6 could provide strong evidence in favor of, or against, the hypothesis that HHV-6 may trigger and perpetuate some cases of CFS.

You can read the full article here: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4758195/

 

Source: Yao K, Crawford JR, Komaroff AL, Ablashi DV, Jacobson S. Review part 2: Human herpesvirus-6 in central nervous system diseases.J Med Virol. 2010 Oct;82(10):1669-78. doi: 10.1002/jmv.21861. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4758195/ (Full article)

 

Antibody to parvovirus B19 nonstructural protein is associated with chronic arthralgia in patients with chronic fatigue syndrome/myalgic encephalomyelitis

Abstract:

Chronic fatigue syndrome/myalgic encephalomyelitis (CFS/ME) is a neuro-immune disease of uncertain pathogenesis. Human parvovirus B19 infection has been shown to occur just prior to development of the onset of CFS/ME in several cases, although B19 seroprevalence studies do not show any significant differences between CFS/ME and controls.

In this study, we analysed parvovirus B19 markers in CFS/ME patients (n=200), diagnosed according to Fukuda CDC criteria, and normal blood donors (n=200). Serum from each subject was tested for anti-B19 VP2 IgM and IgG (by Biotrin ELISA), anti-B19 NS1 IgM and IgG (by immunofluorescence), and B19 DNA (by real-time PCR).

CFS/ME patients and normal blood donors had a similar B19 seroprevalence (75 % versus 78 %, respectively). Eighty-three CFS patients (41.5 %) as compared with fourteen (7 %) normal blood donors tested positive for anti-B19 NS1 IgG (chi(2)=64.8; P<0.0001; odds ratio=9.42, CI 5.11-17.38). Of these 83 patients, 61 complained of chronic joint pain, while 22 did not.

Parvovirus B19 DNA was detected in serum of 11 CFS patients and none of the controls by Taqman real-time PCR (chi(2)=9.35, P<0.002). Positivity for anti-B19 NS1 IgG was associated with higher expression levels of the human CFS-associated genes NHLH1 and GABPA. As NS1 antibodies are thought to indicate chronic or severe courses of B19 infection, these findings suggest that although the seroprevalence of B19 in CFS patients is similar to controls, the immune control of the virus in these patients may not be efficient.

 

Source: Kerr JR, Gough J, Richards SC, Main J, Enlander D, McCreary M, Komaroff AL, Chia JK. Antibody to parvovirus B19 nonstructural protein is associated with chronic arthralgia in patients with chronic fatigue syndrome/myalgic encephalomyelitis. J Gen Virol. 2010 Apr;91(Pt 4):893-7. doi: 10.1099/vir.0.017590-0. Epub 2009 Dec 9. https://www.ncbi.nlm.nih.gov/pubmed/20007355

 

Is human herpesvirus-6 a trigger for chronic fatigue syndrome?

Abstract:

Chronic fatigue syndrome (CFS) is an illness currently defined entirely by a combination of non-specific symptoms. Despite this subjective definition, CFS is associated with objective underlying biological abnormalities, particularly involving the nervous system and immune system.

Most studies have found that active infection with human herpesvirus-6 (HHV-6)–a neurotropic, gliotropic and immunotropic virus–is present more often in patients with CFS than in healthy control and disease comparison subjects, yet it is not found in all patients at the time of testing. Moreover, HHV-6 has been associated with many of the neurological and immunological findings in patients with CFS.

Finally, CFS, multiple sclerosis and seizure disorders share some clinical and laboratory features and, like CFS, the latter two disorders also are being associated increasingly with active HHV-6 infection. Therefore, it is plausible that active infection with HHV-6 may trigger and perpetuate CFS in a subset of patients.

 

Source: Komaroff AL. Is human herpesvirus-6 a trigger for chronic fatigue syndrome? J Clin Virol. 2006 Dec;37 Suppl 1:S39-46. https://www.ncbi.nlm.nih.gov/pubmed/17276367

 

Lymphocyte subset differences in patients with chronic fatigue syndrome, multiple sclerosis and major depression

Abstract:

Chronic fatigue syndrome (CFS) is a heterogeneous disorder of unknown aetiology characterized by debilitating fatigue, along with other symptoms, for at least 6 months. Many studies demonstrate probable involvement of the central and autonomic nervous system, as well as a state of generalized immune activation and selective immune dysfunction in patients with CFS. The aim of this study was to compare the lymphocyte subsets of patients with chronic fatigue syndrome to those of patients with major depression and multiple sclerosis as well as those of healthy control subjects.

No differences were found in total numbers of T cells, B cells or natural killer (NK) cells. However, differences were found in T, B and NK cell subsets. Patients with major depression had significantly fewer resting T (CD3(+)/CD25(-)) cells than the other groups. Patients with major depression also had significantly more CD20(+)/CD5(+) B cells, a subset associated with the production of autoantibodies.

Compared to patients with multiple sclerosis, patients with CFS had greater numbers of CD16(+)/CD3(-) NK cells. Further study will be required to determine whether these alterations in lymphocyte subsets are directly involved in the pathophysiology of these disorders, or are secondary effects of the causal agent(s).

 

Source: Robertson MJ, Schacterle RS, Mackin GA, Wilson SN, Bloomingdale KL, Ritz J, Komaroff AL. Lymphocyte subset differences in patients with chronic fatigue syndrome, multiple sclerosis and major depression. Clin Exp Immunol. 2005 Aug;141(2):326-32. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1809442/ (Full article)

 

A comparison of pregnancies that occur before and after the onset of chronic fatigue syndrome

Abstract:

BACKGROUND: Many women with chronic fatigue syndrome (CFS) fear that pregnancy will worsen their condition, increase the risks of maternal complications of pregnancy, or threaten the health of their offspring. Little empirical evidence, however, has been published on this matter.

METHODS: A detailed questionnaire was administered to 86 women regarding 252 pregnancies that occurred before or after the onset of CFS and the outcomes of these pregnancies were observed.

RESULTS: During pregnancy, there was no change in CFS symptoms in 29 (41%), an improvement of symptoms in 21 (30%), and a worsening of symptoms in 20 (29%) of 70 subjects. After pregnancy, there was no change in CFS symptoms in 21 (30%), an improvement of symptoms in 14 (20%), and a worsening of symptoms in 35 (20%) of the subjects. The rates of many complications were similar in pregnancies occurring before the onset and in those occurring after the onset of CFS. There was a higher frequency of spontaneous abortions in the pregnancies occurring after, vs before, the onset of CFS (22 [30%] of 73 pregnancies after vs 13 [8%] of 171 before; P<.001), but no differences in the rates of other complications. Developmental delays or learning disabilities were reported more often in the offspring of women who became pregnant after, vs before, the onset of CFS (9 [21%] of 43 children vs 11 [8%] of 139 children; P =.01).

CONCLUSIONS: Pregnancy did not consistently worsen the symptoms of CFS. Most maternal and infant outcomes were not systematically worse in pregnancies occurring after the onset of CFS. The higher rates of spontaneous abortions and of developmental delays in offspring that we observed could be explained by maternal age or parity differences, and should be investigated by larger, prospective studies with control populations.

Comment in: Chronic fatigue syndrome, pregnancy, and Addison disease. [Arch Intern Med. 2004]

 

Source: Schacterle RS, Komaroff AL. A comparison of pregnancies that occur before and after the onset of chronic fatigue syndrome. Arch Intern Med. 2004 Feb 23;164(4):401-4. http://www.ncbi.nlm.nih.gov/pubmed/14980991

 

Prevalence of allergen-specific IgE among patients with chronic fatigue syndrome

Abstract:

The prevalence of atopy among patients having chronic fatigue syndrome (CFS) has been reported to be as high as 80% in published surveys of patients with this syndrome. However, many of the reports relied on self-assessment by patients for the presence of atopy or solely used total immunoglobulin E (IgE) levels to assess the likelihood of atopy.

To more critically assess the presence of atopy among patients with CFS, testing was done for total IgE and allergen-specific IgE using the Pharmacia CAP system including 20 common allergens: trees (birch/oak/ash), grass (rye/blue), weeds (common/giant ragweed), molds (Penicillium/Aspergillus/Alternaria), dust mites (Dermatophagoides pteronyssinus/Dermatophagoides farinae), animal dander (cat/dog), and foods (egg white/milk/wheat/corn/peanut/shrimp).

Testing of 50 patients having documented CFS indicated that 78% had total IgE < 100 IU/mL, among whom 26% had a positive test for allergen-specific IgE of class I or greater for one or more allergens. Among the 22% of CFS patients having a total IgE > 100 IU/mL, 73% had a positive test for allergen-specific IgE for one or more allergens. The most commonly positive allergens were dust mites (24-26%), whereas molds (0-6%) and foods (0-4%) were rarely positive. The overall frequency of positive results for the presence of allergen-specific IgE among CFS patients was 36%, not significantly different from the normal prevalence of these antibodies in the general population (20-35%). This assessment of the prevalence of allergen-specific IgE antibodies in patients with CFS fails to support a potential association between CFS and atopy.

 

Source: Kowal K, Schacterele RS, Schur PH, Komaroff AL, DuBuske LM. Prevalence of allergen-specific IgE among patients with chronic fatigue syndrome. Allergy Asthma Proc. 2002 Jan-Feb;23(1):35-9. http://www.ncbi.nlm.nih.gov/pubmed/11894732

 

Neuropsychological function in patients with chronic fatigue syndrome, multiple sclerosis, and depression

Abstract:

Patients with chronic fatigue syndrome (CFS), multiple sclerosis (MS), and major depression were compared with controls and with each other on a neuropsychological battery that included standard neuropsychological tests and a computerized set of tasks that spanned the same areas of ability.

A total of 101 participants were examined, including 29 participants with CFS, 24 with MS, 23 with major depressive disorder, and 25 healthy controls. There were significant differences among the groups in 3 out of 5 cognitive domains: memory, language, and spatial ability. Assessment of psychiatric symptoms indicated that all 3 patient groups had a higher prevalence of depression than the controls. A total measure of psychiatric symptomatology also differentiated the patients from the controls.

After covarying the cognitive test scores by a measure of depression, the patient groups continued to differ from controls primarily in the area of memory. The findings support the view that the cognitive deficits found in CFS cannot be attributed solely to the presence of depressive symptomatology in the patients.

 

Source: Daly E, Komaroff AL, Bloomingdale K, Wilson S, Albert MS. Neuropsychological function in patients with chronic fatigue syndrome, multiple sclerosis, and depression. Appl Neuropsychol. 2001;8(1):12-22. http://www.ncbi.nlm.nih.gov/pubmed/11388119

 

Salivary gland changes in chronic fatigue syndrome: a case-controlled preliminary histologic study

Abstract:

OBJECTIVE: The purpose of this preliminary study is to compare labial salivary gland changes of 11 patients with chronic fatigue syndrome with control subjects.

STUDY DESIGN: Changes in labial salivary glands were graded from 0 to 3+ for acinar dilatation, ductal dilatation, periductal fibrosis, plasmacytic infiltrate, lymphocytic infiltrate, mast cell infiltrate, and lymphocytic aggregates or foci.

RESULTS: Four of the 11 subjects had 2+ to 3+ changes in at least 4 of the 7 parameters examined. Only the presence of mast cells was statistically significant between the 2 groups. Two of these 4 patients had 1 lymphocytic focus per 4 mm(2) of tissue.

CONCLUSIONS: The salivary gland changes in patients with chronic fatigue syndrome show varying degrees of ductal and acinar dilatation, periductal fibrosis, lymphoplasmacytic infiltrates, and occasional lymphocytic foci, all suggestive of primary gland damage. The one parameter that showed statistical significance was the presence of mast cells (Fisher exact test, 0.0125).

 

Source: Woo SB, Schacterle RS, Komaroff AL, Gallagher GT. Salivary gland changes in chronic fatigue syndrome: a case-controlled preliminary histologic study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2000 Jul;90(1):82-7. http://www.ncbi.nlm.nih.gov/pubmed/10884641

 

Acute phase responses and cytokine secretion in chronic fatigue syndrome

Abstract:

This study addresses the hypothesis that clinical manifestations of chronic fatigue syndrome (CFS) are due in part to abnormal production of or sensitivity to cytokines such as interleukin-1beta (IL-1beta) and IL-6 under basal conditions or in response to a particular physical stress: 15 min of exercise consisting of stepping up and down on a platform adjusted to the height of the patella. The study involved 10 CFS patients and 11 age-, sex-, and activity-matched controls: of these, 6 patients and 4 controls were tested in both the follicular and the luteal phases of the menstrual cycle, and the remainder were tested in only one phase, for a total of 31 experimental sessions.

Prior to exercise, plasma concentrations of the acute phase reactant alpha2-macroglobulin were 29% higher in CFS patients (P < 0.008) compared to controls. Secretion of IL-6 was generally higher for CFS patients (approximately 38%), however, this difference was statistically significant only if all values over a 3-day period were analyzed by repeated-measures ANOVA (P = 0.035). IL-6 secretion correlated with plasma alpha2-macroglobulin in control subjects at rest (R = 0.767, P = 0.001).

Immediately after exercise, the CFS patients reported greater ratings of perceived exertion (P=0.027) compared to the healthy control subjects. Ratings of perceived exertion correlated with IL-1beta secretion by cells from healthy control subjects (R = 0.603, P = 0.022), but not from CFS patients, and IL-1beta secretion was not different between groups. Exercise induced a slight (< 12%) but significant (P = 0.006) increase in IL-6 secretion, but the responses of the CFS patients were not different than controls. Furthermore, no significant exercise-induced changes in body temperature or plasma alpha2-macroglobulin were observed.

These data indicate that under basal conditions, CFS is associated with increased IL-6 secretion which is manifested by chronically elevated plasma alpha2-macroglobulin concentrations. These modest differences suggest that cytokine dysregulation is not a singular or dominant factor in the pathogenesis of CFS.

 

Source: Cannon JG, Angel JB, Ball RW, Abad LW, Fagioli L, Komaroff AL. Acute phase responses and cytokine secretion in chronic fatigue syndrome. J Clin Immunol. 1999 Nov;19(6):414-21. http://www.ncbi.nlm.nih.gov/pubmed/10634215

 

Chronic fatigue syndrome: new insights and old ignorance

Abstract:

Chronic fatigue syndrome (CFS) is a condition characterized by impairment of neurocognitive functions and quality of sleep and of somatic symptoms such as recurrent sore throat, muscle aches, arthralgias, headache, and postexertional malaise. A majority of patients describe an infectious onset but the link between infections and CFS remains uncertain. Findings show an activation of the immune system, abberations in several hypothalamic-pituitary axes and involvement of other parts of the central nervous system. The origin is bound to be complex and it may well be that the solution will come together with a more generally altered view about mind-body dualism, and the concept of illness and disease.

 

Source: Evengård B, Schacterle RS, Komaroff AL. Chronic fatigue syndrome: new insights and old ignorance. J Intern Med. 1999 Nov;246(5):455-69. http://onlinelibrary.wiley.com/doi/10.1046/j.1365-2796.1999.00513.x/full (Full article)